Biopesticides

BIOPESTICIDES
Pest Management and Regulation

In memory of Neil Kift
Alastair Bailey
Kent Business School
University of Kent, Canterbury, UK
David Chandler
Warwick HRI Wellesbourne
University of Warwick, Coventry, UK
Wyn P. Grant
Department of Politics and International Studies
Justin Greaves
Department of Politics and International Studies
Gillian Prince
Warwick HRI Wellesbourne
Mark Tatchell
Department of Biological Sciences
BIOPESTICIDES
Pest Management and Regulation
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A catalogue record for this book is available from the British Library, London,
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Library of Congress Cataloging-in-Publication Data
Biopesticides : pest management and regulation / Alastair Bailey ... [et al.].
p. cm.
Includes bibliographical references and index.
ISBN 978-1-84593-559-7 (alk. paper)
1. Natural pesticides--Economic aspects. 2. Natural pesticidesGovernment
policy. 3. Agricultural pests--Biological control. I. Bailey, Alastair. II. Title.
SB951.145.N37B564 2011
338.1'62--dc22
2010020101
ISBN-13: 978 1 84593 559 7
Commissioning Editors: Stefanie Gehrig and Rachel Cutts
Production Editor: Tracy Head
Typeset by AMA DataSet, Preston, UK.
Printed and bound in the UK by CPI Antony Rowe, Chippenham.
1. Introduction 1
2. Pests of Crops 19
3. Pest Management with Biopesticides 71
4. The Economics of Making the Switch in Technologies 131
5. The Regulation of Biopesticides: an International Analysis 148
6. Policy Networks, Change and Innovation 177
7. Retail Governance 198
8. Conclusions 216
Index 223
v
Contents
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CAB International 2010. Biopesticides: Pest Management and Regulation
(A. Bailey et al.) 1
1
Introduction
Sustainable Farming and Pest Management: the Great Challenge of the
21st Century
There is no doubt that the need to improve agricultural productivity and
enhance its sustainability is one of the most signicant challenges facing
humanity. Across the world, farmers, growers and others in the food supply
chain need to be able to make a fair living from agriculture without damaging
the economic, social and environmental prospects of future generations. The
scale of the challenge cannot be overstated. Agriculture needs to meet the
food requirements of a rapidly expanding global population without placing
further pressure on the natural environment and the goods and services it
provides. It must adapt to global climate change and mitigate the effects of
greenhouse gas emissions, to which it is a major contributor. At some stage,
agricultural production which is heavily reliant on fossil fuels for planting,
husbandry, crop protection, harvesting and processing will have to switch to
a low-carbon economy. This will require a radical change in policies.
There is little sign of positive change in agricultural policy; indeed, food
production appears to be becoming less sustainable. The global demand for
food produced using high-carbon-footprint methods is increasing, driven
partly by the rising consumption of meat, while at the same time a succession
of poor harvests and expansion of the growth of crops for biofuels are con-
tributing to food price ination, food insecurity and increasing destruction of
natural habitats for farmland. These issues are highly complex, diverse and
interconnected. It can be difcult to separate short-term changes in food and
farming from long-term trends.
About 40% of the potential global crop yield is destroyed by pests (inverte-
brates, plant pathogens and weeds) before it is harvested. The diversity of
these organisms is set out in Chapter 2. Another 20% is destroyed postharvest.
Therefore, making improvements to pest management should be a very
2 Chapter 1
signicant way of increasing peoples access to food. Since the early 1960s,
pest management has been heavily reliant on the use of synthetic chemical
pesticides. In many respects these have been highly successful tools in
raising crop yields. However, as we detail later in this book, the use of
conventional chemical pesticides can have signicant negative effects for
people and the environment, and reliance on them as the sole means of
crop protection is not sustainable. Governments around the world are now
putting into place policies intended to reduce the use of conventional
chemical pesticides.
How can we achieve sustainable agriculture in general and sustainable
pest management in particular? The starting point is recognizing that agricul-
ture is multifunctional and provides public goods as they are dened in eco-
nomics (non-rivalrous and non-excludable): it produces both commodities
to be traded on the open market and non-commodities such as natural ser-
vices, culture and traditions, social fabric and landscape. When done well,
agriculture can help provide clean drinking water, provide stewardship for
biodiversity and maintain a healthy soil, as well as supplying crops for food,
clothing and other materials. The supply of safe and nutritious food and
drink is vital for human health, in terms of not only preventing chronic and
infectious disease, but also impacting positively on occupational and envir-
onmental health. Local foods and employment in their production provide
people with a sense of place, purpose and tradition. Pest management plays
a central role in all these processes.
However, the standard model of agricultural development has concen-
trated on increasing commodity production and has produced signicant
externalities. In the Global North, increases in the production, marketing and
sale of highly processed, energy-rich, nutrient-poor foods have contributed to
an obesity epidemic. Intensive agriculture has resulted in much loss of biodiver-
sity, degradation of soil and water, air pollution and serious pest management-
related problems in the form of resistance, resurgence and invasive species. In
overall terms, science and technology have been targeted at improving agri-
cultural productivity at the expense of the environment, social well-being and
good health. Things need to change before these problems result in further
damage and greater negative feedback into commodity production. We
require an effective, sustainable model for agriculture and food that takes full
account of the multifunctionality of the supply chain. Unfortunately,
as we explore in this book in relation to crop protection and biopesticides,
progress is being impeded by gaps in our scientic knowledge, by the way in
which agriculture is regulated and by the lack of a market for trading public
goods and externalities.
We believe that the natural and social sciences can make a signicant pos-
itive contribution to the problems facing agriculture in the 21st century. The
research on which this book is based formed part of the UK Rural Economy
and Land Use (RELU) programme funded by the UK research councils,
which facilitated collaborations between social and natural scientists over
contemporary challenges in the land-based economies. Our particular
concern is with making pest management more sustainable by integrating
Introduction 3
different control methods according to an ecologically based paradigm.
This is known as integrated pest management, or IPM.
Useful denitions of integrated pest management
Prokopy (2003) states that IPM is a decision-based process involving coordi-
nated use of multiple tactics for optimizing the control of all classes of pests
(insects, pathogens, weeds and vertebrates) in an ecologically and economically
sound manner. In this useful denition, IPM requires a range of techniques to
control a range of problems. Within this is an implicit reliance on regular crop
monitoring and the careful use of decision rules and thresholds for application
of different pest control tactics. Pest management should be done effectively
but at the same time minimizing impacts on other components of the agro-
ecosystem, thus taking into account the needs of producers, wider society and
the environment (Kogan, 1998). Other workers have placed more emphasis on
making use of ecology within the IPM control strategy. Here, Ullyett (1951)
makes the claim that IPM is the practice of applied ecology.
IPM does not rule out the use of chemical pesticides. However, in IPM
they are not treated as a blanket solution to crop protection but rather are
used selectively to reduce their external costs. IPM assumes a broad palette
of available control methods. Other IPM-compatible methods include bio-
logical, cultural and physical controls, host plant resistance and decision
support tools. These are explored further in Chapter 2. The long-term aim is
to enhance the functioning of self-regulating ecological systems that occur
on farms and which limit the development of pest populations, so that
human intervention is applied only when pest populations reach damag-
ing levels. The emphasis in the non-corrective components is that of pest
population maintenance.
Biopesticides and other alternatives to chemical pesticides
This book focuses on a particular set of tools for crop protection that have
actual or realized potential for farmers and growers. Widely referred to as
biopesticides (although this name paints something of a misleading picture,
which we discuss later), these are mass-produced, biologically based prod-
ucts for crop protection. They include microbial natural enemies and natural
products such as insecticides derived from plants or insect mating phero-
mones and are described in more detail in Chapter 3. However, to date the
sustainability benets that they offer are not being realized and there are
relatively few biopesticides on the market. We discuss some of the ecological
and environmental issues concerning biopesticides, the failures in markets
and the regulatory process and possible ways forward. We are concerned
primarily with the use of biopesticides for the management of plant patho-
gens, weeds and invertebrate pests of crops in industrialized countries,
particularly Europe and North America. Excellent research on biopesticides
4 Chapter 1
has been done in these countries, but a lot of pioneering work has also been
done in the Global South and we hope we have given this proper recognition
in the book.
Agricultural scientists have, for some time, been devoting effort towards
the development of alternatives to chemical pesticides in commercial crop
production. In a review of alternatives to conventional pest control in the
UK, the Advisory Committee on Pesticides (ACP, 2003) identied 14 generic
alternative approaches/technologies to conventional chemical pesticides, in
addition to monitoring and forecasting techniques, at various stages of
development for use in the UK. These approaches are included in Table 1.1.
As Table 1.1 shows, 11 of the generic approaches mentioned by the ACP
report are, to some degree, available for commercial use and over 50% of
them are assessed to hold reasonable promise as pest management tools.
Some of these have achieved high levels of adoption. Good examples include
the augmentative introductions of predators and parasitoids for biocontrol
of pests in protected crops. In addition, crop rotation, crop breeding and vari-
etal choice are currently used, at varying degrees of intensity, in nearly all
annual protected and unprotected crop systems in developed agriculture.
However, for the majority, adoption and impact (as measured by reductions
in use of conventional chemical pesticides) have been minimal. This lack of
commercial adoption could appear to run counter to various assertions by
researchers of the appropriateness and even the superiority of these new
techniques over the incumbent technology.
Table 1.1. Available range of pesticide alternative approaches. (Adapted from ACP, 2003.)
Technology Development Potential
Biological control
Insect pathogenic fungi Current Good
Insect pathogenic viruses Current ?
Microbial antagonists of plant pathogens Current ?
Arthropod predators and parasitoids Current Good
Management of naturally occurring predators of invertebrate pests Current Good
Microbial herbicides Potential ?
Biochemicals
Insect pheromones Current Good
Antifeedants/eating deterrents Potential ?
Plant extracts Near market Variable
Other methods
Commodity chemicals Current Moderate
Modied atmospheres Current Good
Physical and mechanical control Current Good
Crop breeding/varietal choice Current Good
Rotation Current Good
Introduction 5
The challenges associated with biopesticides are part of the wider set
of issues facing global agriculture that have been set out by the Interna-
tional Assessment of Agricultural Knowledge, Science and Technology for
Development (IAASTD). These include:
improving livelihoods and social welfare for people in the rural econo-
my, particularly for those living in marginalized areas;
sustaining natural resources, environmental and cultural services,
increasing productivity of food, bre and biofuels, minimizing the nega-
tive effects of production and other farm activities; and
nding effective ways to manage the generation of knowledge and the
spread of information.
As we shall explore in this book, the complex interplay between techni-
cal issues of pest management, environmental protection, economics, social
concerns, regulation and politics that grew out of the chemical pesticide era
has had unintended consequences for biopesticides. In the European Union
(EU), for example, the regulatory process that resulted rst in the large-scale
commercialization and adoption of synthetic organic chemical pesticides in
the latter half of the 20th century (followed currently by an equally dramatic
withdrawal of products from the market) is now acting as a barrier to the
commercialization of biologically based products. The great pity is that
these biological products can be used in integrated programmes to help
reduce the external costs of chemical pesticides while retaining their benets
as efcacious ways of controlling pests. Moreover, the benecial properties
of biologically based agents such as high specicity (and hence low envi-
ronmental impact), ease of isolation, potential for self-sustaining control and
suitability for cottage production can be a deterrent to a crop protection
industry that has developed along a chemical-based model to focus on
high-return, broad-spectrum products and preservation of intellectual
property rights.
The focus of this book is on biopesticides and their regulation in com-
parison to that of chemical pesticides. Some other components of IPM systems
are also subject to regulations which may differ from country to country. In
particular, the introduction and release of exotic natural enemies for biological
control are frequently subject to environmental legislation designed to pre-
vent the introduction of damaging organisms into new environments. This
subject is not discussed further here.
The Regulatory State
A central theme of this book is the existence of regulatory barriers to the
wider use of biopesticides which could contribute to IPM strategies. An alter-
native paradigm to regulatory failure is that of market failure, which, put at
its simplest, means that some products are insufciently technologically
advanced or reliable in their effects or face a lack of market demand to make
them commercially viable given the cost of their research, development and
6 Chapter 1
registration. There is no doubt that this is a real challenge for the biopesticides
industry, as although there are a few broad-spectrum products, most of those
developed and available on the market tend to be niche products with spe-
cic applications to particular crops that are not produced on an extensive
scale. They are often referred to as minor crops in contrast to broad-acre
crops grown on a large scale, although this term is somewhat misleading as
a contribution to the policy debate as it covers signicant fruit and vegetable
crops such as apples and brassicas.
We do not want to underplay the signicance of these economic consid-
erations and Chapter 4 is written from an economics perspective. There is no
doubt that the industry has from time to time failed to deliver what it prom-
ised and this has been damaging to its reputation. A system of registration is
needed to discourage snake oil products that cause reputational damage
and, indeed, there is a case for more rigorous regulation of so-called grey
market products, which do not make explicit pest control claims and are
therefore generally outside the scope of the regulatory system, but may be
used as a means of pest control.
A central initial hypothesis in our project was the notion of regulatory
failure. It should be emphasized that this did not mean that regulatory
agencies or individual regulators had been incompetent or had failed to
apply regulatory rules properly. Instead it refers to the fact that the regula-
tory system had been designed for synthetic products and had difculty in
responding to the different characteristics and properties of biological
products. Product developers, typically small rms, were discouraged
from applying for registration at all or found the process unduly lengthy,
onerous and costly. As will be discussed in the book, regulatory agencies,
especially the Pesticides Safety Directorate (PSD) (now the Chemicals Regu-
lation Directorate, CRD) in Britain, have attempted to respond systematically
to these challenges and to make the regulatory system more responsive to
biocontrol products.
Our general approach is framed within a widely used paradigm in political
science known as the regulatory state, but our more specic analysis uses
regulatory innovation, discussed below. The regulatory state is an ideal
typical model, i.e. it does not apply to all aspects of political reality, but is
used to capture a movement from the early Keynesian welfare state (substan-
tial elements of which remain) to a new emphasis on regulation as a mode of
governance. Issues raised by the regulatory state debate are relevant to our
consideration of pesticides regulation. Pesticides are amongst the most
strictly regulated of all chemicals (House of Commons, 2005: 6). Models of
the regulatory state, therefore, provide a framework to our discussion.
Morans work (2000, 2002, 2003, 2005) is of particular importance in terms of
developing a model of its essential characteristics. New executive agencies
are contracted to deliver policy; a newly privatized sector is subject to a net-
work of specialized regulatory agencies; and government has turned to the
specialized regulatory agencies to control large areas of economic and social
life (Moran, 2005: 156).
Introduction 7
The regulatory state model has been primarily used in relation to the
developed world and Phillips (2006) has justiably criticized its lack of
applicability to the Global South. However, for our particular purposes,
namely a geographical focus on Europe and the USA (together with Austra-
lia and Canada), the model has explanatory value. Its utility may be limited
to the developed world but it can still have utility in comparing modes of
governance within a particular state. On that particular point our perspec-
tive diverges from the argument made by Phillips that the regulatory state
research agenda offers little purchase on the elements of different varieties
of capitalist organisation, policy orientation and institutional design that
exist within national political economies (Phillips, 2006: 22).
In his initial work on the regulatory state, Moran took a relatively benev-
olent view of the regulatory stage, which in popular discourse might be seen
to refer to what is sometimes called the nanny state. He saw it as a great
improvement on earlier state forms. As he puts it:
As for the old world of command, good riddance to it: good riddance to the men
in Whitehall who know best The world of command infantilised us all never
let us grow up from subjects to citizens
(Moran, 2000: 12)
Indeed, it is possible to read Morans work as an interpretation of a progres-
sive, yet imperfect and complete, transition towards modernity. In ideal typ-
ical terms, the command or Keynesian welfare state is displaced, partly
because of the exhaustion of this earlier paradigm, by the regulatory state.
This involves more indirect forms of state control which may, of course, rein-
vigorate rather than reduce state power (Wolfe, 1999). Progressive features of
the new dispensation include the displacement of club government and the
replacement of self-regulation which was seen to fail both in terms of eco-
nomic efciency and public accountability. In the case of pesticides, for
example, voluntary regulation under the Pesticides Safety Precaution Scheme
in the UK was displaced by statutory regulation in 1986.
Moran has become more impressed by the regulatory states authoritar-
ian potential (M. Moran, personal communication). He suggests we look to
the authoritarian strand in regulation; his recent textbook argues that The
British Regulatory State (Moran, 2003) recognized this strand and paints the
British regulatory state in a threatening and interventionist light (Moran,
2005: 530). Moran now accepts that this remark does not quite gloss it accu-
rately (Moran, 2005: 530). Nevertheless, he explains how his 2003 work
argued that the regulatory state had a Janus face: a democratizing quality,
because it enforces more transparency on elites, but also an authoritarian
quality, because it also centralizes and controls. To complicate matters fur-
ther, the latter feature encourages it in the direction of failures and catastro-
phes, which, in turn, subverts its control capabilities (Moran, 2005: 530). He
argues that the British regulatory state, far from being smart, is, therefore,
often remarkably stupid. He adds, however, that it succeeded a governing
system that was even more stupid (Moran, 2003: 26).
8 Chapter 1
One recurrent theme in the literature on regulation is the danger of
regulatory capture. The new regulatory state sets up relationships between
regulator and regulated that are close, involving daily contact. There is an
obvious danger, therefore:
that the regulator will grow so like the regulated that the two will simply share
common interests and a common view of the world, and the independence so
vital to the new regulatory agencies will be undermined.
(Moran, 2005: 159)
This is a strong theoretical tradition in the USA that reects a system of
government in which historically there have been iron triangle relationships
between congressional committees, regulatory agencies and the regulated
who are often substantial donors to the re-election campaigns of the mem-
bers of the congressional committees. There certainly can be problems of
asymmetric information between regulators and the regulated and there is
some evidence to suggest this has been a problem in utility regulators in the
UK (Willman et al., 1999; Hritier, 2005). We have found little evidence of it
within PSD. The organization has built up its own in-house scientic exper-
tise so that it can make independent and authoritative judgements on pesti-
cide approvals. It seems to be an agency that is relatively insulated from
external opinion and, as we discuss later, a combination of exogenous inter-
vention and internal responsiveness to it was necessary to create a regime
more amenable to biopesticide registration.
Regulatory Innovation
The reinventing government movement in the 1990s was a response, on the
one hand, to the excessive faith in big government that had predominated
from the New Deal of the 1930s to the 1970s and the over-reaction to it in
terms of the belief propagated by Ronald Reagan and Margaret Thatcher in
the 1980s that government was part of the problem not part of the solution.
It was felt that what was needed was a form of government that was both
leaner and smarter and more targeted and focused in its use of limited
resources. The notion of innovation is a key part of the reinventing govern-
ment debate (Osborne and Gaebler, 1993) and has a key role in debates on
regulatory reform (e.g. OECD, 1995; European Commission, 2002). This links
to notions of governance that emphasized that government would steer rather
than row (Rhodes, 2000) and also the desire for smarter, more effective regu-
lation. Public agencies were told that innovation should become one of their
core activities (Cabinet Ofce, 2003). Innovation studies in political science
date back to the 1960s but there has been a revival of interest in studying
specic examples of policy innovation in the delivery of public services by
governmental and voluntary organizations (e.g. Doig, 1997; Light, 1998;
Borins, 2000). There is now also a web-based journal devoted to the topic
(http://www.innovation.cc). The Better Regulation Executive (BRE) operates
within the Department for Business, Innovation and Skills (BIS) and leads
Introduction 9
the regulatory reform agenda across government. Such structures could be
expected to be re-branded by any change of government.
Regulators are typically risk averse. The consequences of making a mis-
take are serious, not least where public safety and environmental protection
are involved. This does not create an encouraging environment for regulatory
innovation: indeed, the term is almost a contradiction. This book will argue
that regulatory innovation has also successfully occurred within CRD (see
Chapter 6). At a basic level regulatory innovation is often needed to offset the
problems of regulatory failure which we referred to earlier. More specically,
in terms of the regulatory state model, the priority given to regulation sets up
expectations of innovation and responsiveness to societal demands for change
which can be hard to meet in practice. There is a fundamental tension, more-
over, between expectations that regulators will be consistent, predictable and
impartial, and yet also innovative.
One image is that regulatory innovation is a matter of rening the
technologies of regulation: again, the search for better tools of governance,
the development of smart regulation (e.g. Osborne and Gaebler, 1993; Spar-
row, 2000). For others, regulatory innovation is seen as necessary in order to
improve strategies for managing risk, as seen, for instance, in the rise of new
public risk management (e.g. Cabinet Ofce, 2000; Sparrow, 2000). In this
image, regulatory innovation is the pursuit of state legitimacy in the risk
society (Beck, 1992). At a more theoretical level, regulatory innovation is an
adaptive response by a system or organization to its environment. The prob-
lem with such images is that they have conicting normative and cognitive
implications (Black, 2005a: 4). Black, therefore, offers a normative neutral
denition which we also propose to use:
Regulatory Innovation is understood to be the use of new solutions to
address old problems, or new solutions to address new (or newly constructed)
problems, but not old solutions to address old problems.
(Black, 2005a: 4)
This is illuminated by Halls (1993) typology of policy change. First-order
changes are changes to the levels or settings of basic policy instruments (not
considered here as innovations). Second-order policy changes involve
changes in technique, process or instrument, but not in the overall goals of
policy or understanding on which it is based. Third-order changes involve
changes in the goals of policy and understandings on which the policy is
based, along with second- and rst-order changes. Third-order changes are
paradigm shifts, changes in the terms of a policy discourse: the understand-
ings on which it is based and the goals pursued (Kuhn, 1962).
The dominant assumption in the literature is that innovation is a good
thing. In Mohrs inuential denition, innovation is seen as the success-
ful introduction into an applied situation of means or ends that are new to
that situation (Mohr, 1969: 112). Innovation was dened by the Cabinet
Ofce, moreover, as new ideas that work and more precisely as the cre-
ation and implementation of new processes, products, services and methods
of delivery which result in signicant improvements in outcomes, efciency,
10 Chapter 1
effectiveness or quality (Cabinet Ofce, 2003: para 2.1). In contrast, Moran
draws attention to some of the errors that may result from too great an emphasis
on innovation (Moran, 2003). Clearly, innovation need not always be success-
ful. Indeed, being in a constant state of innovation can be counterproductive:
initiatives may not be given the time to be properly implemented; costs may be
imposed through the need to change systems and processes; and no policy is
around for long enough for its success or failure to be properly accessed
(Black, 2005a: 14).
So how and why does regulatory innovation occur? Black (2005b) argues
that the different sets of explanations tend to occupy different worlds or
ways of thinking. The outline of each world is not intended to be a complete
account of the theories of innovation that may potentially exist or be grouped
within those worlds, in particular because the literature which specically
refers to innovation is itself quite narrow and does not necessarily seek to
engage with wider questions relating to policy change. The worlds identied
are vefold: the world of the individual, the organization, the state, the global
polity and the innovation. In the world of the individual the individual is
both the site and agent of innovation. The organizational world concentrates
on innovations within organizations, traditionally prot-making organiza-
tions but increasingly non-prot public and private sector organizations. The
state worlds site of analysis is the public policy-making processes of the
state. The global polity looks at policy making by global polity bodies and
networks. Finally, the world of the innovation revolves around the idea of
innovation itself. We look at these worlds in more detail in Chapter 6. In our
particular case, however, a consideration of the contextual and exogenous
and endogenous drivers (while overlapping with Blacks analysis) will be
shown to provide a better framework. Furthermore, we will outline a more
detailed model to account for regulatory innovation in regulatory agencies.
The Interdisciplinary Challenge
The policy challenges faced in todays world often require disciplines that
had not collaborated very much in the past to work together to undertake
analysis and develop policy solutions. In particular, there is an imperative
for economics and political science to collaborate not just with other social
sciences, where there is a signicant amount of relevant experience, but also
with the natural sciences, a territory that is less well mapped and explored.
Such an imperative is not just policy related, but also academically driven.
In our work on biopesticides we have sought to move beyond multidis-
ciplinarity in the sense of research that requires scholars to be aware of
salient contributions from other disciplines and to draw on them in useful
and limited ways (Warleigh-Lack and Cini, 2009: 8). We have sought to move
towards interdisciplinarity involving a much more sustained process of dia-
logue, together with joint problem-denition, and methodology, most prob-
ably devised by a team of scholars from the salient disciplines and areas
(Warleigh-Lack and Cini, 2009: 89). Probably the greatest challenge is to
Introduction 11
develop a common methodology, and we would not claim to have achieved
that. We have not aspired to or achieved transdisciplinarity by adding an
overarching common meta-theoretical perspective to the common denition
of the problem and methods (Warleigh-Lack and Cini, 2009: 9).
It is possible that working with cognate disciplines in the social sciences
may in some cases be more difcult than working with natural scientists, in
part because there may be contested boundaries and fears about capture. The
closer the two disciplines, the greater this fear may be. Because the gap is
wider with natural science, it may be more challenging to bridge, but there
may be fewer fears about leaping the chasm and the rewards of doing so may
be greater.
The natural sciences and the social sciences
There are some evident differences between the natural sciences and the
social sciences. The comparison here is limited to biological science and
political science. Different issues may arise in relation to, say, physics, where
it is at least arguable that a great deal of meta-theoretical speculation takes
place that is not experimentally veriable (Smolin, 2005, but his views are
contested).
In this discussion the focus is on four differences which may not always
be as substantial as they initially appear to be:
1. The Oedipus effect.
2. The greater ease of experimentation within the natural sciences.
3. The use of highly sophisticated systems to understand problems.
4. The possibility of generalizing from an individual organism or species
without committing an individualistic fallacy.
The Oedipus effect
Science is about explanation, but one key test of its worth is its ability to
make sustainable and veriable predictions. If one predicts that a material
will expand at a given rate when subjected to heat, that hypothesis can be
tested and veried and it can inuence the way in which the material is used
in a variety of situations. In social science, a prediction may affect or even
change the outcome. For example, supposing a credible source predicts that
Party A is going to win a substantial majority over Party B in an election and
that the gap cannot be closed. Supporters of Party B could be discouraged
from voting because they think there is little point, or supporters of Party A
could decide that the election is already won and they do not need to vote. In
either case (or a combination of both of them) the outcome is affected, albeit
in somewhat complex or unpredictable ways.
Experimentation
An important difference between biological science and political science
would appear to be the ease with which controlled experiments can be
12 Chapter 1
undertaken in biology. Classically, what makes an experiment is [the]
distinction between the control situation and the experimental situation. In
the experimental situation, the variable of interest is changed to some value
at which we hope to demonstrate causality (Cohen and Medley, 2005: 44).
Much of experimental biology in recent decades has moved away from
the interpretation of associations towards the understanding of causal rela-
tionships in dynamic systems. This has been enhanced by the huge advances
in molecular biology and genetics. Biological science often relies on simpli-
ed systems for study. These often consist of small numbers of experimental
units maintained under controlled conditions. This does raise an issue
whether something that can be observed in the highly controlled conditions
of the laboratory can be replicated elsewhere. Forms of complexity may be
largely hidden in idealized laboratory settings. Csete and Doyle (2002)
explain the concept of spiralling complexity in terms of the need for com-
plex regulatory networks to ensure robustness. They use the example of a
Lego model made mobile, then motorized and nally equipped to avoid
collision in a maze of obstacles, this third step increasing complexity by
orders of magnitude. This is consistent with the claim that biological com-
plexity too is dominated not by minimal function, but by the protocols and
regulatory feedback loops that provide robustness and evolvability (Csete
and Doyle, 2002: 1666). Much of this complexity is not immediately apparent
to the observer. Nevertheless, in order to understand complex phenomena,
it is often necessary to take a reductionist/simplied approach. One does
not want to replicate complexity in any scientic undertaking, but to offer a
parsimonious model of it.
One should not push the notion that science is dominated by manipulative
experiments too far. While a manipulative experiment may be the ideal, the
practical difculties mean that they are often impossible, or restricted to small
sample sizes or unrealistic simplied circumstances. Plentiful observational
data gathered in natural circumstances in the eld are often preferable. In
ecology and epidemiology much work is based on the statistical analysis of
observational data.
The use of highly sophisticated systems
The study of elections has becoming increasingly sophisticated in its use
of quantitative techniques, taking advantage of advances in econometrics.
Nevertheless, this cannot be compared with the advances made in systems
biology. This approach in cell and molecular studies uses mathematics and
sophisticated computing to understand highly complex systems, based on
integrating large data sets collected from many experiments done at the indi-
vidual level. What it makes possible is an understanding of the structure and
dynamics of cellular and organism function, rather than the characteristics of
the isolated parts of a cell or organism. In particular, progress in genome
sequencing and high-throughput measurements, enables us to collect com-
prehensive data sets on system performance and gain information on the
underlying molecules (Kitano, 2002: 1662). It is still a work in progress and
requires improvements in software infrastructure and high throughput and
Introduction 13
accurate measurements, goals that are perhaps beyond the scope of current
experimental practices (Kitano, 2002: 1663).
Systems biology places considerable emphasis on both system structures
and system dynamics. However, In reality, analysis of dynamics and structure
on the basis of network dynamics are overlapping processes (Kitano, 2002:
1662). In political science an analogy can be found in the substantial body of
work on policy networks and communities which we use extensively in this
book. This analysis attempts to dene the boundaries of such networks, how
they interact (including subsystems where relevant) and how this leads to
particular outputs such as legislation or institutional design. However, in
political science, this is very much a meso level rather than a systems level
analysis. It does not have the transformative impact of systems biology
where there is a transition from the molecular level to the system level that
promises to revolutionize our understanding of complex biological regula-
tory systems (Kitano, 2002: 1662). Can political science be as ambitious as
biological science? Does it have the tools to match ambition with appropriate
and rigorous analytical techniques?
Robustness is an essential property of biological systems (Kitano, 2002:
1663). This claim has a relevance to political systems, particularly in terms
of two of the three properties exhibited by robust systems. The rst of these
is adaptation, which denotes the ability to cope with environmental
changes (Kitano, 2002: 1663). Political systems have to be able to adapt to
changes in their wider environment if they are to survive and prosper. For
example, domestic political systems need to be able to cope with the chal-
lenges of globalization, such as by grouping together in new ecologies at a
regional level.
An important property of a political system could also be graceful
degradation, which reects the characteristic slow degradation of a sys-
tems function after damage, rather than catastrophic failure (Kitano,
2002: 1663). Subjected to an external shock, a robust political system should
not collapse completely. A slow degradation allows new structures and
functions to replace it successfully.
Parameter insensitivity as a property of robust systems poses more
challenges for analysis. This is because the boundaries of political systems
are relatively contested and often very permeable. The boundaries are shift-
ing, not just geographically, but in terms of social and economic formations;
indeed, this permeability increases under conditions of globalization. This is
the case both geographically and in terms of who is allowed to constitute a
citizen of the polity, an issue that becomes particularly potent at the interface
of migration and globalization. This observation raises the broader issue
that the very terms we use in political science are essentially contested
because they have a substantial normative component.
The individualistic fallacy
Both the biosciences and political science face the risk of committing the
ecological fallacy and the individualistic fallacy. The ecological fallacy entails
inferring without investigation that relationships among collectivities are
14 Chapter 1
the same as those for individuals. Only under very specic circumstances
are such inferences from ecological data valid; otherwise, the observer has
committed the ecological fallacy (Alker, 1965: 102). In other words, the eco-
logical fallacy involves the identication of statistical relationships at the
aggregate level that do not accurately reect the corresponding relation-
ship at the individual data level. Anyone who draws a conclusion about indi-
viduals based on evidence about groups commits what is called the ecological
fallacy (McIntyre, 2005: 42).
It is likewise a logical error to draw conclusions about groups based on
data gathered with the individual as the unit of analysis (McIntyre, 2005: 43).
This is known as the individualistic fallacy or sometimes as the reductionist
fallacy. The individualistic fallacy is just the opposite of the ecological fallacy
social scientists are likely to try to generalize from individual behaviour to
aggregative relationships (Alker, 1965: 103). In biology, an individualistic fal-
lacy can be committed in two ways: (i) by making inference about a group
from data collected on an individual of the same species; and (ii) by making
inference about one species from data collected on another species.
How is it possible for bioscientists to generalize on the basis of observations
on an individual organism or species without committing an individualistic
fallacy? One approach that is used is the use of model systems/organisms.
These are chosen because they are easy to work with, but they still have rel-
evance to less tractable world systems. Examples of model organisms include
the lab rat and fruit y. In freshwater biology, the crustacean Daphnia magna
Straus is an excellent model organism for stage-structured demographic
analysis. Under favourable conditions, females reproduce parthenogeneti-
cally, producing large broods of female offspring at intervals of 34 days
(Carslake et al., 2009: 1077). There is also the model plant, a widely used
example being Arabidopsis thaliana, a non-commercial member of the mustard
family. Instead of studying many different plants, one can study this particu-
lar plant that has a number of helpful characteristics for research purposes
(although the similarity of Arabidopsis to other owering plants may be a little
simplistic and there have been real difculties in transferring the ndings
from Arabidopsis even to the closely related brassica crops). Nevertheless, it
has real advantages:
it is easy and inexpensive to grow;
it produces many seeds;
it responds to stress and disease in the same way as most crop plants;
it has a small genome (genetic complement) facilitating genetic analysis.
Use of the model plant is possible because all owering plants are closely
related. Complete sequencing of the genes of a single, representative plant
will yield knowledge about all higher plants. Biological material that is
genetically identical can be generated through carefully designed crossing
and backcrossing programmes that produce isogenic lines. This material is
then used to study causal relationships.
Because only one organism/system is studied by many people, resources
are pooled and knowledge is acquired rapidly. The degree to which a scientic
Introduction 15
observation made on the model organism applies to a different species
(i.e. the probability of committing an individualistic fallacy) depends on the
relationship between the two species and the scientic hypothesis that is
being tested. One of the attractive properties of model organisms/systems is
that they provide a baseline or anchor point. You can test a hypothesis in the
tractable, well-studied model organism, and then see if it applies to other
organisms. Human behaviour is much more diverse. We cannot identify a
model citizen from whom we generalize. (Interestingly, the media does
sometimes seek to identify the median voter: in the UK, Worcester woman,
a woman in her 30s living in the city of Worcester, with children, in part-time
work and driving a Ford Mondeo.)
What is not being argued is that biological science is superior to political
science in terms of its predictive and explanatory power simply because of its
subject matter and the research techniques available to it. Although biological
systems are in one sense less complex than politics and so are easier to explain
and predict, at a fundamental level the question of superiority is an unhelpful
distraction, particularly when one is trying to foster collaboration. What is
needed in both biological and political science, and especially in joint pro-
jects between them, is to develop the best methodologies available in order
to understand the system under study in the most complete yet also parsi-
monious way. In any eld of study, the most complex and possibly intracta-
ble systems are those that cannot be described mathematically, but which
have to be described and analysed using words.
Complementarities and differences between the natural and social sciences
The Oedipus effect captures a real difference between the natural and social
sciences in terms of the fact that the social sciences are dealing with human
agents with a capacity to learn and reect, who may change their behaviour
in response to predictions. The use of experimental methods is growing in
political science, but it is still at the periphery of the discipline compared
with its central place in many of the natural sciences. For many of the advo-
cates of interdisciplinarity, the appropriate focus of interdisciplinary study
is on specic complex systems and their behaviour (Newell, 2001: 2). For
political scientists who favour a systems level approach, interdisciplinarity
could offer a welcome refuge. The discussion of the individualistic fallacy
found that biological scientists did not necessarily have more reliable ways
of overcoming it than political scientists.
Conclusions
The food chain faces the challenge of producing enough food sustainably
against the background of a growing world population and increased per capita
demand for food, and for food that demands more resources to produce, as
emerging countries such as China and India become more prosperous.
We face simultaneously a food security challenge and a sustainable production
challenge. An important part of that sustainability challenge is ensuring a
16 Chapter 1
response to climate change mitigation and adaptation, a theme to which
we return in the conclusions (Chapter 8). In emphasizing climate change we
should not forget that other environmental challenges remain such as pollution
control and maintaining biodiversity.
IPM offers a strategy for providing crop protection while tackling envi-
ronmental challenges and consumer concerns. Biocontrol products, of which
biopesticides are a subset, form an important component of an IPM approach.
They have primarily been niche products mainly deployed on high-value
crops grown on small areas rather than broad-acre crops. In the case of broad-
acre crops, a range of agrochemical solutions is available. For many so-called
minor crops, including widely eaten eld vegetables, the number of crop pro-
tection solutions is diminishing rapidly and the availability of suitable biocon-
trol products is an urgent need. The development of new products continues
and sales are growing signicantly, with big companies starting to buy back
into the sector for the rst time since the 1980s. Among the drivers here are the
new EU legislation which we discuss in Chapter 5, the availability of broader-
spectrum products, the illegal synthetics scandal in Spain and the concerns
of consumers about synthetics refracted through retailers (see Chapter 7).
The sector has faced market failure problems in terms of whether the size
of the market for some products is sufciently large to recoup research and devel-
opment costs. Some products have not lived up to the marketing claims made
about them. However, there has also been a regulatory failure problem and this
is a particular focus in this book. This requires the design of appropriate policy
instruments which may range from broad-gauge agri-environmental schemes
(discussed in Chapter 4) to measures designed to promote the regulation of
biocontrol agents (see Chapter 5). It also requires thinking about the scope of
regulation in terms of grey market products which may undercut products
that have incurred the costs of registration. Many challenges remain for IPM
and biocontrol, but there is also an unparalleled window of opportunity
within the EU.
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2
Pests of Crops
A pest is any organism that reduces the availability, quality or value of a human
resource including our crop plants (Flint and van den Bosch, 1981). Crop pest
organisms include plant pathogens (fungi, oomycetes, bacteria, viruses, nema-
todes and some other taxa), weeds, invertebrates (primarily insects, mites and
molluscs) and a small number of vertebrate species. Each species and variety
of crop plant is exploited by a community of pest species, the composition of
which varies according to country and region. Rice, for example, is susceptible
to more than 20 major insect pests and plant pathogens (Bonman et al., 1992),
while oilseed brassica crops are attacked by about 50 major insect pests and
plant pathogens (Lamb, 1989; Leino, 2007). Overall, there are estimated to be
about 67,000 different pest species and they are a signicant constraint on
agricultural production, responsible for around 40% loss of potential global
crop yields (Oerke et al., 1994; Pimentel, 1997). Of this, 15% is caused by
arthropods, 1213% by plant pathogens and 1213% by weeds. A further 20%
loss in yield is estimated to occur after crops have been harvested and placed
into storage. These losses occur despite the very considerable efforts made at
pest control and they suggest that improvements in pest management are
likely to be a signicant route forward for improving yields and access to
food in the years ahead (Oerke and Dehne, 2004). About 90% of the worlds
food energy intake comes from only 15 species of crop plant, and 66% from
just three species: rice, maize and wheat (FAO, 2010). If our crop protection
systems for any one of these crops were to fail, then the consequences could
be severe. The loss potential of pests worldwide has been estimated to vary
from less than 50% on barley to more than 80% on sugarbeet and cotton
(Oerke and Dehne, 2004). Famines and starvation due solely to pests are mer-
cifully rare, but they have occurred in the past. Probably the best-known
example, the Irish potato famine of 1846, caused mass starvation and the
creation of the Irish Diaspora. More commonly, the effects of crop pests com-
bine with other constraints on crop production (weather, soil fertility, labour,
20 Chapter 2
farmer access to knowledge, market prices and government policies on
agriculture) to cause food insecurity (Speranza et al., 2008). As the pressure
on our food supply increases over the next decades, then crop pests are
bound to become more of a concern for global food supplies.
In nature, consumption of plants is a fundamental component of virtually
every terrestrial food web, and hence we should not be surprised that there
are plenty of organisms out there that are able to feed on our crops. But
what is often not fully appreciated is that the creation and management of
agricultural land cause the conditions under which pests ourish. Growing
crops in monoculture provides a concentrated food resource that allows phy-
tophagous pest populations to achieve far higher densities than in natural
environments, while clearing the ground by ploughing creates ideal condi-
tions for the growth of weeds. All plant life stages and all portions of the
plant are vulnerable to pests. Reduction in yield or shortfall in crop quality
occurs because of consumption of plant nutrients by pathogenic microorgan-
isms and herbivorous animals or by competition for resources with agricul-
tural weeds. The different mechanisms by which pests affect the crop have
evolved as a result of natural selection and are driven by competitive interac-
tions between the pest and the plant, between different pest species (e.g. for
food and space), with other members of the ecological community (e.g. with
predators or disease) and the abiotic environment. Crops are attacked by
both generalists, which affect many plant species, and specialists, which feed
on a narrow spectrum of plant species and show specic adaptations to plant
defences or certain habitats. Pest damage can be direct (i.e. the plant is eaten
by a pest) or it can be indirect, in which case there is a reduction in yield or
quality due to competition for resources (most weeds reduce crop yields in this
way) or because the pest acts as a vector of a plant disease. In general, seed-
lings and young plants are more vulnerable than mature plants. Direct dam-
age is most serious when it occurs to the harvestable part of the plant. Plants
can also exhibit compensatory growth in response to pest attack and hence a
crop may be able to tolerate partial loss of leaves without a reduction in yield.
Biology of the Main Groups of Agricultural Pests
Describing the biology, ecology, behaviour and function of the main agricul-
tural pests in detail is beyond the scope of this book, and indeed many books
have been devoted to this task. For more information we recommend Hill
(1994), Naylor (2002) and Agrios (2005). Here we provide a brief introduction to
pest biology as a foundation for later sections in the book on biopesticides and
sustainable agriculture.
Invertebrates
Insects
Insects are among the most abundant and diverse groups of animals on the
planet. There are estimated to be 610 million extant species and they make
Pests of Crops 21
up about half of all species of higher organisms (Gullan and Cranston, 1994).
There are about 30 insect orders, of which ten orders and over 50 families are
considered to contain major pests of crops (Hill, 1994, 1997). These include
the Orthoptera (pests in this order include locusts, grasshoppers and crick-
ets), Hemiptera (sap-feeding insects that include a wide variety of pests such
as aphids, whitey, plant hoppers, leaf hoppers, scales and capsid bugs),
Thysanoptera (thrips), Coleoptera (beetles and weevils), Lepidoptera (but-
teries and moths), Diptera (root and stem ies) and Hymenoptera (sawies).
A list of some of the most important members of these taxonomic groups is
given in Table 2.1. Most insect species have evolved specialized mouthparts
for biting, sucking or chewing, and immature and adult stages of agricultural
pests use these to attack different parts of the host plant. The hard, waxy
exoskeleton of insects means that many species are resistant to desiccation
and can survive in harsh conditions. Some of the most important insect pests
cause indirect damage by vectoring plant pathogens. Aphids (Aphididae),
leaf hoppers (Cicadelidae) and plant hoppers (Delphacidae) are all vectors of
plant viruses, while some beetle (Coleoptera) pests are vectors of fungal
Table 2.1. Insect pests of agricultural crops. (From Hill, 1994, 1997.)
Order Description
Diptera Ecologically diverse, the order is best known for containing species of medical
and veterinary importance, such as mosquitoes and blackies. However, there
are also species that damage plants. These include the Psilidae (such as the
carrot y Psila rosae) and the Anthomyiidae (such as the cabbage root y Delia
radicum). Some species with carnivorous larvae (e.g. hoveries) are used for
biological control of crop pest insects.
Lepidoptera The larvae of most species in this order feed on plants, and hence it contains
many crop pest species. Some of the most important are members of the
following families: Tortricidae, the larvae of which feed by boring into fruit,
stems, buds or leaves; Pieridae, containing larval pests of legumes and
crucifers; Noctuidae, the larvae feed on all above-ground parts of the plant.
Noctuid pests are often referred to as worms and they include cutworms
(living in soil or in leaf litter and cutting stems of young plants), fruitworms,
rootworms, bollworms (which feed on cotton), as well as species that burrow
into stems (stem borers) and armyworms (foliage-feeding caterpillar species
that occasionally form massive outbreak populations that move as a group to
new areas of vegetation having exhausted their food supply).
Hymenoptera This order contains many species of benecial insects, including parasitoids of
crop-feeding insect pests, which are used as biological control agents, and
pollinators of crops, for example the western honeybee Apis mellifera. The
larvae of some hymenopteran species in the suborder Symphyta (sawies) are
plant feeders, consuming foliage and tunnelling into tissue. They are important
pests of forestry, particularly conifers. Sirex noctilio is a European species that
has invaded Australia and caused signicant damage to conifer forests.
European spruce sawy Gilpinia hercinia is native to Europe but is also an
invasive species in North America where it is a major pest of forestry.
Continued
22 Chapter 2
Table 2.1. Continued
Order Description
Coleoptera The more important crop pests can be found in the following families: Scarabaeidae,
which include cockchafers and white grubs, whose larvae feed in plant roots and
are important pests of trees and turf, while the adults feed on foliage; Elateridae,
larval forms known commonly as wireworms that eat roots of cereals and bore
into potato tubers; Meliodae, which include pollen beetles and longhorn beetles,
which are important pests of trees; Chrysomelidae, leaf beetles; Curculionidae
(weevils), one of the largest groups of beetles showing a lot of variation and
containing many agricultural pests, the adults generally feed on foliage while
larvae feed on stems, roots, seeds and fruits depending on the species.
Hemiptera The Homoptera usually feed on phloem (plant sap) and some are vectors of viral
plant pathogens. Serious pests occur within the following families: Delphacidae
(plant hoppers), include species that feed on rice and sugarcane; Cicadellidae
(leaf hoppers), include species feeding on crops such as rice; Aleyrodidae
(whiteies), important virus vectors and pests of glasshouse crops, citrus and
cotton, include some serious polyphagous species such as the tobacco white-
y Bemisia tabaci; Aphididae (aphids), among the largest and most important
groups of pests, aphids are highly fecund, reproducing during summer months
by parthenogenetic vivipary (giving birth to live young without the need to mate
with a male), and they vector plant viruses and cause direct feeding damage;
Coccidae (scales and mealybugs), common in the tropics and subtropics where
they are important pests of citrus and other tree fruits. Important crop pests in the
Heteroptera are found in the families Miridae (capsid bugs), which feed on crops
such as cotton, tea and cacao in the tropics, and the Scutelleridae (shield bugs).
Thysanoptera In addition to causing direct feeding damage on plants, some thrips species are
vectors of plant pathogenic viruses. One of the most serious crop pests is the
western ower thrips, Frankliniella occidentalis. A polyphagous species, it feeds
on vegetables, cotton, owers and citrus in its home range in America. It is
also an invasive species in Europe where it is highly damaging to glasshouse
crops and is a vector of plant pathogenic viruses and fungi.
Orthoptera Most important pests are located in the family Acrididae (short-horned
grasshoppers and locusts) about 500 species are considered to be important
crop pests. Complexes of acridid species form the dominant insect grazers in
the main grassland areas of the world; therefore they form important pests of
agricultural grassland and cereals grown in these areas. In some species,
massive outbreak populations can occur. These include the dispersive swarms
of the desert locust, which can cause devastation to crops and other plants
over wide areas. Locust swarms occur on one-third of the worlds land surface
and have been recorded as causing crop devastation since biblical times.
pathogens, e.g. Dutch elm disease. Some insects are important vectors of
diseases of people and livestock. For example, mosquitoes are vectors of
malaria, dengue virus and West Nile virus; bubonic plague is transmitted
by the oriental rat ea Xenopsylla cheopsis; Chagas disease is vectored by the
kissing bug Triatom infestans; human sleeping sickness and animal trypano-
somiasis are carried by tsetse ies; and bluetongue, a serious virus disease
Pests of Crops 23
of ruminants and cattle, is transmitted by the midge Culicoides imicola. Insect
pests can also be particularly problematic if they have developed resistance
to the chemical pesticides used against them, or if they move outside their
native range into new territories. We must remember, however, that most
insects are not pests. Many insect species provide vital, benecial environ-
mental services, for example as pollinators of crops and wild plants. There is
also a wide array of predator and parasitoid species that consume crop pests
and thus act as biological control agents.
Case study: the Colorado potato beetle
The Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chry-
somelidae), is the most serious pest of cultivated potato and also one of the
most difcult of all agricultural insect pests to control (Hare, 1990). It is
thought to have originated in central Mexico, but was rst described from a
specimen feeding on buffalo bur, Solanum rostratum, collected from the US
Rocky Mountains. The adult beetles are about 10 mm long, with a yellow-
orange coloured body and black stripes. The beetle is conned to feeding on
solanaceous plants and has been recorded feeding on about 20 species. In the
1860s it expanded its host range and started feeding on cultivated potato,
Solanum tuberosum, in the USA. It quickly became a serious pest of potato
throughout the eastern USA. It was accidentally introduced into Europe dur-
ing World War I. It is now established throughout Europe with the exception
of the British Isles. The adult beetles overwinter in the soil. In spring, females
lay egg masses, comprising 2060 eggs, on the underside of leaves. In labora-
tory experiments, females were recorded to lay up to 4000 eggs each. The
larvae and the adults feed on plant foliage. If not controlled, then populations
of the beetle will defoliate potato plantings before tubers are formed.
Because of its seriousness for potato production, Colorado potato beetle
was the rst agricultural pest to be controlled on a large scale with synthetic
insecticides. Dichlorodiphenyltrichloroethane (DDT) was used very widely
against it after World War II and was very successful initially. However, the
beetle has a propensity to develop resistance rapidly to pesticides, which
may be connected to its ability to tolerate the glycoalkaloids produced by
solanaceous plants. Resistance to DDT evolved as early as the 1950s. It has
subsequently developed resistance to all types of pesticide deployed against
it including modern compounds such as neonicotinoids (Alyokhin et al.,
2007). Pesticide resistance appears to occur more rapidly each time a new
active ingredient is used.
Acarina: mites
Mites (subclass Acarina) are members of the class Arachnida, which also
includes spiders and scorpions (Lindquist, 1984; Walter et al., 1996). Most
species of the Acarina have no detrimental impact on humans. Indeed,
many perform vital functions within natural and managed ecosystems as
decomposers and predators. However, there are still a large number of aca-
rine species that damage crops. A brief summary of the pest status of the
different acarine orders is given in Table 2.2. Most acarine pests of crops are
24 Chapter 2
contained within the Prostigmata, especially the Eriophyidae and the Tetrany-
chidae, which are obligate plant feeders. Members of these groups attack a wide
range of cultivated plants including fruits, vegetables, cereals, coconut, cassava,
sugarcane and ornamentals (Hill, 1994). The Tetranychidae feed by piercing the
epidermal tissue of the host plant and feeding from cells underneath this layer
(Bondada et al., 1995; Warabieda et al., 1997). Once considered to be of second-
ary importance, they have become serious pests because of their capacity to
develop resistance to pesticides (Cranham and Helle, 1985). In Africa, the
exotic cassava green mite, Mononychellus tanajoa, introduced accidentally
from South America, is a major threat to cassava production (Yaninek and
Herren, 1988). The Eriophyidae are second in importance to the Tetranychi-
dae as phytophagous pests, but still contain some economically important
species. Of the approximately 3000 known species of eriophyoid mites, some
40 species are considered major pests (Lindquist et al., 1996). Some species
transmit viruses. The wheat curl mite, Aceria tulipae, for example, is the vector
of the highly destructive wheat streak mosaic rymovirus, which is wide-
spread in the grain belts of the USA and Canada (Styer and Nault, 1996). Note
also that some species of Acarina most notably in the order Ixodida (ticks)
are important veterinary and medical pests, feeding on blood and transmit-
ting diseases to their hosts. The order Mesostigmata also contains some pest
Table 2.2. Acarine pests of agricultural, veterinary and medical importance. (Detailed
reviews can be found in Helle and Sabelis, 1985a,b; Sonenshine, 1993; Hill, 1994; Lindquist
et al., 1996.)
Superorder Order Pest status
Actinotrichida Astigmata Generally minor pests. Include pests of stored products such
as the our mite, Acarus siro. The bulb mite, Rhyzoglyphus
echinopus, is a pest of bulbs, including onion, and mushrooms.
Prostigmata The Eriophyidae contain about 40 species that signicantly
affect crop production. Some of the more important species
include: the apple rust mite, Aculus schlechtendali; the citrus
bud mite, Aceria sheldoni; the citrus rust mite, Phyllocoptruta
oleivora; the tomato russet mite, Aculops lycopersici; the
coconut mite, Aceria guerreronis; and the wheat curl mite,
Aceria tulipae.
The Tetranychidae contain about 20 species of important crop
pests. Important species include the two-spotted mite,
Tetranychus urticae, and the green cassava mite, Mononychel-
lus tanajoa.
Anactinotrichida Ixodida Over 100 species that are important pests of man and livestock.
Transmit more blood-borne diseases than all other arthropods.
Key genera include Ixodes, Ripicephalus, Amblyomma,
Dermacentor and Boophilus.
Mesostigmata The Mesostigmata contain a small number of important pests.
The red poultry mite, Dermanyssus gallinae, is a vector of
viruses to domestic fowl. The varroa mite, Varroa destructor,
is a major pest of honeybees.
Pests of Crops 25
species of animal hosts. The varroa mite, for instance, is a pest of European
honeybees, having switched from its original host the Asian honeybee in the
20th century, and has had a highly detrimental impact on European honeybee
populations in nearly all countries where they are kept.
Molluscs: slugs and snails
There are thought to be between 90,000 and 250,000 species of molluscs. The
majority live in marine environments and include the cephalopods (octopus
and squid), which have well-developed nervous systems and advanced
functions. Terrestrial slugs and snails occur within the gastropod group of
molluscs and are very important plant pests in some countries (Godan, 1983).
Feeding occurs both above and below ground, on living plant tissue and on
decaying vegetation. Small leaves can be completely consumed while large
ones may have holes in them or be eaten around the edge. Most damage and
plant loss occurs during plant establishment. Additional crop damage occurs
as a result of the growth of bacteria and fungi on snail faeces and slime. In the
temperate climate of central Europe snails are of less signicance as pests than
slugs. Important species include the European eld slugs Deroceras reticulatum
(Muller) and Deroceras agreste (L.). These species are highly polyphagous,
attacking autumn-sown cereals and main crop potatoes, peas, clover, root
crops and reseeded rye, especially in the seedling stages.
Plant pathogens
All species of crop plants are susceptible to infection by parasitic micro-
organisms, which together cause 1213% loss of potential global crop yield,
although yield loss varies widely between different crop species (Pimentel,
1997). Ten different groups of microorganisms have evolved to be parasitic on
plants and cause signicant levels of disease: fungi, algae, oomycetes, plasmo-
diophoromycetes, trypanosomatids, bacteria, phytoplasmas, nematodes,
viruses and viroids. With such a wide array of different types of pathogen
species it is not surprising that understanding plant pathogen biology is crucial
to sustainable disease control. Plant pathogens of crops are widespread and
common in all countries. In economic terms, the most important pathogens
are fungi, oomycetes and viruses. Each crop species is exploited by an aver-
age of about 100 different plant pathogen species (Agrios, 2005). They infect
all parts of the plant (roots, stems, leaves, vascular system) and all life stages
from seed to seedling to mature plants, although generally it is the seedling
stage that is most susceptible. A single pathogen species that can infect a
range of host plant species can, as a result, be responsible for many different
diseases. For example, it is estimated that North American crops suffer from
100,000 different diseases caused by 8000 different fungal species (Agrios,
2005).
Plant pathogens are broadly categorized by the mechanisms by which
they obtain nutritional resources from the host plant. Necrotrophs use toxins
and cell-wall-degrading enzymes to rapidly kill host plant cells and consume
26 Chapter 2
the plant cell nutrients that are released. In contrast, biotrophs require living
plant cells in order to grow and complete their development (Carlile et al.,
2001). As a result they are often specialists and have evolved a complex set of
genes and transcriptional responses associated with virulence as a result of
the arms race for survival between pathogen and host. The negative impact
of biotrophs on the host plant occurs as a result of the pathogen diverting
host nutrients for its own purposes. Pathogens that are described as being
hemibiotrophic use a combination of strategies. The initial phases of infec-
tion are marked by biotrophic growth on host tissues but then as infection
proceeds there is a switch to necrotrophy with extensive cell death. Pure
biotrophs are obligate parasites. However, a range of species of fungal and
bacterial plant pathogens are able to grow both on living hosts and on decaying
organic matter (i.e. saprotrophy) at different stages of their life cycle. Plant
disease manifests itself as a result of a three-way interaction between the
pathogen, the plant host and the environment (Strange, 2003).
Fungi
There are estimated to be about 1.5 million species of fungi. Most are
saprotrophs (i.e. feeding on dead organic matter). Relatively few species
are parasites of animals, but there are estimated to be over 10,000 species that
are parasites of plants. In fact, all plant species are susceptible to fungal
pathogens. Infection generally occurs by the germination of spores on the
host surface, with subsequent development of hyphae on or in the plant. Life
cycles of individual species vary widely and they can be complex. Some spe-
cies are conned to growing on the plant epidermis, while some penetrate
plant tissues between cells and others grow through plant cell walls or
through the vascular system. Transmission can be by vegetative growth or
in some cases by agellated zoospores, which are able to swim a short dis-
tance in free water. However, most fungal plant pathogens are transmitted
by non-motile spores. In particular, the production of large numbers of
asexual spores appears to be a key feature of the rapid spread of fungal
plant pathogens, and they can be transported long distances by air currents
or vectored by animals. Some fungal species produce resting structures
which remain inactive in soil for long periods until contact is made with a
susceptible plant.
Five phyla of true fungi are recognized: Chytridomycota, Zygomycota, Glom-
eromycota, Basidiomycota and Ascomycota. Examples of some key fungal plant
pathogens are given in Table 2.3. The largest number of plant pathogenic spe-
cies is located in Ascomycota. Members of this phylum are characterized by
the production of a sac-like structure (the ascus) that contains the sexual
spores. Infection can occur from both sexual and asexual spores. There are
many species in the Ascomycotina in which the sexual phase is not known and
which reproduce entirely asexually, and which have only been conrmed to
be members of the Ascomycota by using molecular (DNA) data. Some asco-
mycete plant pathogens produce toxins which are highly dangerous to mam-
mals if ingested and which have historically caused severe chronic and acute
problems for people and their livestock. For example, fungal species of the
Pests of Crops 27
Table 2.3. Some important plant pathogens occurring within the true fungi. (From Lucas,
1998; Agrios, 2005.)
Phylum Class Genus Example of host plants/disease
Zygomycota Zygomycetes Rhizopus Soft rots and postharvest decays
of fruit and vegetables
Mucor Stored vegetables and fruits
Olpidium Infects brassicas and transmits
pathogenic viruses
Ascomycota Dothideomycetes Alternaria Foliar diseases, stem rot and fruit rot
and postharvest disease on a wide
range of fruit and vegetables
Septoria Leaf spot and blight on fruit,
vegetables and cereals
Eurotiomycetes Aspergillus Aatoxins
Leotiomycetes Erysiphe Powdery mildew on a range of
ornamentals and vegetables
Botrytis Blossom blights and fruit rots in fruit,
vegetables and ornamentals;
postharvest decays of fruits and
vegetables
Sclerotinia Rots and moulds in very wide range
of vegetables, ornamentals and eld
crops
Sordariomycetes Nectria Cankers in many tree species
Magnaporthe Rice blast
Colletotrichum Anthracnose diseases in many annual
crops and ornamentals
Claviceps Ergot in cereals and grasses
Fusarium Wilts on vegetables, owers, some
plantation crops; head blight on
grains, root and stem rots of
vegetables, owers and eld crops;
postharvest decay on
vegetables and ornamentals;
mycotoxins
Ophiostoma Dutch elm disease (wilt)
Gaeumannomyces Take-all disease of cereals
Basidiomycota Pucciniomycetes Pucccinia Severe diseases on crops from the grass
family wheat, rye, barley, oats,
sugarcane. Some species cause
disease in cotton, vegetables or
ornamentals
Uromyces Rusts on legumes
Phakopsora Soybean rust
Ustilaginomycetes Entyloma Rice leaf smut
28 Chapter 2
genus Claviceps are pathogens of cereals. They grow in developing cereal
grains on the maturing plant and replace the seeds with fruiting structures
known as ergots. These contain fungal alkaloids and when eaten they are
highly toxic; effects include skin blisters, convulsions, hallucinations (known
as St Anthonys re), permanent mental damage, spontaneous abortion and
gangrene. Ergotism has resulted in countless deaths, probably since the start
of cereal cultivation. A range of mycotoxins are also produced by other fungal
species growing on both live plants and harvested crops. Aatoxins, pro-
duced by the fungus Aspergillus avus and related species, are carcinogenic
and highly toxic to people and livestock, and are produced on fungal-infected
cereal grains, legumes and nuts. Chronic and acute effects occur depending
on the dose received.
The Basidiomycetes contain the rusts and smuts, which are obligate
biotrophic plant pathogens and contain a number of economically important
species. Rusts are members of the class Pucciniomycetes. They are among the
most destructive of plant diseases. These are obligate plant pathogens that infect
leaves and stems. For example Puccinia species cause severe infections on wheat,
other cereals and also crops such as cotton. Most species within the genus are
highly specialized, infecting just a small number of plant species or genera.
Smuts are members of the class Ustilaginomycetes. They have a worldwide dis-
tribution and comprise about 1200 species. The plant is not normally killed
by the infection but growth can be severely restricted.
Oomycetes
Some of the most important plant diseases are caused by organisms that have
very similar morphologies and life histories to fungi, but have been shown
by molecular studies to be members of different biological taxa and thus
evolved the ability to parasitize plants independently. Of these the most
important are the oomycetes, which were considered to be true fungi until
about 1990, but are actually part of a large group of eukaryotic protists
termed the stramenopiles that includes the brown algae and diatoms. The
oomycetes produce infective, motile haploid zoospores that are released
from sporangia. They swim over the plant surface, germinate and grow into
the plant tissue to cause disease. Sexual reproduction which may or may
not be present leads to the production of diploid zoospores, which enable
survival over winter.
Some of the most important oomycete plant pathogens are listed in Table
2.4. The main oomycete plant pathogens are contained within two orders
the Saprolegniales and the Peronosporales. The latter contains some of the most
important of all plant pathogens. Pythium species cause damping off on seed-
lings, seed and root rots. Phytophthora species cause blights, fruit and root rots
in a range of plants (and include Phytophthora infestans, the cause of late blight
of potato, which resulted in the Irish famine). Phytophthora ramorum
is an emerging disease that causes sudden oak death and has resulted in
signicant losses of oaks in California and Oregon; it has recently arrived
in Europe. The oomycetes also include the downy mildews, which contain
different groups that infect mono- and dicotyledonous plants, respectively.
The Economics of Switching Technologies 29
Table 2.4. Some oomycete plant pathogens. (From Lucas, 1998; Agrios, 2005.)
Species Example of host plants/disease
Pythium spp. Damping-off diseases of seedlings of a very wide range of plants.
Also cause seed, root and fruit rots
Phytophthora infestans Potato late blight
Phytophthora ramorum Sudden oak death
Peronospora spp. Downy mildews in a range of plants, e.g. onion, tobacco,
soybean, lucerne, clover
Hyaloperonospora brassicae Downy mildew of brassicas
Plasmopara viticola Downy mildew of grapes
Examples include Bremia and Peronospora species, which infect a range of
fruit and vegetable hosts. Hyaloperonospora brassicae causes downy mildew
on brassicas. Albugo candida causes white rust on crucifers.
Bacteria
There are about 1600 known bacterial species and only about 100 of these are
parasites of plants. Agrobacterium tumifaciens causes the disease crown gall
and infects about 200 different plant species. Species in the genus Erwinia
cause blights, wilts and soft rots in many crop species. For example Erwinia
amylovora causes the disease known as reblight, a serious disease of apples
and other species. Xanthomonas campestris pv. campestris is the main bacterial
disease of crucifers and can cause severe epidemics in these crops.
Viruses
There are about 700 different viruses pathogenic to plants and they include
some that are highly important economically (Strange, 2003). Viruses comprise
nucleic acid (single-stranded or double-stranded DNA, or single-stranded
RNA) in a protective protein coat. Most plant viruses are of the single-stranded
RNA type. Host cells become infected when viral nucleic acid passes through
the cell membrane and uses the host cell metabolism for its own reproduction.
Infection occurs through wounds made mechanically, by a vector or by vertical
transmission from infected pollen grains. Some of the most serious plant
pathogenic viruses are vectored by insects and there is often a high level of
specicity between virus and vector. For example, barley yellow dwarf virus
a member of the luteoviruses is transmitted by aphids and infects 150 spe-
cies of grasses including all cereals. The largest number of plant pathogenic
viruses (over 100 species) is contained within the potyviruses (named after
potato virus Y, PVY) and they affect crops such as sugarcane, beans, salad and
root crops. Some of the most economically important potyvirus species are
transmitted by aphids. Geminiviruses are single-stranded DNA viruses and
cause serious diseases of vegetable crops, being transmitted by whiteies and
leaf hoppers. They include African cassava mosaic virus (which is estimated to
result in a 50% loss of the annual potential yield of cassava in Africa), maize
streak virus, and tomato yellow leaf curl virus.
30 Chapter 2
Plant pathogenic nematodes
Nematodes (phylum Nematoda) are unsegmented worm-like animals. They
are very diverse (about 80,000 species have been recorded) and include many
parasitic species of animals and plants (about 15,000 species). Most plant
pathogenic nematodes are associated with the soil. They reduce both crop
yield and market value by causing cosmetic damage. Infection is generally
done by juveniles, which hatch from eggs and penetrate young roots to feed on
plant tissue. Important groups include root-knot nematodes, Meloidogyne spp.,
which infect over 2000 plant species including vegetables as well as staples
such as potatoes and yam. Infection results in the formation of galls, within
which the nematodes feed and which make the roots appear knotted. Cyst
nematodes are common in temperate regions, and consist of species in the
genera Heterodera and Globodera. Examples include soybean cyst nematode,
Heterodera glycines, and potato cyst nematode, Globodera pallida.
Case study: the Irish Famine
Crop losses to some plant pathogens have resulted in severe famines that
have had global geopolitical repercussions. Perhaps the best known exam-
ple in the Western world is the Irish Famine of the mid-19th century. In the
1800s, cultivation of potato (Solanum tuberosum) became widespread in
Europe because the crop gave excellent yields (Agrios, 2005). Potatoes were
particularly well suited to the cool and wet climate in Ireland and gave
good yields to feed poor tenant families who had to survive on very little
land. By the 1840s a third of the population was entirely dependent on the
crop. However, crop failures occurred in 1845 and 1846 as a result of a new
disease, termed late blight, which had not been present in Ireland before
and which caused up to 75% of the crop to be destroyed. The cause of the
disease was not discovered until 1861 when a fungus (which is now known
to be an oomycete pathogen), Phytophthora infestans, was shown to be the
infective agent. The disease was accidentally introduced with potatoes
from central Mexico, which is now known to be the centre of origin of the
disease. It was rst recorded outside Mexico in the USA in 1842 and
appeared in Europe shortly thereafter. The blight epidemics of 1845 and
1846 occurred across Europe and in North America, but they were far
more severe in Ireland than elsewhere because of the widespread habit of
keeping potatoes in underground stores after harvest, which were also
wiped out by blight. Cool moist weather that favoured potato production
also favoured disease. The situation was inamed by a range of socio-political
and economic factors including restrictions on aid imposed by the British
government. The failure of the potato harvest led to famine, collapse of
civil society and associated epidemics of cholera, dysentery and other dis-
eases. Family breakdown, starvation, disease and forced expulsion resulted
in many leaving the land. The famine is thought to have resulted in one
and a half million deaths while the same number of people emigrated,
mainly to North America. The potato famine remains a source of much
historical debate and retains a strong cultural resonance within the Irish
Diaspora to this day.
Pests of Crops 31
Today, late blight is controlled using a combination of cultural practices,
pesticide sprays and varietal resistance. The centre of origin of P. infestans in
Mexico is also a centre of genetic diversity for Solanum species closely related
to the cultivated potato, S. tuberosum. As a result of the co-evolution of P.
infestans and its host species, resistance genes were discovered in native Sola-
num species (Grunwald and Flier, 2005). However, when single gene resis-
tance was bred into cultivated potato it was rapidly overcome. The emphasis
now is on breeding durable resistance based on quantitative traits (Solomon-
Blackburn et al., 2007).
Phytophthora infestans can reproduce asexually and sexually. Sexual
reproduction requires the presence of two mating types (A1 and A2) in the
pathogen population. The late blight pathogen that was accidentally intro-
duced into Europe in the 1800s consisted of just one genetic strain of the A1
mating type (Fry et al., 1992; Goodwin et al., 1994). The A2 mating type was
accidentally introduced into Europe in the 1980s. This facilitated sexual
recombination in the species and as a result new strains of the pathogen have
evolved. Some of these have increased aggressiveness to host plants and
resistance to metalaxl fungicides (Agrios, 2005).
Weeds
Weeds are undesirable plants. This denition is dependent on context, since
a plant species that is undesirable in one situation may be desirable in another.
For example, many arable weeds reduce the yield or quality of a crop but
they also serve as a resource for benecial invertebrates and birds, and
thus are important for farmland biodiversity and conservation of wildlife.
Weeds can be placed into four overlapping categories.
1. Agricultural weeds interfere with farm production by competing with
crops for resources (soil nutrients, light, water), by contaminating the harvest
with their seeds, by acting as reservoirs for invertebrate pests and plant
pathogens, or because they are poisonous to people or livestock. There are
estimated to be around 500 major species of weedy plants in the USA (Hajek,
2004) and in the UK there are about 300 potential weed species found in
arable land alone (Naylor and Drummond, 2002). Approximately 40% of
agricultural weeds occur in two families: the Poaceae (grasses) and the Astera-
ceae (composites and asters).
2. Invasive weeds are plant species that have been introduced to an area,
region or country where they are not indigenous and which subsequently
become established and spread.
3. There are also a number of weed species that are parasitic on other plants.
4. Finally, volunteers are crop plants that grow in undesired locations.
These can be a real problem when the farmer practises crop rotation, i.e. if
crop plants cultivated last season survive over winter as seeds or plant debris
and grow up among the following crop grown in same eld. Some crops
such as oilseed rape are also good at escaping from the eld and growing as
weeds elsewhere on the farm.
32 Chapter 2
In ecological terms, many agricultural weeds are ruderal species,
i.e. plants that are adapted to colonize disturbed habitats. Weed establish-
ment occurs from seeds that are carried by the wind, by animals, by human
activity (e.g. on farm machinery) or by the germination of seeds that are already
present in the soil (i.e. the weed seed bank) (Radosevich et al., 2007). Cultivated
elds are continually being disturbed, and this creates an unusual form of
cyclical plant succession that favours the growth of ruderal weed species. The
weed ora of agricultural elds tends to be dominated by herbaceous annual
species that have a greater competitive ability in the seedling stage than peren-
nial plants. Weeds are also favoured by features of agricultural production
that counteract the normal limitations on plant population development. This
can include an absence of herbivores and soil nutrient enrichment by applica-
tion of fertilizers. While many agricultural weeds are opportunists, it would
be wrong to think of them all as ecological generalists. Agrestals, for example,
are specialist plants that require the disturbance associated with tillage and
ploughing, and are associated with particular cropping systems.
Pest Control
Today, most farmers and growers are reliant on chemical pesticides for pest
management. Alongside advances in mechanization, crop breeding, irriga-
tion and synthetic fertilizers, they have been of tremendous benet in increas-
ing crop yields in the last half century. However, their use is becoming more
difcult due to the evolution of resistance in pest populations, pest resur-
gence and the emergence of secondary pests following the destruction of
natural enemies. An increasing number of pesticide product withdrawals are
happening because of health and safety legislation or lack of prot for the
product manufacturers, and this is adding to the challenge. All of these fac-
tors are reducing the availability of effective compounds. Further pressures
on pesticide use are happening where consumers and other groups are
expressing concerns about the safety of pesticide residues in food. When
used injudiciously, synthetic pesticides may also cause harm to the environ-
ment. Some older compounds have caused serious health effects in agricul-
tural workers, primarily because of inadequate controls and safety equipment
during handling, and unsurprisingly this occurs nearly always in economically
deprived countries.
Farmers and growers in many countries are trying to reduce the amounts
of conventional chemical pesticides used, in response to demands from
retailers, governments and pressure groups. This needs to be done without
sacricing crop quality and agricultural productivity. The latter is a key issue:
the world population is forecast to reach 7 billion people in 2012 and to be
greater than 9 billion by 2050 (UN, 2004, 2009). This means that production of
food and other agricultural crops will have to increase signicantly in future
years. However, this must be done without putting additional strain on natu-
ral ecosystems and the global climate (agriculture is a major contributor to
greenhouse gas emissions).
Pests of Crops 33
Historically, many of the improvements in crop protection were
by-products of new developments in agronomic practice. The use of crop
rotations, growing local crop varieties and the better control of water and
drainage are good examples of this (Thacker, 2002). Rational inquiry into crop
protection, driven by theory and experiment, is a relatively modern endeav-
our. Systematic advances in crop protection only really started during the lat-
ter part of the 19th century with the use of nicotine for insect control and the
development of inorganic salts, such as elemental sulfur and Bordeaux mix-
ture, against plant pathogenic fungi (Thacker, 2002). These compounds had
low biochemical specicity and they tended to be toxic to mammals. They
were superseded by the development of more specic, less harmful, synthetic
organic pesticides during and after World War II. Synthetic organic pesticides
revolutionized agriculture and their development marked the start of the true
era of modern crop protection science. They were part of a set of related
advances in technology that also included nitrogenous fertilizers, plant breed-
ing, irrigation and sophisticated mechanization. Crop protection rapidly
became reliant on technology and the intensive use of non-renewable
resources. This approach has been dubbed industrial farming and has
become the dominant paradigm in the Global North. Alongside other compo-
nents it is responsible for increasing agricultural production in Europe by 68%
and in the USA by 100% since the 1960s (Pretty, 2008). However, industrial
farming is not without signicant costs. These include environmental pollu-
tion, soil erosion, pesticide poisonings of people, and a signicant loss of the
biodiversity upon which we depend for ecosystem services such as plant pol-
lination, natural pest control, and clean air and water. We shall discuss these
issues in more depth later, but it is tempting to conclude that, while society had
sufcient knowledge to develop the agricultural technology to dramatically
increase crop yields, it lacked the ability to use it in a sustainable way.
The development of the industrial paradigm of pest management and the global
adoption of chemical pesticides
The 30 or so years after the end of World War II saw a wide range of synthetic
organic chemicals developed for use as pesticides. These compounds were
effective, could be synthesized cheaply, and different application systems
were available to suit agronomic practice, such as sprays, baits, dusts,
drenches and fumigants. Their high efcacy, low cost and ease of application
enabled reliable pest control for the rst time. They were seen as a silver
bullet approach to pest management, one consequence being that they were
used as prophylactics, with frequent, high-dose applications usually on a
calendar basis irrespective of the size of the pest population. The aim of this
approach was eradication of pest populations using chemical pesticides. As
we shall see, it has resulted in signicant negative effects.
The history of the development of these products has been characterized
by improvements in the environmental performance of active compounds
and a decrease in the amount of material applied to control a pest population.
34 Chapter 2
Let us take insecticides as an example. Four major groups of synthetic organic
insecticides were introduced widely from the 1940s: organochlorines, organo-
phosphates, carbamates and pyrethroids. The rst synthetic organic insecti-
cide, the organochlorine (OC) DDT, became commercially available in 1942
(Thacker, 2002). DDT works by disrupting ion movement across neurons. It
was cheap to produce, stable and persistent, selective for insects and with a
broad spectrum of insect activity. It allowed high levels of control of many
insect pests of agricultural crops for probably the rst time in history and it
has also been of major signicance for the control of medically important
insects. For example, it has been used widely to control mosquito vectors of
malaria and it is still in use against mosquito pests today. However, the high
persistence of DDT and other OCs means that they can bioaccumulate in the
fat reserves of animals, becoming increasingly concentrated along the food
chain and resulting in toxic effects in non-targets. Concerns about the mam-
malian toxicity of DDT and other OCs have resulted in these compounds
being banned in much of the world. Development of OCs was followed rap-
idly by the introduction of organophosphates (OPs), which include common-
name compounds such as parathion, fenitrothion and pirimiphos-methyl.
OPs act as neurotoxins, with anticholinesterase activity, but they are less per-
sistent in the environment than OC compounds. Some have systemic proper-
ties and thus can be applied to one part of a plant but still kill insects feeding
on another part. This is highly valuable for insect pests that feed on the
underside of leaves and are shielded from direct contact with pesticide
sprays. OPs are often toxic to insects in the order Hymenoptera, which
includes many species of parasitoid that are important natural enemies of
insects, and hence this can create problems for use in IPM, which seeks to
promote the action of natural enemies in the crop environment. Concerns
about the ecotoxicological effects of OPs and their potential impact on people
are leading increasingly to these products being withdrawn.
The two other major groups of insecticides from the post-war period
were the carbamates and the pyrethroids. The carbamates (common names
of carbamate molecules include aldicarb, carbofuran and bendiocarb) are
closely related to the OPs, and like them have anticholinesterase activity.
They were rst introduced in the late 1950s. They tend to be broad-spectrum
compounds that work by contact action or when the pest insect has eaten
them. The pyrethroid pesticides are a class of neurotoxic compounds that
work by affecting the activity of sodium channels in the plasma membranes
of nerve cells. They are based on synthetic forms of pyrethrum, a natural
extract of chrysanthemum with insecticidal properties, modied to improve
their chemical stability. Pyrethroids have a very low toxicity to mammals and
birds and thus are popular choices as insecticides. They are, however, highly
soluble in water and toxic to sh and other aquatic life, and hence are not
used in situations where they can contaminate watercourses, and they can
also have negative impact on non-target insects as their insecticidal activity
is not specic. Pyrethroids are used very widely against pests of agricultural
and horticultural crops. Common names of pyrethroid molecules include
deltamethrin, cypermethrin and fenuthrin.
Pests of Crops 35
During the same period after World War II, new groups of synthetic
chemical fungicides and herbicides were also developed. Synthetic fungi-
cides included the dithiocarbamates, trichloromethylmercapto compounds
(such as captan), imidazoles (inhibitors of ergosterol biosynthesis, an essen-
tial component of the cell membrane in true fungi, and which have systemic
action), benzimidazoles (such as carbendazim and benomyl), acylalanines
(compounds with systemic action that are effective against oomycetes) and
carboxamides (used against Basidiomycetes) (Morton and Staub, 2008). Crude
herbicides, such as oil wastes, thiocyanates and creosote, which had to be
used in very high doses were replaced with selective compounds. The rst
selective, synthetic organic herbicide, 2 methyl-4,6-dinitrophenol, was devel-
oped in the 1930s1940s and used as a selective herbicide on cereals. It has
toxicity to mammals but is less toxic than the insecticides developed and
used in this period; however, it was associated with causing health problems
in operators when it was introduced as they were unaccustomed to safe
operating procedures necessary for chemical sprays (Green et al., 1987). Other
selective herbicides developed in this period included compounds that
mimic the plant growth hormone indol-3-acetic acid and cause abnormal
plant growth, and are used as hormone weedkillers in cereals. These include
phenoxyacid compounds developed in World War II such as 2,4-D (2,4-di-
chlorophenoxyacetic acid), phenoxybutyrics and pyridine acid herbicides
(e.g. picloram, a systemic compound used against broad-leaved weeds).
Other herbicide compounds achieved selectivity though physical factors,
such as absorption through roots rather than through foliage. These include
herbicides such as paraquat, a foliage-acting herbicide. It is toxic to humans
if taken as an overdose and the effects are irreversible, hence it has a notori-
ous reputation as a poison as it used to be widely available to the public as a
garden weedkiller. Glyphosate is a widely used organophosphorus com-
pound (but not related to OP insecticides) that has very low mammalian tox-
icity and acts on plant foliage (Duke and Powles, 2008). There is also a wide
variety of herbicide compounds based on the urea and triazine chemical
families. Triazines are taken up by plant roots and inhibit photosynthesis,
and include herbicides such as atrazine, which is used for weed control in
maize (Knott, 2002).
Problems Associated with Using Pesticides According to the Industrial
Approach to Farming
Viewed solely from the standpoint of increasing food production, industrial
farming has been highly successful. Today most farmers and growers in the
developed world rely on chemical pesticides for crop protection. Synthetic
organic pesticides have made an enormous contribution to increases in crop
yields and will continue to play a key role in crop protection. However, their
use as part of industrial farming is not without signicant external costs, as
listed below. And while these pesticides will remain an important tool for
farmers and growers, they are not a panacea for crop protection.
36 Chapter 2
Broad-spectrum activity and environmental persistence
Until the 1980s, most of the pesticide compounds used tended to be broad-
spectrum agents that were sprayed on a regular basis according to strict calendar
dates or crop phenology. Until this period there was little attempt to target
pesticide applications according to when pest populations were most active
or at their most threatening (a process known as supervised spraying, super-
vised control or guided control). The injudicious use of broad-spectrum
pesticides, applied without supervised control, in combination with other
aspects of agricultural systems, can be a source of environmental harm
and social tension (Tilman, 1999; Millennium Ecosystem Assessment,
2005). Concerns about the environmental and human safety impacts of
pesticides were raised soon after the widespread adoption of the rst gen-
eration of synthetic organic compounds following World War II and came
to the fore with the publication of Rachel Carsonss book Silent Spring in
1962. As has been stated above, some pesticides can become bioaccumu-
lated resulting in acute and chronic toxicity to animals at the top of the
food chain. Ecosystem effects of pesticides can include disruption to micro-
bial communities and their activity in soils. There can be other adverse
effects on terrestrial and aquatic environments caused by pesticides killing
non-target organisms. These can have multiplier effects by reducing the
availability of food for species at higher trophic levels, for example by
removing insects that act as food for birds. However, we must emphasize
that because chemical pesticides vary signicantly in their physicochemi-
cal properties, the extent of any negative impact varies according to the
particular active ingredient.
Effects on non-target organisms
Basic economics means that pesticides with a broad spectrum of activity are
more attractive to agrochemical companies and to farmers. Pesticides are
expensive to develop and hence an active ingredient that kills a wide range
of pest species will result in a larger market for manufacturers, while for
farmers there are considerable savings to be made if only one product needs
to be used for pest control. However, pesticides with too broad an activity
will create problems by lowering the biodiversity of non-pest organisms. The
negative effects of broad-spectrum insecticides on benecial arthropods are
well documented (Thacker, 2002). The pollination of crops by honeybees and
other insects, for example, is thought to account for the production of about
a third of our food plants, and thus actions that reduce pollinator numbers
must be avoided (Pimentel, 1997). Conventionally, the effect of pesticides on
non-target arthropods has been estimated by: (i) calculating the median
lethal dose of the pesticide; and (ii) making an informed decision on whether
this dose is likely to be received by non-targets in the eld. However, it is
becoming increasingly apparent that a range of sublethal effects can occur on
benecial arthropods and these need to be taken into account for a full under-
standing of the ecological impact of a candidate pesticide. These include phys-
iological effects, for example on development, immune function, fecundity
and sex ratio, as well as effects on arthropod behaviour such as navigation,
Pests of Crops 37
feeding and oviposition. These effects can interact, resulting in negative
impacts on community ecology, and may result in economic losses due to
reductions in pollination or natural enemy activity (Desneux et al., 2007). We
must be careful in jumping to conclusions, however. The sublethal effects of
pesticides are often temporary, and the risks can be managed by controlled
application so that chemical residue does not come into contact with non-
crop areas, such as hedgerows or eld margins. Moreover, not all interactions
are detrimental. For example, pyrethroid insecticides sprayed on to elds can
interact additively with naturally occurring aphid parasitoids for aphid control
(Desneux et al., 2007). This points to a need for improving our understanding
of the effects of pesticides on non-targets that can be incorporated into the
regulatory system and used to minimize negative effects.
Target pest resurgence
Target pest resurgence occurs when a pesticide kills both a pest and its natural
enemies, and the pest population recovers rapidly afterwards because of the
absence of natural enemies. Often the pest population will become larger
than before the pesticide was applied. The size of the effect depends on the
spectrum of activity of the pesticide and its persistence in the environment
and will vary according to the active ingredient.
Secondary pests
Secondary pests can occur when previously innocuous organisms, which
were maintained at low levels because of the action of natural enemies,
increase to problem levels because a broad-spectrum pesticide has killed
their natural enemies. This can lead to increased application of pesticides to
control the new pest, which only serves to make the problem worse. For
example, use of broad-spectrum pesticides for production of cotton in the
USA from the 1960s to the 1980s led to an increase in the number of serious
pest species from two to eight (Begon et al., 2006).
Pesticide resistance
Inappropriate use of pesticides can also lead to negative effects that reduce
the effectiveness of the pesticide to control target pest populations. Herit-
able resistance can occur through decreased sensitivity of target cells or the
evolution of mechanisms for pesticide detoxication. Individuals that have
evolved genetically based pesticide resistance will be favoured by natural
selection and their offspring will form an increasingly large proportion of
the population over time while the selection pressure remains. The expres-
sion of the resistant phenotype will become apparent in the pest population
as control failures. Generally, the risk of resistance developing increases if
only pesticides with the same mode of action are used. This can lead to
cross-resistance (i.e. resistance to different pesticides that have the same
mode of action). Multiple resistances (resistance to pesticides with different
modes of action) can also occur. Resistance to pesticides evolved soon after
the rst synthetic pesticides were introduced. For example, resistance to
DDT was observed within 7 years of this pesticide rst being used (Hajek,
38 Chapter 2
2004). Insecticide resistance often evolves within 10 years and herbicide
resistance within 1025 years of introduction of a new compound (Palumbi,
2001). Worldwide, over 500 species of arthropod pests have resistance to
one or more insecticides (Hajek, 2004). Over 347 biotypes of 200 species of
herbicide-resistant weeds have been documented by the International
Survey of Herbicide Resistant Weeds (WeedScience.com, 2010). Fungicide
resistance occurs in only a few plant pathogens but it has been recognized
as a problem for some while (Skylakakis, 1987; Milgroom et al., 1989; de
Waard et al., 1993).
Pesticide resistance can be the driver for alternative control measures as
part of IPM. A good illustration is the two-spotted spider mite, Tetranychus
urticae, attacking glasshouse crops and many outdoor crops. Resistance to a
wide range of pesticides in T. urticae populations has forced a change in its
management in glasshouse crops from chemical to biologically based con-
trol using predatory phytoseiid mites (Hussey and Scopes, 1985; Coop and
Croft, 1995). Elsewhere, such as on apples and citrus, control of tetranychids
has moved increasingly to IPM management strategies that conserve natu-
ral enemies (McMurtry, 1985; Hardman et al., 1995; Croft and Slone, 1998;
Lester et al., 1998).
Toxicity
Pesticides can have mammalian toxicity and, depending on the overall level
of exposure, this can cause a variety of serious health effects in people.
Human poisonings of agricultural workers and others exposed to pesticides
can occur from handling pesticides during manufacture or application, or
from environmental contamination, such as contaminated water sources.
This is mainly a problem in the Global South in situations where those work-
ing with pesticides have inadequate access to protective equipment and
proper training. Worldwide, 26 million cases of pesticide poisoning are esti-
mated to occur annually, predominantly in developing countries, which also
see the largest number of fatalities, estimated at 220,000 globally per annum
(Paoletti and Pimentel, 2000).
Interactive effects
The problems associated with the industrial approach to pest management
do not sit in isolation from other pest management concerns. For example,
some species that have developed pesticide resistance are also invasive alien
species, such as the varroa mite or western ower thrips. Different pest species
also interact to create further problems. Thus almost to add insult to injury
the pesticide-resistant, alien invasive, western ower thrips, Frankliniella
occidentalis, is a vector of plant pathogenic viruses. The arrival of an invasive
pest species can disrupt the current control methods used to control other
pests. And we must remember that an organism that is a pest in one context
may be benecial in another, as we have seen already in the case of arable
weeds, which are also important as food for farmland birds. There are wider
issues too, for example the long-term viability of using pesticides that are
Pests of Crops 39
derived from fossil fuels. These issues make pest problems particularly com-
plex to address and to solve.
Declining availability of products
Problems of resistance, resurgence and secondary pests associated with
industrial farming can result in farmers entering a negative spiral in which
they have to increase the number and type of pesticide applications year on
year. Such an approach soon becomes untenable. Leaving aside the potential
agronomic and environmental consequences of this approach, the rate at
which new products are made available to farmers has declined rapidly
since the 1970s. Due to a fall in the discovery of new active molecules and
the increasing costs of registration, the availability of new pesticide active
ingredients is declining (Thacker, 2002). New active ingredients are now
estimated to cost around US$200 million and take about 10 years to develop.
The availability of conventional, synthetic organic pesticide products is
likely to decline further in the future. The number of agrochemical compa-
nies concerned with the development of new pesticides has reduced due to
mergers, meaning that the crop protection market is now dominated by a
small number of large corporations. The high costs of development will
mean that these companies will concentrate on producing pesticides only
for a small number of broad-acre crops such as cotton, rice, maize and wheat.
At the same time, the pool of available products is being squeezed by
increased government regulation or restrictions put on farmers by retailers.
For example, at the time of writing, European Commission proposals for a
new pesticides Regulation are being negotiated that will affect the whole of
the EU. The Regulation will update the human and environmental safety
cut off criteria by which plant protection products are approved. This is
likely to result in the prohibition of a signicant number of synthetic chemi-
cal pesticide products. Impact assessments undertaken in the UK suggest
that production of minor crops might be particularly affected, mainly
because the majority of herbicides approved for these crops would no longer
be approved. The loss of pendimethalin as a pre-emergence treatment would
jeopardize weed control in cereals. The availability of fungicides that are
considered to pose a hazard as endocrine disruptors could be reduced also,
which might result in 2030% yield losses in wheat due to an inability to
control Septoria tritici, and would jeopardize disease control on oilseed rape
leading to signicant yield loss (PSD, 2008a,b).
Integrated Pest Management
New systems of crop protection must be effective in improving crop yield
and quality, be safe for people, not cause unacceptable environmental harm,
prevent the evolution of pesticide resistance and be adaptable to cope with
emerging pests. In large part, the shortcomings of the industrial approach to
crop protection stem from the fact that its practitioners do not utilize know-
ledge of agro-ecology to strategically control the use of pesticides. Most
40 Chapter 2
experts agree that the way to improve crop protection is through IPM. A
pragmatic denition is that IPM is a systems approach that combines a wide
array of crop protection practices with careful monitoring of pests and their
natural enemies. IPM was dened formally in 1967 by the United Nations
Food and Agriculture Organization Panel of Experts on Integrated Pest
Control as:
a pest management system that, in the context of the associated environment
and the population dynamics of the pest species, utilizes all suitable techniques
and methods in as compatible a manner as possible and maintains the pest
populations at levels below those causing economic injury.
(Bajwa and Kogan, 2002)
A more ecologically focused denition was given in Flint and van den Boschs
(1981) seminal book, Introduction to Integrated Pest Management:
Integrated pest management (IPM) is an ecologically based pest control strategy
that relies heavily on natural mortality factors such as natural enemies and
weather and seeks out control tactics that disrupt these factors as little as
possible. IPM uses pesticides, but only after systematic monitoring of pest
populations and natural control factors indicates a need. Ideally, an integrated
pest management program considers all available pest control actions, including
no action, and evaluates the potential interaction among various control tactics,
cultural practices, weather, other pests, and the crop to be protected.
IPM practices include resistant varieties, physical and cultural (i.e. culti-
vation) methods, biological controls and judicious use of modern, selective
pesticides. These different tactics can be combined in various ways to suit
local needs. Decisions can be made about what tactics to use, and when and
where to use them, based on an understanding of the ecology of the pest, its
natural enemies, and agronomic and environmental conditions. The aim of
IPM is not pest eradication; rather it is the more realistic goal of reducing a
pest population below its economic injury level.
In industrialized economies, IPM is seen as technologically based and is
focused on using a suite of complementary control options in combination
with pest monitoring and economic action thresholds. Here, IPM is a natural
progression from supervised or guided control, in which the farmer uses eco-
nomic thresholds to decide when to apply chemical pesticides. It is doubtful
whether farmers and growers could take up IPM successfully unless they
were already familiar with supervised control. In some developing nations,
however, a different IPM model has been developed, based on training farm-
ers to better understand the importance of natural biological control and to
rely on their own observations in order to decide when to spray pesticides
(Waage, 1997; Dent, 2000). In both situations, the goal is the same; namely to
achieve a exible and durable system that minimizes impacts on other com-
ponents of the agro-ecosystem (Kogan, 1998). Examples of IPM practice in
different crop types are given below.
IPM is signicantly more complex compared with the simple spray-and-
pray approach to pesticides used in industrial farming. Therefore IPM pro-
grammes are best developed incrementally. There are many different types of
Pests of Crops 41
IPM programme and a wide range of levels of sophistication. IPM is also
dynamic, in the sense that the pest problem is always changing; for example,
when new pests emerge, when pesticide resistance develops or pesticides are
withdrawn, when new crop varieties become available or when agricultural
practices change. Prokopy (1993) set out four levels of IPM that are divided
up according to their degree of sophistication (Fig. 2.1). The baseline level,
Level One, concerns integrating different chemical, biological and cultural
controls for the management of a single species of pest on a single type of
crop. The top level, Level Four, involves incorporating all pest management
practices within an overall Integrated Crop Management system that
involves all members of the policy network (farmers, extension services,
industry, retailers, regulators, non-governmental organizations, etc.) and
takes account of the social, cultural and political context of farming. All four
levels require sound information on: (i) the causes of the pest outbreak; (ii)
the natural factors that limit outbreaks and which can be exploited for pest
management; (iii) how the pest population changes over time and when
pest control tactics should be deployed; and (iv) the costs and benets of the
different control tactics at the farmers disposal.
Understanding the Natural Factors that Determine Pest Population
Levels: Some Basic Ecological Concepts
IPM begins with understanding the life history strategy of a particular pest,
together with the factors that naturally determine its abundance. Some inherent
features of agricultural production cause pests to proliferate, but on the other
LEVEL ONE IPM
Multiple management tactics integrated for individual pests in each class of pests
Multiple management tactics integrated for a single group of pests (arthropods,

pathogens, weeds or vertebrates)
LEVEL TWO IPM
Multiple management tactics integrated across all groups of pests
LEVEL THREE IPM
All pest management tactics integrated with all farming practices
LEVEL FOUR IPM
IPM integrated with social, cultural and political realm; involve farmers, researchers,
extension, industry, environmentalists and regulatory agencies
Fig. 2.1. Prokopys four levels of integrated pest management (IPM). (From Prokopy, 1993.)
42 Chapter 2
hand there are also factors that limit the size and range of pest populations.
An ecological approach enables a better understanding of why pest outbreaks
occur and hence the effective measures that can be put in place to prevent or
manage such outbreaks in ways that cause minimum disturbance to other
components of the agro-ecosystem. Knowledge of pest ecology allows ex-
ible, responsive pest management. For example, understanding the causes of
pest outbreaks can allow changes to be introduced to farming practice that
may prevent an outbreak occurring in the rst place, such as encouraging
populations of natural enemies or growing mixtures of crop varieties that
slow down the spread of a pest population. It also allows predictions to be
made of when pests are likely to be most active, and enables therapeutic
agents to be applied only when necessary, as opposed to applying them
regardless of pest numbers, as occurs with calendar-based spraying of pesti-
cides. This not only saves the farmer money but also helps prevent unwanted
effects such as the evolution of resistance to pesticides.
The factors that determine pest population dynamics interact in complex
ways. This can make it difcult to obtain denitive evidence for individual
mechanisms from experiments or observational data. We also need to distin-
guish between factors that inuence the general abundance of a pest in farming
regions and those that are temporally and spatially explicit, i.e. which cause
a uctuation in pest population levels during the course of a cropping season
or within a single eld. These factors include environmental conditions,
intrinsic features of pest life history, intra-specic competition and interaction
with other species, particularly natural enemies. It is the combination of factors
affecting both the general level of abundance of a pest and its seasonal
population dynamics that ultimately determine whether and when a pest
population passes the point at which it becomes economically prudent to
introduce control measures.
Life history strategies
The life histories and reproductive strategies of organisms have evolved by
natural selection in response to their physicochemical and biological envi-
ronment. They are encapsulated in ecological theory by the concept of r and
K selection (MacArthur and Wilson, 1967; Statzner et al., 2001). In nature,
there is a continuum of strategies and r- and K-selecting strategies lie at either
extreme. The term r refers to the intrinsic rate of increase of an organism
while K refers to the carrying capacity of a population that is limited by
competition. Habitats can be r- or K-selecting.
Theory predicts that an r-selected population lives in an unstable, ephem-
eral or uctuating habitat that is free from competition, for example a weed
species that is adapted to colonize areas of bare ground. An r-selected indi-
vidual is one that reproduces rapidly and produces many offspring, with little
investment in each progeny. In contrast a K-selected individual has a low
reproductive rate but puts more investment in progeny (e.g. by producing
fewer but larger offspring and by protecting them from natural enemies). A
Pests of Crops 43
K-selected population lives in an environmentally stable habitat and will be a
good competitor. It may be able to survive, for example, in a nutrient-poor
environment (rust fungi that tolerate the harsh conditions on the phylloplane,
with little water and lack of nutrition, are K-selected organisms) or with high
levels of predation and parasitism, whereas an r-selected population will
occur in an unstable habitat and is a poor competitor.
This concept provides a valuable way of thinking about how adaptation
and natural selection results in particular patterns of birth, reproduction and
death and is thus highly relevant in ecologically based pest management.
Where an organism sits on the r- and K-selection continuum depends on the
conditions of its environment and competition with other individuals. Plant
pathogens such as Rhizoctonia and Pythium that attack seedlings or weakened
plants are r-selected, for example. Any biocides applied against them will
have to be fast-acting to cope with a rapidly developing pest population.
Alternatively, a control measure could be put in place that limits the develop-
ment of an r-selected pest population by providing it with high levels of com-
petition. Such a strategy is used for the control of some plant pathogens by
using antagonistic microbes that compete for soil resources. Some perennial
crops such as fruit orchards can attract K-selected pests. In these circum-
stances ecological theory predicts slower-acting therapeutic agents could be
used, but that trying to prevent pest build-up by introducing competitors is
unlikely to be successful.
Factors that naturally limit pest populations
Physicochemical conditions
The physicochemical conditions of an environment help determine the occur-
rence and abundance of all living things including the properties of soil or
water (pH, salinity), climate (temperature, rainfall, radiation) and weather.
Most species of agricultural pests are poikilothermic (cold blooded) and tem-
perature has a major impact on where they live and the rate at which their
populations develop during the year. The effect of temperature on the devel-
opment of poikilothermic organisms follows a dened mathematical rela-
tionship that can be used not only to determine the minimum, optimum and
maximum temperatures for growth but also to identify how much thermal
energy is required to reach a particular developmental stage. This informa-
tion can be used to forecast times of peak pest activity and to target interven-
tions such as pesticide sprays or the application of crop covers.
Competition
Individuals of the same species have very similar resource requirements,
such as radiation (for photosynthesis), water, carbon dioxide, oxygen, min-
eral and organic nutrients, space or breeding partners. The supply of resources
in an environment is often limited, and hence individuals from the same spe-
cies will compete for them. This leads to intra-specic competition maintain-
ing the population density within certain limits. Competition also occurs
44 Chapter 2
between species. Ecological theory predicts that inter-specic competition
can result either in the exclusion of one species by another or in stable
co existence, dependent on the amount of niche differentiation between species
(Begon et al., 2006). This knowledge can lead to ecological solutions for pest
management, for example by adjusting crop planting density to outcompete
weeds or by the development of mathematical models that identify the best
time to remove weed plants from a eld.
Predation
As primary producers, crop plants are consumed by a wide range of
herbivorous organisms including insects, mites, molluscs, nematodes
and microorganisms. In turn, herbivores are consumed by carnivorous and
parasitic organisms. The natural enemies of crop herbivores form a large part
of the worlds biodiversity and perform a vital function in limiting the popula-
tions of crop pests. It has been estimated that each agricultural pest species
is fed upon by 50250 natural enemy species. This vast number represents
a highly valuable but underexploited resource for crop protection through
biological control.
Factors that cause an increase in pest population size
Resource concentration
Crops are usually grown as monocultures. This presents potential pests with
a concentrated resource, enabling them to increase their general level of
abundance before intra-specic competition regulates pest population den-
sity. Evidence for the resource concentration hypothesis comes from experi-
ments showing that phytophagous insects occur at denser populations in
pure stands or larger patch sizes of plants (Root, 1973; Rhainds and English-
Loeb, 2003) and that specialist species of phytophagous insects are less ef-
cient at selecting a suitable host plant when it is growing in a diverse
background of other, non-suitable species (Finch and Collier, 2000). Introdu-
cing a new crop species to an area will have similar effects in that it provides
a new, concentrated resource for species able to exploit it. Genetically uni-
form crops, in which plant defences have been inadvertently removed
through breeding, will be more susceptible to pests than populations of wild
relatives. Ecological theory on the apparency of different plant types to herbi-
vores in natural ecosystems (Feeny, 1976) proposes that ephemeral plants are
protected to an extent because they grow unpredictably in both time and space
and thus are harder to locate. Therefore they are less likely to have evolved
physical and chemical defences. This suggests that plant species that are
exploited by humans as annual crops are more likely to be susceptible
to consumers than perennial species.
Agricultural disturbance
Many broad-acre crops rice, wheat, maize, cotton, soya are planted once
in a year in a particular eld. Other annual crops such as eld vegetables,
Pests of Crops 45
which are eaten fresh, are planted in sequential blocks within a eld system in
order to provide continuity of supply throughout the season. Both agronomic
situations create an ephemeral and ecologically unstable environment. For
example, after the ground has been made bare after ploughing, it is vulner-
able to colonization by r-selected weed species that grow from the weed seed
bank in the soil. A colonizing weed species that is able to grow in the newly
disturbed habitat and has a high rate of reproduction can quickly build up to
pest levels.
The perturbations associated with agricultural production also have a
destabilizing effect on the relationships between pests and their natural ene-
mies. Inappropriate use of broad-spectrum chemical pesticides can lead to
resurgence in a pest population when the same pesticide spray kills natural
enemies. The effects may vary depending on whether the natural enemies
are generalists or specialist on one particular prey type. Generalist natural
enemies are effective at preventing population outbreaks when the prey pop-
ulation is at a low level, whereas specialist natural enemies tend to dominate
the regulation at high prey densities (Hesketh et al., 2009). The population of
a specialist natural enemy is dependent on that of a particular prey species,
leading to a lag between the reproduction of the prey and the natural enemy
that creates a cyclical or boom-and-bust population pattern for both. Eco-
logical theory indicates that stochastic effects associated with abiotic factors
(e.g. changes in weather or other forms of environmental disturbance) can
shift a pest population from a stable, low level regulated by generalist nat-
ural enemies to a cyclical, dynamic state characteristic of specialist natural
enemies (Dwyer et al., 2004). Needless to say, farmers want to avoid cyclical
patterns of abundance of crop pests when the boom part of the pest cycle
results in damage to the crop above the economic threshold.
Changing physicochemical conditions
Agronomic practices designed to make the environment more favourable for
crop production can also make it more favourable for pests. This could
include improved irrigation and fertilization, which encourages the develop-
ment of weeds, or growing crops under protection with raised temperatures,
which encourages the development of invertebrate pests and plant patho-
gens. Stressing the crop, e.g. by drought, can also make it more vulnerable to
pests. Seedlings are less able than mature plants to withstand detrimental
changes to the physicochemical environment and as such are more vulnera-
ble to damping-off diseases, etc.
Alien species
Some of the most serious pest problems arise through alien (i.e. non-native or
non-indigenous) species being introduced accidentally to a new country or
continent. About 10% of alien species establish and spread from their origi-
nal point of introduction, and of these approximately 10% cause signicant
economic or ecological damage. More than 11,000 alien species have been
documented in Europe alone, for example (DAISIE, 2009). Economic losses
to crops from alien invertebrates, pathogens and weeds are estimated at
46 Chapter 2
?4.5 billion per annum in the UK (approximately ?75 per person), ?55 billion
for the USA, ?4.5 billion for Australia and ?72 billion for India (Pimentel
et al., 2001). Wheat yellow rust fungus Puccinia striiformis, for example, was
accidentally imported into Australia in the late 1970s and had a major impact
on wheat production as it established and spread through the country.
Serious losses to European crop production have occurred since the early
1990s from alien insect pests, such as the western ower thrips F. occidentalis
and the silver leaf whitey Bemisia tabaci (Table 2.5).
The seriousness of alien invasive species can be illustrated by looking in
more detail at a single example. In North America, the western corn rootworm
(WCR), Diabrotica virgifera (Coleoptera), is a major pest of maize (Gray et al.,
2009). The larvae feed on roots of maize and some other grass species and the
adults feed on the foliage and pollen. The pest originates in Guatemala, where
it has been known for around 5000 years, and is thought to have spread and
become a serious problem with the advent of intensive maize monoculture
systems introduced by Spanish colonizers. It was resident in the western part
of the US Great Plains in the 1870s and has since spread east to occupy about
half the land mass of the USA with a rapid range expansion after World War
II as maize production increased. WCR used to be controlled successfully by
crop rotation with soybean, although insecticide treatments were still
required and over US$1 billion was spent annually on its control in the USA.
In 1995 a population in Illinois evolved that had lost delity to maize and
was able to survive on soybean (Gray et al., 2009). This new variant has spread
within the USA. Farmers were then forced to switch their management
practice towards use of insecticides and transgenic Bt maize. WCR has
Table 2.5. Alien invasive insect pest of importance in Europe. (From DAISIE, 2009.)
Species Common name Threat
Aphis gossypii (Hemiptera) Melon and cotton aphid Polyphagous pest of vegetable crops
and citrus
Bemisia tabaci (Hemiptera) Silver leaf whitey Polyphagous, serious pest of edible
horticultural crops and ornamentals
Ceratitis capitata (Diptera) Medy Larvae develop in wide range of
fruits
Diabrotica virgifera
(Coleoptera)
Western corn rootworm
Larvae feed on roots of maize
Frankliniella occidentalis
(Thysanoptera)
Western ower thrips Pest of outdoor and protected
horticultural edible crops and
ornamentals
Leptinotarsa decemlineata
(Coleoptera)
Colorado potato beetle Pest of potato crops
Liriomyza huidobrensis
(Diptera)
South American leaf miner Larvae feed on wide range of hosts
especially vegetables and
ornamental plants
Spodoptera littoralis
(Lepidoptera)
Cotton leaf worm
Larvae feed on cotton, fruits and
vegetable and ornamental crops
Pests of Crops 47
developed resistance to certain insecticides, making Bt maize the most
viable option. WCR was accidentally imported to Belgrade airport in 1992,
probably as a stowaway, and established in local maize elds. Since then it
has spread to 20 European countries. Currently it is controlled in Europe
using rotation with a non-host crop. However, it is now known that multiple
introductions have occurred. This increases the risk that an introduction
of the rotation-resistant variant will occur in Europe. This could create a
dilemma because the current optimal strategy for WCR control is Bt maize,
but there is resistance from the public to growing genetically modied (GM)
crops in Europe. Research is being done on biological control, which is consid-
ered to be a potential market for organic maize and maize seed production
elds. Elsewhere farmers rely on insecticides. However, there is a concern that
farmers in the USA and Europe have largely abandoned basic IPM practices
for maize and that this is likely to create problems for the future, such as
insecticide resistance (Gray et al., 2009).
Alien pests can also damage native habitats by excluding other species,
causing a loss of habitat for animals and microbes, altering plant community
succession and interfering with the normal interactions of plants and other
organisms, such as pollinating insects. Accidental introductions of some alien
pest species have resulted in wholesale change in plant communities. For
example, invasion of rangeland areas of the Midwest and western USA by
cheatgrass, an annual grass, has resulted in the loss of much of the native
sagebrushbunchgrass range. In eastern North America, invasion by three
insect species the hemlock woolly adelgid (Adelges tsugae), the gypsy moth
(Lymantria dispar) and the emerald ash borer (Agrilus planipennis) has caused
signicant damage to native forests over millions of hectares. These inva-
sions are proving difcult to control. For example, the hemlock woolly adel-
gid is expected to lead to the extinction of hemlock within a decade in some
areas such as the southern Appalachians. For all three of these forest pests,
invasion has resulted not only in major tree decline, but also signicant
effects at the community and ecosystem levels.
The success of alien invaders has often been explained in terms of escape
from the natural enemies that would regulate them in their native range
through inter-specic competition. However, formal support for the hypoth-
esis was thin until two recent meta-studies of the scientic literature. Torchin
et al. (2003) compared the parasites of exotic animal species in their native
and introduced ranges. They found that the number of parasite species affect-
ing native populations was twice that of exotic populations and the propor-
tion of infected individuals was lower in introduced versus native populations.
Mitchell and Power (2003) examined fungal, oomycete and viral pathogens
of exotic plants in their native and introduced ranges. They showed that
exotic populations had 84% fewer fungal and oomycete pathogen species
and 24% fewer viral species than in their native range. Both studies lend clear
support to the enemy release hypothesis. However, introduced species do
not escape regulation by inter-specic competition entirely. In their analysis
Mitchell and Power (2003) also found support for the biotic resistance hypoth-
esis, which proposes that the invasiveness and impact of an alien species can
48 Chapter 2
be limited by competition with native species including natural enemies. A
negative relationship was found between the noxiousness of exotic agricul-
tural weeds and the number of pathogen species they had accumulated in
the new range. Thus acquiring natural enemies in a new range can impact on
invasiveness.
The natural enemies escape hypothesis leads to the obvious conclusion
that introducing natural enemies from their original home range to the new
area can counteract alien, invasive pests. This is a form of biological control
known as classical control. However, escape from natural enemies is not the
only explanation for the success of invasive species. The probability of suc-
cessful invasion depends on a complex interaction between the characteristics
of the habitat in which the alien species is introduced as well as the biological
traits of the alien itself. These interactions vary on a case-by-case basis,
although some general factors that contribute to the probability of invasion
success other than natural enemy escape include: (i) the evolutionary history
of the resident community (i.e. the idea that communities with intense com-
petition will be resistant to invasions); (ii) community structure; (iii) the level
of natural disturbance; and (iv) human activity such as pollution, local extinc-
tion of native species and accidental dispersal of alien organisms on vehicles
(Radosevich et al., 2007).
Emerging pests
Pests new to production agriculture can arise through the evolution of new
pest strains. Increased reliance on a small number of pesticides and the
widespread growth of crop species with limited genetic diversity are increas-
ing the selective pressure for new pest strains to evolve. New strains can also
evolve to overcome plant defence mechanisms. A new strain of the wheat
stem rust fungus Puccinia graminis f.sp. tritici, termed Ug99, evolved in
Uganda in 1999. It is now spreading towards Asia and Europe. It is able to
overcome the resistance gene bred into standard wheat lines and as a result
it is highly virulent, capable of causing 100% yield loss (Mackenzie, 2007).
The potato blight oomycete P. infestans is a pathogen that can reproduce
asexually and sexually. Sexual reproduction requires the presence of two
mating types in the oomycete population. The pathogen that was acciden-
tally introduced into Europe in the 1800s from its original home in Mexico
consisted of just one genetic strain, i.e. a single mating type (Goodwin et al.,
1994). Unfortunately, the second mating type was introduced into Europe in
1976, facilitating sexual recombination in the species and as a result new
strains of the pathogen have evolved. Some of these have increased aggres-
siveness to host plants and there are concerns that pesticide resistance may
develop more rapidly.
Economic Thresholds
Understanding the factors that limit pest populations or which cause them to
proliferate can inform us about suitable management approaches. This needs
Pests of Crops 49
to be combined with economic thresholds to decide when to apply a pest
treatment. It is self-evident that the nancial costs of controlling a pest must
be less than the benet obtained in terms of improved crop yield or quality.
The aim is rarely to eradicate a pest population; rather it is to manage it so
that the population is maintained below the economic injury level. This is
formally described as the pest population density at which the cost of pest
damage equals the cost of the available control measures. On paper, the eco-
nomic injury level represents the point at which it becomes nancially viable
to use pest management methods. It is normally thought of in terms of reme-
dial treatments for pests (pesticide sprays, for example), but as a concept it
applies equally to preventive treatments. In practice, once a pest population
has reached the economic injury level it is usually already too late to apply
the control measure, because it takes time for a control programme to work.
The key decision metric in a pest management programme, therefore, is the
economic threshold, which is the density of the pest where control measures
must be exerted in order to prevent it reaching the economic injury level. The
economic threshold is determined in essence by a costbenet analysis
(Mumford and Norton, 1984). Economic thresholds have been important in
the implementation of effective supervised pesticide spray programmes and
they should be equally valuable in IPM. However, because they rely on
detailed monitoring of pest populations and mathematical models of pest
population dynamics they have been criticized, reasonably, for being too com-
plicated and unwieldy for many farmers to implement (Orr, 2003; Rodriguez
and Niemeyer, 2005). This criticism was made mainly in relation to resource-
poor farmers in developing nations, but it is true to say that many farmers in
the Global North also do not use formal, research-derived economic thresh-
olds, although nearly all farmers scout their crops for evidence of pests and
act accordingly. The most sophisticated economic threshold systems are used
in high-value, labour-intensive crops that are subject to intense pest pressure
and are heavily dependent on external inputs. In the Global North these
would typically be greenhouse crops such as glasshouse salads, ornamentals
and some soft fruit such as tunnel-grown strawberries, while in the Global
South this would usually be horticultural edible and ower crops grown by
large commercial operations for the export market.
Crop Protection Methods Used in Integrated Pest Management
In the past, under the industrial farming paradigm, the standard way of
managing pests was by the application of chemical pesticides with little
regard to the reason why the pest was present, the amount of crop injury
being caused or the costs to the environment. Chemical pesticides were cheap
and effective enough to make this an economically viable strategy. This is
clearly no longer the case. From the information presented so far in this book,
it should be apparent that the strategy used to control a particular pest should
have a rm evidence base, i.e. it should be tailored according to the cause of
the pest outbreak. Synthetic chemical pesticides have a vital role to play in
50 Chapter 2
modern crop protection, but they should be integrated with other methods in
order to reduce the onset of resistance and, of course, to reduce harm to the
environment and to people.
Although the crop protection industry is dominated in market size terms
by conventional synthetic pesticides, there are a wide range of alternative
methods that are being used increasingly by farmers and growers (in the
context of this book, we use alternative in the sense of giving farmers and
growers a choice of different crop protection methods). These methods are
commonly referred to in the literature under the following categories.
Modern selective pesticides
New knowledge on pest biochemistry, coupled with approaches such as
molecular engineering and targeted screening for active compounds, have
produced new synthetic pesticide compounds with far better environmental
and human safety proles than the old chemistry of the 1950s and 1960s.
Good examples of modern chemistry include synthetic insect growth regula-
tors such as buprofezin and pyriproxyfen, which have high levels of selectivity,
low mammalian toxicity and are classed by regulators as low-risk com-
pounds (Grafton-Cardwell et al., 2006). These new compounds are very
important for crop protection (for a good review see Smith et al., 2008). The
development of new actives is a complex process involving the screening
and characterization of a wide array of candidate molecules. Increasingly,
these pesticide development programmes target specic sites within the cells
and organelles of the pest organism. A huge array of bioactive molecules is
synthesized in nature, and hence chemists are turning more to natural prod-
ucts as the leads for pesticide screening. In addition, the whole genomes of
pest species are starting to be sequenced and this is paving the way for iden-
tifying new targets through comparative genomics and transcriptomics.
However, as we have described previously in this book, the development of
new synthetic pesticides is slow and expensive, and the benets of a new
compound may be lost quickly if pesticide resistance evolves. Thus, it is
imperative to use new chemistry within an IPM framework that incorporates
resistance management. Unfortunately, as we shall see shortly, most farmers
still do not practise IPM and this is undoubtedly wasting the opportunity to
get the full benets from modern pesticides.
Cultural practices
Cultural methods of pest control involve changing the way a crop is grown
in order to reduce or avoid pest damage. Crop rotation is one of the oldest
strategies for managing pests and is particularly useful for controlling pest
species with limited dispersal ability and host range (Minnis et al., 2002).
Rotation with non-host crops can break a plant pathogens life cycle. Crop
rotation may prevent the build-up of weed species that are adapted to any
single crop or cropping system (Bond and Grundy, 2001). Other cultural
control methods involve good crop management, such as destruction of crop
residues, and careful choice of planting date to avoid key periods in pest life
cycles, such as the laying of insect eggs (Ellis et al., 1987). Techniques such as
Pests of Crops 51
intercropping, undersowing and companion planting may also reduce
colonization by certain insects, pathogens and weeds (Theunissen and
Schelling, 1996; Finch and Collier, 2000; Bond and Grundy, 2001).
Physical methods
Physical control methods are non-chemical/non-biological measures that
destroy the pest, disrupt its development or activity, or modify the environ-
ment to a degree that is unacceptable or unbearable to the pest (Vincent et al.,
2003). Examples include the use of mechanical weeders or growing crops
under covers or with mulches. Mechanical in-crop weeding is possible in
crops with wide row spacings (e.g. horticultural crops but not arable crops)
and developments continue to be made in vision guidance systems for greater
precision and intra-row weed control (Bond and Grundy, 2001).
Natural compounds
Living organisms produce a wide variety of molecules that can be used in
pest management, such as biocidal compounds extracted from plants (often
referred to as botanicals) or insect or plant signalling molecules
(semiochemicals). Some plant compounds, such as pyrethrum, have been
used as natural pesticides for many years although compared with syn-
thetic pesticides they are relatively unstable, have lower potency and
greater price. Some new, highly effective pesticides are based on natural
products from microorganisms, such as the insecticide Spinosad. Insect
pheromones are used widely to monitor insect populations and are being
used increasingly to control pest populations by disrupting the ability of
insects to nd mates.
Plant breeding
New crop cultivars with total or partial resistance can be bred using conven-
tional methods or with genetic modication technology. Plant breeding can
enhance plant resistance to pests, and considerable efforts are expended each
year to develop new resistant varieties. There is some effort to breed for resis-
tance against invertebrate pests, but most of the work has been done with
developing varietal resistance against pathogens. Many hundreds of patho-
gen resistance genes have been identied in crop species. Unfortunately,
most resistance conferred by single plant genes does not remain available for
long because of the ability of many pathogens to overcome plant resistance
through natural selection (Pink et al., 2008). Pathogen resistance that is deter-
mined by several plant genes tends to be more durable than single gene resis-
tance. However, it is more difcult to handle in a breeding programme and is
often partial, i.e. some disease still develops. The technical difculties of dealing
with multi-gene resistance are now being overcome with new technology
such as marker-assisted breeding (Collard and Mackill, 2008). Partial resis-
tance may not be an issue if some yield reduction is acceptable. However, in
fruit and vegetables, where marketable yield is determined by quality, any
disease blemishes may be unacceptable. Therefore it is vital that partial
52 Chapter 2
resistance is used as part of an IPM programme to reduce pest damage to
acceptable levels.
Biological control agents
For the purposes of this book, biological control is the use of living organisms
to suppress the population of a specic pest organism, making it less abundant
or less damaging than it would otherwise be (Eilenberg et al., 2001). The
organisms used as biological control agents include predatory insects and
mites, parasitoids, parasites and microbial pathogens and antagonists (Bel-
lows and Fisher, 1999; Bale et al., 2008). In Europe and North America, typical
examples of where these agents are being used include: (i) the application of
parasitoids to control whiteies in glasshouses; (ii) parasitic nematodes against
slugs; (iii) mycoparasitic fungi to control plant diseases of horticultural crops;
(iv) use of viruses to control codling moth in apple orchards; and (v) building
habitats on farms to increase natural populations of predators and other bene-
cial organisms. The ways in which biological control agents are used vary
according to the type of pest (plant, microorganism, vertebrate or invertebrate),
the biological characteristics of the control agent, as well as the agricultural set-
ting. There are three broad biocontrol strategies: (i) introduction (release of an
alien control agent to control an alien pest); (ii) augmentation (application of
natural enemies that already live in the area of use); and (iii) conservation
(manipulating agricultural practices or the environment to enhance natural
control).
Biopesticides
There is no universally recognized denition, but in general terms biopesti-
cides are mass-produced, biologically based agents manufactured from living
microorganisms or natural products that are sold for the control of plant
pests (Copping and Menn, 2000). In some countries, such as the USA, bio-
pesticides also include GM plants expressing introduced genes that confer
protection against pests or diseases (so-called plant incorporated protectants).
Some authors consider that mass-produced macro biological control agents
(predatory insects, parasitoids, nematodes) are also biopesticides (e.g. Waage,
1997). While this is undoubtedly correct as a scientic description, most reg-
ulatory agencies reject this view. Governments have tended to use different
legislative approaches for macro biocontrol agents and microbial agents/
natural products.
Genetic methods
The mass production and release of sterile male insects as a mating dis-
ruption strategy has proved very effective against some pests, such as
screw-worm and fruit ies. It involves the release of very large numbers
of sterilized insects into the vicinity of the crop, so that they will mate
with resident insects and so prevent them producing young. The insects
to be released are sterilized using irradiation or chemicals. The release
ratio ranges from 10:1 up to 100:1 sterile to wild insects. The technique is
expensive, mainly because large numbers of insects must be reared and it
Pests of Crops 53
usually requires releases over large areas. It has been used successfully to
eradicate the screw-worm y (Cochliomyia hominivorax) in areas of North
America. There have also been many successes in controlling species of
fruit ies, most particularly the medy (Ceratitis capitata) (Hendrichs
et al., 2002).
Because this book focuses on biopesticides, it is not our intention to go into
detail about other, alternative methods of pest control. However, crop protec-
tion practitioners, regulators and others who work with biopesticides need
to have a thorough understanding of other crop protection methods in order
that the best use can be made of biopesticides within IPM. For further infor-
mation on crop protection technologies, readers should consult Smith (1995),
Agrios (2005) and Radcliffe et al. (2008).
It is worth pointing out some potential aws and pitfalls in the way crop
protection agents are currently categorized. Some of the categories listed
above clearly overlap. Microbial biopesticides, for example, are also biological
control agents. New synthetic pesticides may be based on the molecular
structure of natural compounds. Unfortunately, there are no universally
agreed denitions for many of the crop protection approaches used around
the world. Take biological control, for example. In this book, we are sticking
with a traditional view of biological control as requiring the use of living
organisms. However, some authors consider it to include genes and gene
products. Thus the US National Academy of Sciences (1988) describes bio-
logical control as the use of natural or modied organisms, genes or gene
products to reduce the effects of undesirable organisms (pests) and to favour
desirable organisms such as crops, trees, animals and benecial insects and
micro organisms. According to this denition, biological control includes
agents such as GM organisms and natural products that have pesticidal
properties (e.g. neem oil) or can modify pest behaviour (e.g. insect phero-
mones). Crop varieties modied genetically to express the insecticidal protein
from Bacillus thuringiensis could be categorized as plant breeding, as a biope-
sticide or as biological control. Some biological control experts are happy
with the expanded denition of biological control, while others think it loses
the original emphasis on applying theories about interactions between species
and their natural enemies. Obtaining universally agreed denitions is impor-
tant because it affects how governments regulate crop protection agents and
how scientists and practitioners develop them.
Integrated Pest Management in Practice
The rst aim of IPM must be to use chemical pesticides at a sustainable level
without causing unacceptable loss of crop yields. However, in order to keep
up with the increase in global food production that will be required in the
next 20 years, IPM will need to be capable of moving to the next level fairly
rapidly, namely to enable yields to be increased while still keeping use of
pesticides and other inputs at sustainable levels. Can IPM deliver? In a
54 Chapter 2
groundbreaking study, Pretty (2008) analysed data from 62 IPM projects in 26
industrialized and developing countries, covering over 5 million farm house-
holds farming 25 million ha. His analysis indicates that IPM is successful in
most cases. Only one out of the 62 IPM projects resulted in an increase in
pesticide use and an associated decline in yields. Over 60% of the IPM proj-
ects resulted in a reduction in pesticide use (average reduction of 75%) and
an increase in yields (average yield increase of 40%). An additional 15% of
projects resulted in an increase of both yield (average 45% increase) and pes-
ticide use (average 20% increase). These were mainly conservation farming
projects that incorporated zero tillage to conserve soils and reduce water pol-
lution and they tended to result in greater use of herbicides for weed man-
agement. Approximately 20% of the IPM projects resulted in a slight reduction
in yield (average 5% reduction) and lowered pesticide use (average 60%
reduction). These mainly consisted of cereal production projects in Europe.
So if IPM is successful, are many farmers using it on the ground? Figures
for the estimated area of crops currently under supervised control and IPM
in Europe for different crop types are given in Table 2.6 (Bale et al., 2008).
Table 2.6. Supervised and integrated control programmes used in Europe.
(From Bale et al., 2008.)
Crop Type Elements
Area under IPM in
Europe/reduction
in pesticides on
that area
Field
vegetables
Supervised Monitoring; sampling; disease-resistant
crop varieties
5% of total area/
2080% reduction
Cereals Supervised Monitoring; sampling; forecasting;
resistant crop varieties
10% of total area/
2050% reduction
Maize Integrated Mechanical weeding; resistant crop
varieties; biological control of insects
4% of total area/
3050% reduction
Vineyards Integrated Biological control of insects and mites;
disease-resistant crop varieties;
pheromone mating disruption
20% of total area/
3050% reduction
Olives Integrated Cultural control; biological control of
insects; disease- and insect-resistant
crop varieties; monitoring; sampling;
pheromones
Very limited
Orchards Supervised Monitoring; sampling; selective
pesticides
15% of total area/
30% reduction
Integrated Monitoring; sampling; pheromone
mating disruption; biological control;
disease-resistant crop varieties
7% of total area/
50% reduction
Greenhouse
vegetables
Integrated Monitoring; sampling; biological control
of insects, mites and diseases;
disease-resistant crop varieties; selective
pesticides
30% of total area/
5099% reduction
Pests of Crops 55
The data show that few farmers use IPM, although there are exceptions, such
as greenhouse growers in the UK and the Netherlands. A lot of research has
been done on IPM since the mid-1980s, so the fact that most farmers have yet
to adopt it raises major issues about how research can be translated into
farmer practice. The degree to which IPM has been adopted and is successful
(i.e. leads to reductions in pesticide use and still maintains yield) varies sig-
nicantly according to the type of crop grown. Crop protection tactics have
to be chosen that are appropriate not only to the crop plant, but also to the
physical area of production, the type and number of pests, and the physical,
chemical and biological environments. Different tactics must also be capable
of being integrated, and they must be affordable for the farmer. It is not sur-
prising that IPM is most advanced in high-value glasshouse crops, such as
fresh salads or ornamental plants. For these crops, growers can afford to spend
comparatively large sums on crop protection (including labour-intensive
methods such as spot-treating individual plants). There are also strong driv-
ing forces to make IPM work in the form of a signicant pesticide resistance
problem, extremely high quality standards from retailers, and pressure from
consumers and others to use fewer pesticides. In contrast, producers of out-
door broad-acre crops such as cereals, potatoes and cotton have much less to
spend on pest management per unit area of crop, and have to work in a much
more challenging physical and ecological environment.
Integrated pest management in greenhouse crops
The global area of crop production done in greenhouses (which include
glasshouses, polythene tunnels and other forms of protective structure) is
estimated at around 2.4 million ha, of which around 45,000 ha is done in
glasshouses (van Lenteren, 2006). Greenhouse growers are able to produce
high-value crops on a small area of land. Unfortunately, greenhouse crops
also provide an excellent environment for pest insects, mites and plant patho-
gens. Pesticide resistance evolved in some key glasshouse pests as long ago
as the 1960s, prompting the early development of biocontrol. This was fol-
lowed by the widespread adoption of bumblebees for pollination, which
required growers to stop using broad-spectrum insecticides. Growers of
greenhouse edible crops are also under severe pressure from retailers to
deliver produce with zero detectable pesticide residues because of consumer
concerns about residue safety (Pilkington et al., 2010).
Some very sophisticated and effective IPM programmes have been devel-
oped for glasshouse crops (Table 2.7). These were mainly instigated through
publicly funded research and involved close working between research sci-
entists, growers and industry. We would class these as Level Four IPM accord-
ing to the Prokopy scale (Prokopy, 1993). In Europe, IPM is used in over 90%
of glasshouse tomato, cucumber and sweet pepper production in the Nether-
lands (van Lenteren, 2000) and is standard practice for glasshouse crops in
the UK. In Almeria, Spain, the area under IPM has increased from just 250
ha in 2005 to around 7000 ha in 2008, while the proportion of the Dutch
56 Chapter 2
chrysanthemum crop grown under IPM has increased from just 1% in 2002 to
80% in 2007 (R. GreatRex, Syngenta Bioline, personal communication). Glass-
house IPM uses a combination of biological and physical controls, selective
pesticides and resistant varieties, with very careful monitoring of pest popu-
lations to determine when they have passed the economic threshold. This
system requires considerable knowledge on behalf of the grower but it has
been adopted widely because it has clear benets. These include reliable pest
control, lack of phytotoxic effects, better fruit set and the fact that because
synthetic pesticides are used sparingly operators do not have to be excluded
from the glasshouse after spray applications so often. Unlike for synthetic
pesticides, there is no statutory interval between the application of preda-
tors/parasitoids and harvesting the crop, while for biopesticides the harvest
interval tends to be very short. This means that these agents can be used right
Table 2.7. Integrated pest and disease management programme as applied in tomato in
Europe. (From van Lenteren, 2000.)
Pest/disease
Method used to prevent or control
pest/disease
Pests
Whiteies (Bemisia tabaci, Trialeurodes
vaporariorum)
Parasitoids: Encarsia, Eretmocerus
Predators: Macrolophus
Pathogens: Lecanicillium, Paecilomyces,
Aschersonia
Spider mite (Tetranychus urticae) Predators: Phytoseiulus
Leaf miners (Liriomyza bryoniae, Liriomyza
trifolii and Liriomyza huidobrensis)
Parasitoids: Dacnusa, Diglyphus, Opius,
natural control
Lepidoptera (e.g. Chrysodeixis chalcites,
Lacanobia oleracea, Spodoptera littoralis)
Parasitoids: Trichogramma
Pathogens: Bacillus thuringiensis
Aphids (e.g. Myzus persicae, Aphis gossypii,
Macrosiphum euphorbiae)
Parasitoids: Aphidius, Aphelinus
Predators: Aphidoletes, natural control
Nematodes (e.g. Meloidogyne spp.) Resistant and tolerant cultivars, soil-less
culture
Diseases
Grey mould (Botrytis cinerea) Climate management, mechanical control,
selective fungicides
Leaf mould (Fulvia = Cladosporium) Resistant cultivars, climate management
Mildew (Oidium lycopersicon) Selective fungicides
Fusarium wilt (Fusarium oxysporum lycopersici) Resistant cultivars, soil-less cultures
Fusarium foot rot (Fusarium oxysporum radicis/
lycopersici)
Resistant cultivars, soil-less culture, hygiene
Verticillium wilt (Verticillium dahliae) Pathogen-free seed, tolerant cultivars,
climate control, soil-less culture
Bacterial canker (Clavibacter michiganesis) Pathogen-free seed, soil-less culture
Several viral diseases Resistant cultivars, soil-less culture, hygiene,
weed management, vector control
Pollination Bumblebees or bees
Pests of Crops 57
up to harvest, which is a considerable benet when the produce quality stan-
dard demanded by retailers is so high. Most of the biological control used in
glasshouses is concerned with managing insect and mite pests. Some micro-
bial biopesticides are available against plant pathogens and can be integrated
with selective pesticides but a greater range of products is required. Many of
the main plant diseases are tackled currently using resistant crop cultivars,
although an increasing number of effective microbial antagonists are becom-
ing available. Typically, selective synthetic chemical insecticides and acari-
cides will be used at the start of the season as a clean-up for insect and mite
pests before switching to inundative applications of predators, parasitoids,
parasitic nematodes and insect pathogens. Short-persistence pesticides
are used on an at-need basis to knock back pest populations if they start to
outstrip the ability of the biological control agents to regulate them.
Integrated pest management in eld vegetable crops
Retailers and consumers in the industrialized countries increasingly demand
vegetables that are relatively uniform in size and shape and free from blem-
ishes and pest-related debris. Field vegetables generally have a higher value
than cereals, but a lower value than glasshouse crops. Because of the emphasis
on quality, the risk of producing an unmarketable crop is relatively great.
Vegetable growers are, therefore, generally risk averse. Pesticides remain the
mainstay of crop protection for many vegetable crops. Most of the crop pro-
tection is based around supervised spraying of pesticides or there may be
some integration of different tactics to control an individual pest species,
which we would class as Level One IPM. Other components of IPM that are
in use in eld vegetables include crop rotation (with some exceptions), good
crop management (removal of plant residues, application of fertilizers and
irrigation) and adjustment of planting or harvesting dates (USDA, 2001).
This may involve the use of pest or disease forecasts (Gilles et al., 2004).
Growers walk their crops regularly and make decisions based on their nd-
ings. In the USA, research-based economic thresholds are available for a
range of crops; however, they are used less often in Europe (Collier and
Finch, 2007). Pest- and disease-resistant cultivars are grown where available
and if the cultivars meet other market requirements. For example, lettuce
with resistance to downy mildew is grown widely. Use of physical methods
of pest control is increasing. Mechanical weed control can be effective and cov-
ers or mulches have been used to control pest insects and weeds; however,
most growers still rely on chemical herbicides for weed control, especially
glyphosate, which has a very good human safety and environmental prole.
Biological control with microbials or arthropods is relatively undeveloped.
This is due to a combination of factors: lack of environmental control and
problems of conning released natural enemies to the crop, the relatively
high cost of biological control methods compared with the value of the crop,
reduced and variable efcacy compared with pesticides, and the limited
research and development input in this area. However, there are some
58 Chapter 2
exceptional examples of Level Two IPM that indicate how things could be
done across much of the vegetable crops sector in the future. Notably, these
IPM systems have been driven by very much the same set of conditions
that has forced the development of IPM in glasshouse crops. IPM pro-
grammes for the production of tomato crops in Florida, for example, were
developed in response to pesticide resistance and severe secondary pest
problems with Liriomyza leaf miners caused by the use of broad-spectrum
insecticides sprayed against Spodoptera spp. caterpillars. The IPM system
that was developed uses pest monitoring and economic thresholds to
inform the application of foliar sprays of the bacterial insecticide Bacillus
thuringiensis (Bt), which is highly selective and preserves natural enemies
(Walker et al., 2003).
Integrated pest management in orchard crops
Retailers in the industrialized countries also have high quality standards for
orchard crops. Up until the 1970s, pest management in orchard crops relied
on calendar sprays of broad-spectrum pesticides, but pesticide resistance
became common in many of the key pests. The IPM strategies currently
used in orchards are a step forward from supervised pesticide spray pro-
grammes developed in the 1970s and 1980s, and are largely based on stop-
ping sprays of broad-spectrum pesticides and allowing natural enemies
to re-establish, such as the predatory phytoseiid mite, Typhlodromus pyri,
which is a key predator of the two-spotted spider mite, T. urticae, in apple
orchards (Blommers, 1994). The level of sophistication of the pest manage-
ment programme can vary widely from grower to grower, but in the last
decade there has been an increasing awareness of the benets of adopting
IPM by growers in many of the main producer countries. Pesticide sprays
are still essential tools for the majority of farmers, especially for the control
of diseases such as scab and powdery mildew, but progressive growers
are using disease forecasts in order to target spray applications better
(MacHardy, 2000). The development of some sophisticated decision support
tools (pest thresholds, monitoring and models) has allowed the targeted
application of selective insecticides, insect pheromones for mating disrup-
tion, microbial control agents and predators and parasitoids against aphids
and moth pests without harming predatory mites (Solomon, 1987; Mac-
Hardy, 2000; Cross and Berrie, 2006). This is combined with careful manage-
ment of sites away from the tree where pests overwinter or which act as pest
reservoirs, such as the soil, border areas and vegetation beneath the tree
canopy. Although monitoring has costs associated with it, successful grow-
ers nd that savings on reduced application of pesticides and other control
agents offset these. There is still much work to be done. For example, effec-
tive biopesticides are required for aphid pests and plant pathogens, many of
the main commercial crop varieties have low levels of disease resistance,
and there is a requirement for better integration of the different IPM
systems used for individual pests and diseases.
Pests of Crops 59
Integrated pest management in broad-acre crops
There have been signicant problems since the 1950s with the over-use of
synthetic chemical pesticides in broad-acre crops including cereals, maize
and cotton. In some well-documented cases, such as cotton production in the
Canete valley of Peru, this has included complete failure to control insect
pests following the rapid evolution of pesticide resistance (Thacker, 2002).
Broad-acre crops generally have high economic thresholds for pest manage-
ment interventions, meaning that low densities of many pests can be toler-
ated (the exceptions are for pre- and postharvest fungal diseases, some of
which pose a serious hazard to human health). There is, therefore, good
scope for IPM, but it is not yet being used widely. For example, it is estimated
that only 10% of cereal production is done under IPM (van Lenteren, 2008).
The majority of schemes are based on host-plant resistance and forecasting/
monitoring to guide pesticide applications, rather than on biological control.
An exception is the use of the parasitoid Trichogramma to control outbreaks of
the European corn borer, Ostrinia nubilalis, on maize (Burn, 1987). As we will
discuss later in this book, since the beginning of the 21st century maize and
cotton production has been revolutionized by the commercialization of GM
varieties that express a gene from the entomopathogenic bacterium
B. thuringiensis, which codes for a selective, insecticidal protein that kills lep-
idopteran pests. This protein is safe for mammals and other vertebrates and
does not affect the arthropod natural enemies that occur in maize and cotton
elds. It has been taken up widely by farmers in many regions of the world
with the exception of Europe, where there are deep-seated societal concerns
about GM crops. Similarly, weed control has changed greatly since the intro-
duction of GM, herbicide-resistant crops in 1996. Most of these crops
have been engineered to be resistant to glyphosate. Over 80 million ha of
herbicide-resistant crops were grown in 2006 (Gianessi, 2008). Most of these
crops are maize, canola (oilseed rape), soybean or cotton. For example, 80%
of US-grown cotton is now resistant to glyphosate. Because glyphosate is a
broad-spectrum herbicide, the development of glyphosate-resistant crops
has simplied weed control by enabling the farmer to use just the one type of
herbicide during production and lowering the number of sprays that have to
be applied including the use of pre-emergence herbicides. Glyphosate has a
low toxicity to mammals and other vertebrates and, because it is readily
adsorbed by soil, there is little risk of it leaching into groundwater (Bayliss,
2000). Even though glyphosate-resistant crop seed is sold to farmers at a pre-
mium price, this is offset by reduced costs from herbicides and mechanical
weed control and higher yields due to better weed management. The global
cumulative farm income benet from herbicide-resistant crops for the period
19962005 is estimated at over US$19 billion (Gianessi, 2008). Resistance to
glyphosate is still relatively rare considering the extent to which it is used, and
so far only 18 resistant weed species have been documented (WeedScience.
com, 2010). However, given the large-scale uptake of glyphosate-resistant
crops, there are concerns that there will be increased selection pressure for
resistance in weed populations. Hence the recent development of glyphosate
60 Chapter 2
resistance in two important weeds of soybean, Sorghum halepense and Euphor-
bia heterophylla, in glyphosate-resistant soybean elds in South America is
something of a worry (Vila-Aiub et al., 2008).
In Europe, the use of conservation biological control methods, such as
wildower headlands and beetle banks, is promoted through various agri-
environment schemes but in the UK, for example, most of these have had a
very low uptake (Boatman et al., 2007). There is greater use of IPM techniques
within organic arable production, but even here there is limited use of bio-
logical control, with the majority of integrated crop management schemes
relying on improved monitoring and reduced applications of approved
chemical controls (MacKerron et al., 1999). This is not to say that IPM cannot
be made to work on broad-acre crops. If the correct research is nanced, done,
and translated into practice, then IPM is possible. As an example of what
can be achieved, a highly successful programme for management of the
whitey B. tabaci was implemented on cotton in Arizona in 1995 (Naranjo
and Ellsworth, 2009a,b). The programme relies on decision support tools
based on pest sampling and economic thresholds for the targeted application
of selective insecticides, including insect growth regulators such as bupro-
fezin and pyriproxyfen. The use of these insecticides controls outbreak popu-
lations of the whitey and preserves natural populations of arthropod
predators, which typically consist of about 20 different taxa and which sup-
press the whitey population below the economic threshold for up to a year
after spraying (Naranjo and Ellsworth, 2009a,b). The system has now been
integrated with the planting of GM Bt cotton for control of the principal
lepidopteran pest, pink bollworm, Pectinophora gossypiella. It has resulted in a
70% reduction in the use of foliar insecticides together with control cost savings
of over US$200 million in the 14 years from 1995 to 2009.
Integrated pest management in developing countries
Farmers in developing nations face different constraints and opportunities
compared with their counterparts farming in industrialized countries. Sub-
sistence farmers in sub-Saharan Africa, Asia and Latin America, for example,
operate on narrow economic margins in an ecological environment where
crop production is severely constrained by environmental factors such as
water availability and soil fertility. These farmers often cannot afford pesti-
cides and other inputs and it is important that improvements are made to
basic agronomy before IPM can be considered seriously (Way and van Emden,
2000). This is not to say that IPM has no role here, but it must be suitable and
workable for local needs. Where farmers in developing nations are less con-
strained by access to resources, then the full spectrum of IPM tactics outlined
earlier in this book has much to offer providing that they are affordable. Self-
evidently, IPM must be tailored to the needs of local farming communities; it
is not a case of simply transferring an IPM model from the Global North to
the Global South. That, very clearly, could never be justied on economic,
environmental, agronomic or social grounds. Although it is not the focus of
Pests of Crops 61
this book, we must not lose sight of the fact that there is a deep connection
between the development of IPM and issues of social justice, fair trade, the
development of an effective policy environment (many developing countries
lack clear policies on IPM), access to loans and subsidies for IPM and other
tools, and improvements to the market infrastructure such as better roads
and transport for agricultural produce.
Historically, many farmers in developing countries have suffered the
same problems associated with uncontrolled pesticide use as elsewhere,
namely the rapid evolution of pesticide resistance, resurgence, problems of
secondary pests and environmental pollution. The intensive use of broad-
spectrum pesticides for rice production in South-east Asia, for example,
which was associated with the adoption of new high-yielding varieties in the
Green Revolution of the 1960s1970s, created major problems of resurgence
and secondary pest outbreaks. In general, there is still an over-reliance on
spray-and-pray approaches in many developing countries. The agricultural
science research base in these countries is generally highly capable and adept
but suffers from a lack of investment. Nevertheless, there have been impor-
tant and exciting successes in IPM in developing nations since the 1970s
(Way and van Emden, 2000). In South-east Asia, the development of resistant
rice varieties, combined with publicly funded pest surveillance and IPM
training through farmer eld schools and participatory experiments, has
allowed signicant reductions to be made in pesticide applications (Thacker,
2002). In India, an IPM programme based on insecticide resistance manage-
ment in cotton has operated over ten different states since 1992. The pro-
gramme is based on targeted applications of selective insecticides to preserve
natural enemies and pesticide rotation, done according to the same ecologi-
cal principles used in the Arizona cotton IPM programme discussed previ-
ously. The Indian system has resulted in a 30% reduction in the amount of
pesticide applied to the crop, and although it has not increased yields, it has
increased the average net nancial returns of farmers participating in the
programme by 11% (Peshin et al., 2009). In Africa, classical biological control
has proved effective against some invasive pests, most notably on cassava
and maize, while intercropping and the development of the pushpull
strategy are proving successful for maize and sorghum production. Develop-
ing countries are also now investing in home-grown biotechnology research
to produce new crop varieties with improved resistance to arthropods and
plant pathogens. Low labour costs have also enabled the mass production of
arthropod natural enemies and microbial biopesticides to be done economi-
cally using relatively unsophisticated but robust methods. Indeed, the indus-
trialized countries have much to learn from the developing nations about the
effective implementation of biopesticides and biological control. Thus, while
much of the English-language published research on entomopathogenic
fungi comes from Europe and North America, the practical use of fungal
bioinsecticides and bioacaricides has really been pioneered in Central and
South America; 50% of all such products have been developed and commer-
cialized here (Faria and Wraight, 2007). A critical point to note is that while
IPM initiatives are often done according to a top-down approach, in which
62 Chapter 2
pest problems are identied and researched by scientists and the results are
then transferred to farmers, some of the most effective IPM initiatives in
developing nations have been more bottom-up, with farmers and research-
ers working together to identify the main pest issues. Training and educa-
tion have then been provided for farmers, which has enabled them to
develop their own solutions catered to their particular needs and making
best use of traditional agricultural systems (for an excellent discussion of
this topic in relation to biopesticides, the reader is referred to Rodriguez and
Niemeyer, 2005). A highly important development for Africa and Latin
America has been the creation of new export markets to Europe and North
America, particularly for smallholders growing under contract to multina-
tional retailers. In Kenya, for example, 16% of the countrys smallholders
now grow horticultural crops under contract for export (Nwilene et al., 2008).
The requirement for these growers to comply with international standards
for food safety and environmental protection (e.g. the EurepGAP standards
of the EU) has led to signicantly greater focus on IPM done to European
and North American standards.
Using Alternatives to Synthetic Chemical Pesticides in Integrated
Pest Management
As we look to the future, it is clear that synthetic chemical pesticides will
remain a critical tactic in crop protection, but they should be used only when
necessary in order to reduce the chances of resistance developing and to
minimize negative effects on non-target organisms and the wider environ-
ment. This will inevitably mean that alternative crop protection methods
will have to be used more. This includes biological controls, biopesticides,
cultural methods and a wider use of resistant varieties. It will inevitably
require greater consideration to be given to tactics that some people are
uncomfortable with for ethical or moral reasons, such as GM crops. We argue
that the debate about the future of IPM must be framed in terms of the best
practices that can be adopted from all farming systems to make crop protec-
tion more sustainable. Thus, according to Pretty (2008), sustainable agricul-
ture does not mean ruling out any technologies or practices on ideological
grounds. If a technology works to improve productivity for farmers and
does not cause undue harm to the environment, then it is likely to have some
sustainability benets.
There are a number of caveats about alternative, non-pesticide methods
of pest control that must be borne in mind: (i) these methods are generally
not like-for-like replacements for synthetic chemical pesticides; (ii) they have
different modes of action and, thus, different strengths and weaknesses; (iii)
many have lower efcacy than synthetic pesticides, are slower to act or are
vulnerable to breakdown; (iv) many are affected by environmental condi-
tions; (v) they often cost more to buy than synthetic pesticides and they
require specialist knowledge to use them; (vi) there are also many remaining
scientic and technical challenges to their development, not helped by
Pests of Crops 63
under-investment in crop protection research; and (vii) some of the features
that make them attractive from an environmental standpoint can be a problem
in economic terms. For example, the narrow prey spectrum of many biological
control agents means that they are appropriate only for niche markets, with
individual agents often earning less than ?1 million per product per annum,
which discourages companies from developing them. To quote Gelernter
(2005): The features that made most BCPs [biological control products] so
attractive from the standpoint of environmental and human safety also acted
to limit the number of markets in which they were effective.
Many of the perceived weaknesses of non-pesticide agents are based
on comparison with the performance of synthetic chemicals. The unsuitable
adoption of a chemical pesticide development model for these agents can
lead to false and unrealistic expectations of chemical-like performance.
However, the very fact that alternative crop protection methods do not
function in the same way as synthetic chemical pesticides means that they
can be used to compensate for the weaknesses of the latter. Biological control
agents are able to reproduce within the pest population, giving various levels
of self-perpetuating control. Many biological control agents are also able to
actively locate their prey, making them highly useful where pests occupy
cryptic habitats. Biological control, plant breeding and cultural controls gen-
erally do not require the same level of protective equipment to be used as for
chemical pesticides. The lack of a toxic residue on crops and, therefore, the
absence of a preharvest application interval, can be a real benet. Using
knowledge of the causes of pest outbreaks it is possible to use conservation
management, plant breeding, physical methods and cultural techniques to
help prevent the build-up of pest populations in a total systems approach
(Lewis et al., 1997). Moreover, the wide variety of crop protection methods
available means that different combinations can be put together in complemen-
tary ways. This is vital if we are to achieve effective, sustainable pest manage-
ment. There is ample evidence that the various non-chemical pesticide methods
can make valuable contributions to crop protection as part of IPM. In some
situations, a combination of these methods may be able to replace synthetic
pesticides, for example where a pest has developed pesticide resistance. But in
most cases the most practical way forward is to use them in combination
with chemicals in a fully integrated programme.
Table 2.8. Estimated share of 2004 global product sales
for biologically based control agents. (From Gelernter, 2005.)
Class of product Market share (%)
Microbial biopesticides 6570
Benecial macroorganisms 1516
Semiochemicals 1019
Botanicals 48
Microbial soil and plant enhancers 12
64 Chapter 2
Compared with synthetic chemical pesticides, the current market size for
alternative crop protection products is small. For example, the global market
for biologically based plant protection products (by which we mean biopesti-
cides plus predators and parasitoids) represents just 2.5% of the global chem-
ical pesticide market, and is currently valued at ?60 million (Evans, 2008). At
present biopesticide products based on microorganisms make up the major-
ity of the market share for biologically based control agents (Table 2.8)
(Gelernter, 2005). However, market size alone undoubtedly underestimates
the contribution these methods can make to improve sustainability, for exam-
ple by reducing the resistance pressure on chemical pesticides. And as we
shall read in Chapter 3, the market for biopesticides and other alternatives is
increasing. With this in mind, we shall now turn our attention to biopes-
ticides: what are they, what are their properties, and how can they be used in
crop protection?
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3
Pest Management with
Biopesticides
There is no internationally agreed, formal denition of a biopesticide. The
description favoured in this book which is one that tends to be followed by
many national governments for the purposes of regulation is that a biopes-
ticide is a mass-produced, biologically based agent manufactured from a
living microorganism or a natural product and which is sold for the control
of plant pests. The agents used as biopesticides are usually broken down into
three categories: (i) microorganisms (bacteria, fungi, oomycetes, viruses and
protozoa); (ii) biochemicals (which include plant products such as essential
oils, and various compounds synthesized by other organisms such as chitin
and chitosan); and (iii) semiochemicals (most of which are insect pheromones
used in traps or for mating disruption). The authorities in the USA also
include genes that are engineered into crops using recombinant DNA tech-
nology to protect them against pests (these genes are known as plant incor-
porated protectants, PIPs). All of the agents approved for use under these
categories of biopesticide are considered by the authorities to present a low
risk to people, wildlife and the environment. For this reason, some regulators
such as the US Environmental Protection Agency (EPA) group biopesticides
together with other low-risk products such as commodity chemicals. If you
visit the active ingredient index on the US EPA Biopesticides website (http://
www.epa.gov/pesticides/biopesticides/), for example, you will nd that
true biopesticides are listed alongside inorganic compounds such as kaolin
and iron phosphate. While it makes sense to list all these low-risk substances
together, it is misleading to label minerals and other compounds that are not
made by living organisms as biopesticides.
Worldwide there are around 1400 biopesticide products being sold
(Marrone, 2007; R. Gwynn, personal communication). At the time of writing
this book (April 2010), there were 68 biopesticide active ingredients regis-
tered in the EU and 202 in the USA (plus an additional 16 PIPs in the USA)
(Table 3.1). The EU biopesticides consisted of 34 microbials, 11 biochemicals
72 Chapter 3
and 23 semiochemicals, while the USA portfolio comprised 102 microbials,
52 biochemicals and 48 semiochemicals. There are about 225 microbial prod-
ucts being sold in total in the countries of the Organisation for Economic
Co-operation and Development (OECD) (Kabaluk and Gazdik, 2007). These
biopesticide products represent a very small fraction of the total pesticide
(conventional chemical plus biopesticide) market. In 2005, global biopesti-
cide sales were put at US$700 million, equivalent to just 2.5% of the total
pesticide market (Bailey et al., 2010). However there is rapid growth in the
biopesticides sector, with a 5-year compound annual growth rate of 16%
compared with 3% for synthetic pesticides and an expected global market
worth up to US$10 billion by 2017 (Marrone, 2007). The number of biopesti-
cide active ingredients is also small compared with the number of species
of arthropod (predator and parasitoid) natural enemies being used for bio-
logically based pest control. In Europe, about 80 species of arthropod natural
enemies are commercially available (EPPO, 2002) while over 850 species
have been used worldwide (Cook et al., 1996). However, as mentioned in
Chapter 2, biopesticides represent the bulk of the nancial market share for
biologically based pest control agents (i.e. biopesticides plus predators
and parasitoids) at about 85% of the value of this market, compared with
approximately 15% for arthropod natural enemies (Gelernter, 2005).
Despite being just a small part of the overall pesticide market, biopesti-
cides encompass a very broad range of living and non-living entities, with
varying modes of action and a wide range of characteristics. However,
because they are all classed as biopesticides, they are all governed by the
same overarching regulation. Usually, this is based on plant protection
products legislation that was originally designed for synthetic chemical pes-
ticides, and which may or may not have been modied to take biopesticides
into account. This poses challenges for government regulatory agencies in
Table 3.1. Number of biopesticide active substances available in the USA or on the EU Active
Substances List (April 2010).
Insecticide Fungicide Herbicide Nematicide Attractant Repellent
Plant growth
regulator
USA EU USA EU USA EU USA EU USA EU USA EU USA EU
Microorganisms
Bacteria 31 4 21 3 1 1
Fungi 9 5 18 15 5 2 1 1
Viruses 8 5 4 1
Oomycetes 1
Biochemicals 11 3 5 1 1 3 5 23 4 4 3
Semiochemicals 48 23
PIPs
Bacteria 15
Viruses 1
Total 74 17 49 20 7 6 1 54 23 23 4 5 3
PIP, plant incorporated protectant.
Pest Management with Biopesticides 73
terms of managing the potential human safety and environmental risks of
biopesticides, as well as issues of efcacy and the need to deliver govern-
ment policies that improve the sustainability and productivity of agriculture.
For an area such as regulating the potential health risks to farm operatives
who are handling biopesticide products, it makes some sense to include
microbial control agents and natural products within the same legislative
framework as synthetic chemical pesticides because the potential routes of
operator exposure are usually identical (e.g. risks of skin contact and inhala-
tion of sprays, dusts or powders in a concentrated form). However, when it
comes to environmental risk assessment, the issues affecting natural prod-
ucts are very different from those affecting microbial agents. The potential
environmental risks of natural products can reasonably be grouped together
with those of synthetic pesticides. In contrast, the environmental risks associ-
ated with microbial biopesticides have much more in common with the risks
associated with higher organisms used for pest control, such as predators,
parasitoids and parasitic nematodes.
For making the best use of a product within the framework of sustain-
able IPM, then it is undoubtedly the case that the use of the chemical pesti-
cide regulatory model for microbial agents has impeded their development
by drawing attention away from their benecial characteristics as living
organisms, in particular their ability to reproduce within host populations
and thereby give extended pest control, and instead has forced them to be used
as synthetic pesticide clones with unrealistic expectations of chemical-like
efcacy (Waage, 1997).
Comparing Microbial Agents with Other Natural Enemies Used
in Biological Control
Biological control programmes operate throughout the world in agriculture
and forestry. The organisms used for biological control are natural enemies:
a natural enemy is an organism that kills or debilitates another organism.
When a natural enemy is used for biological control, it is referred to as a bio-
logical control agent. Biological control agents include the following:
(i) predatory insects and mites; (ii) parasitoids, which are insects with a free-
living adult stage and a larval stage that is parasitic on another insect; and
(iii) parasites, microbial pathogens and antagonists, such as nematodes,
fungi, bacteria, viruses and protozoa (Bellows and Fisher, 1999; Bale et al.,
2008). Some examples of microbial control agents are given in Table 3.2.
Natural enemies represent a large component of the worlds biodiversity.
It has been estimated that each agricultural pest species is affected by 50250
species of natural enemies (van Lenteren, 2000). These organisms play a key
role in preventing pests reaching damaging levels. It has been suggested that
about 99% of all potential pests are controlled by the natural enemies or
antagonists that reside naturally within agro-ecosystems (Thacker, 2002).
However, only a small proportion of the available species have been investi-
gated for use as biological control agents. Thus, while approximately 750
74 Chapter 3
species of insect pathogenic fungi are known, fewer than 20 have received
serious attention as microbial biopesticides of insect pests (Hawksworth
et al., 1995).
Before we start to look in detail at microbial biopesticides, it is worth
considering for a moment a particular group of biological control agents that
sit halfway between the macro agents that include predators and parasit-
oids and the micro control agents that includes bacteria, viruses, fungi and
the like. Pathogenic nematodes are multicellular animals, about 0.5 mm in
length, which are used for the biocontrol of insects and molluscs and show
close similarities to microbial pathogens in the ways they infect, kill and
reproduce in their hosts. Like predators, parasitoids and the authorized
microbial biopesticide products, they are recognized as posing minimal or
zero safety risk to people. Entomopathogenic nematodes in the genera
Xenorhabdus and Heterorhabditis kill their insect hosts using symbiotic bacte-
ria, which the nematodes carry in specialized internal structures and which
are released during infection to cause a fatal septicaemia in the insect host.
For these reasons, many biocontrol researchers, practitioners and learned
societies, such as the Society for Invertebrate Pathology, tend to group
Table 3.2. Examples of microorganisms used as control agents of agricultural pests.
(For more information see Copping, 2004.)
Organism Use Pest Target crops
Bacteria
Agrobacterium
radiobacter
Antibacterial
agent
Crown gall (Agrobacterium
tumefaciens)
Soft fruit, nuts, vines
Xanthomas campestris
pv. poannua
Herbicide Annual bluegrass Turf
Bacillus subtilis Fungicide Fusarium, Pythium,
Rhizoctonia spp.
Legumes, cereals,
cotton
Bacillus thuringiensis Insecticide Various Lepidoptera,
Diptera, Coleoptera
Vegetables, fruit,
cotton, rice, forestry
Fungi
Lecanicillium
longisporum
Insecticide Aphids Glasshouse edible and
ornamental crops
Phytophthora
palmivora
Herbicide Strangler vine Citrus
Trichoderma
harzianum
Fungicide Pythium, Phytophthora,
Rhizoctonia spp.
Orchards, ornamentals,
vegetables,
glasshouse crops
Protozoa
Nosema locustae Insecticide Grasshoppers, crickets Pasture
Viruses
Cydia pomonella
granulosis virus
Insecticide Codling moth Apple, pear
nematodes with the true microbial pathogens, while recognizing the differ-
ences. However, in the USA, the EU and other OECD countries their use is
exempted from biopesticide regulations. Instead they fall within the legisla-
tive framework for the use of higher organisms. These regulations are usu-
ally concerned with the introduction of non-native species. For example, in
the UK, the use of non-native species of nematodes for biological control is
prohibited, being enforced through the UK Wildlife and Countryside Act
and overseen by the Department for the Environment, Food and Rural
Affairs. In this book, we give some coverage to nematodes for biological con-
trol because we believe the comparison with true microbial biocontrol
agents is informative. Indeed, from an IPM perspective, it is important to
consider microbial biopesticides using the same concepts that are applied to
other natural enemies. Because all natural enemies are alive, they share com-
mon ecological properties, including the potential to reproduce and the
requirement for nutrition and other resources. When applied as a biological
control agent, the ability of a natural enemy to multiply and persist within
the vicinity of its host or prey enables it to give a degree of self-sustaining
pest control. Natural enemy reproduction is an important component of
most biological control strategies. Unfortunately, it has tended to be over-
looked for microbial biopesticides as a result of them being developed and
regulated by a system designed originally for chemical agents.
The Biology of Microbial Natural Enemies
Fungi, bacteria, viruses and protists are all being used for biological control
or are being investigated as potential biological control agents. These bene-
cial microorganisms are widespread in nature, where they contribute to the
natural regulation of invertebrates, plant diseases and weeds. They have a
range of properties that make them desirable for IPM (Hajek, 2004). The
microorganisms selected for use as biological control agents do not naturally
infect vertebrates, and so are considered safe to humans, livestock and verte-
brate wildlife. They produce little or no toxic residue, and development and
registration costs are signicantly lower than those of synthetic chemical pes-
ticides (Hajek, 2004). They can be applied to crops using the same equipment
used to apply chemical pesticides, formulated in similar ways to pesticides
to enhance their efcacy, and they tend to have very short harvest intervals.
As living organisms, they can reproduce on or in close vicinity to the target
pest, and this provides various degrees of self-perpetuating control depend-
ing on the agent used. Microbial agents may also prevent the target pest from
feeding or reproducing. Microbial agents used for biocontrol are selective,
making their use compatible with the deployment of other natural enemies.
The exact host range varies among different types of control agent. Baculovi-
ruses, for example, are highly specic and will generally infect only a single
species or genus of insect. In contrast, some species of entomopathogenic
fungi are able to infect insects across a range of taxonomic orders (Tanada
and Kaya, 1993). Many microbial biopesticides can be produced locally,
76 Chapter 3
which can be important in terms of choosing and matching natural enemies
to small-scale needs (Waage, 1997). Like other biological control agents, the
successful use of microbial natural enemies requires fundamental knowl-
edge of the pathogen and the pest (Collier and van Steenwyck, 2004; Bale
et al., 2008). When this condition is satised, and the agent is used rmly
within IPM, then biological control can sometimes be more cost effective
than purely chemical control (Tisdell, 1990; van Driesche and Bellows, 1995).
However, under the present market system, many microbial biopesticides
products have not competed well with less expensive and more effective
synthetic pesticides (Gelernter, 2005). The downsides of using microbial nat-
ural enemies are that many are niche-market products, pest control is not
immediate, there can be a lack of environmental persistence, and efcacy can
be unpredictable in outdoor environments. Microbial agents that can only be
cultured in vivo can also be expensive to mass-produce. Like all living organ-
isms, they are adapted to certain physical conditions and this can restrict the
environments in which they are used. For example, fungi require conditions
of high water availability to germinate and grow, and hence fungal control
agents naturally function best in the soil or in environments where humidity
can be controlled, such as glasshouses. Baculoviruses and entomopathogenic
bacteria tend to be susceptible to degradation by ultraviolet light, and so they
may not persist well when sprayed on to plant foliage. However, some of
these limitations can be overcome using formulations such as stickers, wet-
ters, oils and ultraviolet protectants. Often, efcacy can be improved signi-
cantly by paying careful consideration to the method of application, for
example by using low-volume or ultra-low-volume sprays and mists that
place the microbial agent on the underside of leaves.
Strategies for Using Biological Control Agents, Including Microbial Agents
The ways in which biological control agents are used vary according to the
type of pest and the biological characteristics of the control agent, as well as
the agricultural setting. Unfortunately, researchers and other specialists
working with biological control agents of arthropods, plant pathogens and
weeds have adopted different terms to describe the control agents and how
they are used. These terms can have subtly different meanings, which can
cause confusion. For example, entomologists nearly always refer to insect
parasitoids and predators as natural enemies, but microbiologists working
with pathogens of insects rarely use this term. Those working on the micro-
bial control of plant pathogens often refer to their control agents as antago-
nists, which reects the fact that many microbial control agents of plant
disease work by outcompeting plant pathogens for space or nutrients rather
than killing or injuring them. This term is never used by insect pathologists
working on insect microbial control, as the microbial agents used for insect
control work by directly killing the insect host. The lack of a common lan-
guage is undoubtedly an impediment for the biological control policy net-
work, including regulators, policy makers, farmers and growers. Some of the
terms used have little or no scientic meaning, or they were derived from
concepts that were valuable at the time but are now confusing. For example,
the use of an alien biological control agent to control an alien, invasive pest is
referred to as classical control. The word classical has no inherent biologi-
cal meaning; rather it refers to the fact that introductions of alien natural
enemies to control alien pests were historically the rst successful examples
of biological control (e.g. the control of cottony cushion scale on citrus in
California in the late 1800s) and thus are considered an established model for
biocontrol.
Since the beginning of the 21st century, there has been a drive to unify
some of the terms used in biological control (Eilenberg et al., 2001). In this
book, we are using the Eilenberg et al. (2001) unied denitions of biocontrol
strategies as much as we can. There are three broad biocontrol strategies: (i)
augmentation (i.e. application of natural enemies that already live in the area
of use); (ii) introduction (i.e. release of an alien control agent to control an
alien pest); and (iii) conservation (i.e. manipulating agricultural practices or
the environment to enhance natural control).
Augmentation biological control
Augmentation is a strategy that uses, as a biological control agent, a species
of natural enemy that lives naturally in the country or region of use. Natural
enemies are widespread in the environment and exert a degree of control
over pests as part of normal ecological processes. The augmentation strategy
is aimed at increasing the effectiveness of control by releasing a control agent
in crop environments where it is absent or at low levels. The natural enemy
is released without the expectation that it will establish permanently or give
autonomous regulation of the pest. The word augmentation derives from
the idea that individuals of the same species, which have been grown in a
specialized production facility, have augmented local natural enemies.
Augmentation is used very widely within the specialist biological control
literature, particularly for biological control using arthropod natural ene-
mies. However, it is not a self-explanatory term and it almost certainly causes
confusion for those outside biological control research.
There are two different approaches to augmentation biological control.
The inundation approach is The use of living organisms to control pests when
control is achieved exclusively by the organisms themselves that have been
released (Eilenberg et al., 2001). Individuals of the biological control agent
are mass-produced in specialized production plants and then applied in very
large numbers into the close vicinity of the target pest. The intention is to
achieve rapid pest control, with no expectation that the control agent will
reproduce itself in the environment. As a consequence, applications will have
to be repeated if the pest population increases again past the economic
threshold. Microbial biopesticides used for the inundation approach are usu-
ally formulated as liquids, emulsions, powders or granules so that they can
be applied using the same kind of sprayers and other apparatus used for the
78 Chapter 3
application of chemical pesticides. The inundation approach is based on the
hypothesis that natural factors limiting the persistence and spread of the bio-
logical control agent (such as abiotic conditions, poor dispersal of the control
agent, or a patchy distribution of the target pest) can be overcome by repeated
applications of large numbers of the control agent (Hallett, 2005). An exam-
ple of the inundation approach is the use of the insect pathogenic bacterium
Bacillus thuringiensis. This bacterium produces an insecticidal protein crystal
during sporulation, and a mixture of bacterial spores and the protein crystal
is sprayed on to insects for their control. When they are ingested, they cause
ion leakage from gut cells and kill the target insect in 2448 h. However, for
most target pest insects, the bacterium does not reproduce to any signicant
extent and control is caused by the combination of the protein crystals and
the individual bacterial cells that have been sprayed.
The inoculation approach is The intentional release of a living organism
as a biological control agent with the expectation that it will multiply and
control the pest for an extended period, but not that it will do so perma-
nently (Eilenberg et al., 2001). Thus, the control agent is able to respond to
changes in the size of the pest population. The biological control agent con-
sists of a product that has been grown or cultured in a specialized facility, but
smaller numbers are applied to the target pest compared with the inundation
approach, and the environment must be suitable to support its reproduction
and localized spread. As an example, many of the microbial control agents
used against plant pathogens in the soil rely on the ability of the control
agent to grow and multiply in the root zone, particularly for those agents that
function by outcompeting plant pathogens for space or other resources
(Whipps, 2001). The length of time over which the inoculum continues to
reproduce in the environment varies according to each situation, and is
dependent upon the life history of the control agent (r- or K-selection, spe-
cialist or generalist) and the highly complex ecological interactions between
the control agent, the pest, the envir onment, and other components of the
biotic community including, of course, the crop plant. In general terms, over
time the population of the control agent will be supported at the natural car-
rying capacity of its environment, because the species of natural enemy that
has been released is already a natural component of the biota in the region of
use. Successful control relies on the assumption that the control agent is not
present in effective numbers within the immediate vicinity of the pest as a
consequence of agricultural practice.
In practice, because all living biological control agents have potential to
reproduce in the environment, there is not a straightforward distinction
between inundation and inoculation. Thus, control agents applied according
to the inundation approach will exhibit a certain amount of localized repro-
duction and spread, resulting in a small amount of self-sustaining control. In
inoculation, most control may be given by the released organisms with the
effects of the progeny declining over time (Hajek, 2004). For this reason, they
are always considered together as forms of augmentation control. All micro-
organisms used for augmentation control come within our denition of
biopesticides, regardless of whether they work by the inundation or the
inoculation approach, and their use is covered by biopesticides regulations.
However, the regulatory situation for the next strategy for biological control,
classical control, is not so clear-cut.
Classical biological control
Classical biological control is the intentional introduction of an exotic bio-
logical control agent for permanent establishment and long-term pest con-
trol (Eilenberg et al., 2001). In this context the term exotic refers to a
non-indigenous organism. It is based on the natural enemy release hypothe-
sis and is targeted at the control of alien invasive species that have estab-
lished and spread in a new country as a result of separation from their
co-evolved natural enemies in their homeland. It is intended to work over
very large geographical scales. A limited number of releases of the biological
control agent are made, with the expectation that a permanent relationship
between pest and its co-evolved natural enemy will become re-established,
i.e. invasion by the natural enemy is desired. In order for it to work success-
fully, in other words to permanently control the pest population with no
adverse side effects of the biological control agent on the environment, then
a detailed and thorough ecological knowledge is required. Classical biologi-
cal control is not commercially protable, and for this reason it is imple-
mented through government-funded programmes. Invasive alien species
cause very signicant amounts of economic and ecological damage and clas-
sical control is the only realistic option available for permanent control in
many cases. It has been used successfully in the past, although it is true to say
that, in Europe at least, introductions have become more difcult in recent
years because of public fears over environmental impact, an absence of
appropriate legislation and some high-prole cases where unsuitable, gener-
alist natural enemies have been released due to ineffective regulations and
impacted beyond their intended target. A more detailed discussion of the
environmental safety issues surrounding classical control is included at the
end of the chapter.
The rst, and still the best known, example of classical control concerned
the cottony cushion scale, Icerya purchasi. This insect was unintentionally
introduced into Californian citrus orchards from Australia in 1868 and
pushed the Californian citrus industry to the verge of collapse in less than 20
years. Natural enemies of the scale were identied in Australia and around
500 predatory vedalia beetles, Rodolia cardinalis, were released. The beetle
population expanded rapidly and their subsequent spread was aided by
moving beetle-infested branches to new orchards. The strategy was so suc-
cessful that the scale was completely controlled by 1890. Today, classical bio-
logical control of insect pests is used on 350 million ha worldwide, equivalent
to 10% of the total global area of cultivated land, and is reported to have a
costbenet ratio in the range of 1:20 to 1:500 (Bale et al., 2008). Most of the
natural enemy species introduced have been insects: around 2000 species
have been introduced worldwide, leading to the permanent reduction of 165
80 Chapter 3
arthropod pest species (van Lenteren et al., 2006). There are estimated to have
been about 130 examples of classical introductions against insect pests in
Europe (Sheppard et al., 2006). Microbial natural enemies have been used less
frequently in classical control. Around 135 classical introductions of micro-
bial pathogens including nematodes have been recorded for the control of
insect and mite pests (Hajek and Delalibera, 2010). We will include some
examples as we go through this chapter.
Classical release of microbial natural enemies for control of crop pests
does not fall within our denition of a biopesticide. Classical microbial
control agents are not mass-produced entities and they are not sold for
commercial prot. However, we will consider them briey in this book for
two reasons. First, knowledge of classical control is very instructive when
considering the potential environmental risks associated with microbial
biopesticides. Second, classical microbial control agents are affected by plant
protection products legislation. Unfortunately, as is the case for microbial
biopesticides, the plant protection products legislation in place in organiza-
tions such as the EU was not developed with biological control in mind and
this is hindering the development and use of microorganisms in classical
control (Sheppard et al., 2006). For example, the EU plant protection products
legislation requires information on directions of use of the product to be
available to users and detailed information on eld efcacy in comparison
with standard chemical treatments, neither of which is appropriate to classi-
cal control. Registration costs, including the costs of statutory toxicological
testing, are also very high for these agents, which are developed using the
limited funds that are available from public money.
Conservation biological control
Conservation biological control is modication of the environment or exist-
ing practices to protect and enhance specic natural enemies or other organ-
isms to reduce the effect of pests (Eilenberg et al., 2001). It does not require
application of natural enemies, but is intended to enhance the numbers and
activities of natural enemies living naturally within the vicinity of pest popu-
lations. Like other forms of biologically based control, it is not a stand-alone
solution and must be rmly embedded within the overall context of IPM.
Conservation biological control techniques are in place for enhancing the
activities of arthropod natural enemies and there is a large body of evidence
suggesting that provision of oral resources, alternative food and shelter
habitats can increase the abundance and diversity of predators and parasit-
oids, but there is as yet limited evidence that this leads to decreased pest
damage or increased yields ( Jonsson et al., 2008). However, successful con-
servation biocontrol of insect pests with predators and parasitoids has been
demonstrated for a small number of crops including outdoor lettuce and
grapes (Chaney, 1998; Berndt and Wratten, 2005; Berndt et al., 2006). Because
it entails habitat management, it could provide additional public goods, such
as biodiversity conservation, ecological restoration and tourism (Fielder
et al., 2008). Wine producers in New Zealand, for example, are now growing
owers in between vines in order to lure and retain naturally occurring para-
sitoids; these oral displays also attract tourists to the region and are being
used to market the wine as a premium, environmentally friendly brand
(Anon., 2006).
Conservation biological control can also take advantage of microbial
natural enemies. Successful examples include: (i) the exploitation of micro-
organisms that antagonize plant pathogens in disease-suppressive soils;
(ii) the development of a service that predicts natural outbreaks of the
insect pathogenic fungus Neozygites fresenii in populations of cotton aphids
in the south-eastern USA; and (iii) reducing or avoiding fungicide sprays
that inhibit the entomopathogenic fungus Neozygites oridana, which
improves the natural biological control effect of this fungus against the
two-spotted mite, Tetranychus urticae, in the maizegroundnutsoybean
agrosystem in the USA (Smitley et al., 1986; Dick et al., 1992).
Using a microbial natural enemy for conservation biological control is
patently different from application of a microbial biopesticide: it requires no
product to speak of and falls outside plant protection products legislation;
hence there is no statutory testing of safety or efcacy. It is based on an eco-
logical hypothesis that manipulating agricultural practice can increase the
activity of microbial natural enemies that are residing within the locality. It
is important to keep this in mind when considering the principles of envi-
ronmental risk evaluation for microbial biopesticides, not least because
augmentation microbial control and conservation microbial control use the
same kinds of microbial natural enemy. The main difference concerns the
level of exposure to microorganisms in terms of human safety. Because aug-
mentation microbial control uses mass-produced microorganisms, there are
potential safety risks associated with sensitization and developing allergies
for people who regularly come into direct contact with high concentrations
of microorganisms, particularly if there is a chance that microbial spores and
other entities could be inhaled. For classical control using a limited number
of small releases, the exposure is likely to be conned to just the very small
number of people doing the releases.
Microbial Natural Enemies of Invertebrate Pests, Plant Pathogens
and Weeds
Pathogens of invertebrates and their use in biological pest control
Invertebrates are utilized as a source of food and for reproduction by a
wide variety of microbial parasites in nature. Those pathogens with suitable
properties in terms of their ecological characteristics, safety to humans
and the environment, and the ease with which they can be used in a practical
way can make useful biological control agents. The pathogens of insect
and mites are collectively referred to as entomopathogens. There are also
pathogens of molluscs that can be used for biocontrol.
82 Chapter 3
The main groups of invertebrate pathogens used for biocontrol are fungi,
bacteria and viruses. The entomopathogens used for biological control all
work by causing lethal infections in their hosts, although their modes of
action vary signicantly depending upon the taxonomic group of pathogen.
For this reason, it is sensible to divide up our discussion of the biology of
entomopathogens according to their taxonomic classication. In contrast, the
biggest division between the microbial control agents of plant disease is
functional rather than taxonomic. Here, there is a logical division between
microbial antagonists, which interact directly with plant pathogens, and
agents that act indirectly by boosting a plants ability to withstand disease.
Insect pathogenic bacteria
Entomopathogenic bacteria occur in about five different taxonomic fam-
ilies. Most of these are opportunistic pathogens that only infect insects
that are under some kind of environmental stress. In contrast, a small
number of bacterial species have evolved as specialist insect pathogens.
The most important species occur in the genus Bacillus. Two species of
these Gram-positive, spore-forming bacteria are used as augmentation
biological control agents using the inundation approach. Bacillus sphaeri-
cus is a pathogen of mosquito larvae and has been used for their control
(Lacey and Undeen, 1986). Bacillus thuringiensis (known simply as Bt) is
naturally widespread and can be found in soil, on plant surfaces and in
grain storage dust. It consists of a range of different subspecies and
strains, each of which is pathogenic to a narrow range of insect species.
As part of its life cycle, Bt produces a large protein crystal associated
with spore formation, known as a parasporal crystal. There is normally
one crystal per cell. The proteins, referred to as -endotoxins, are formed
outside the spore and are toxic to insects, although some types of
Bt produce crystals with no known activity. The -endotoxin is host-
specific, does not harm vertebrates and is very active (Bond et al., 1971;
Siegel, 2001). Wild-type strains of Bt usually have more than one crystal
gene, called cry genes, which occur on plasmids (extrachromosomal
DNAs) and the parasporal crystal usually consists of combinations of
different proteins. Following ingestion, the alkaline environment of the
insect midgut causes the crystals to dissolve. At this stage, the toxins are
inactive, and are trimmed by gut proteases to an activated, N-terminal,
truncated form. The activated toxin binds to specic receptors on the mid-
gut epithelial cells, inserts itself into the membrane using the N-terminus
of the protein and forms pores that kill the epithelial cells by osmotic
lysis (Gill et al., 1992). In some highly susceptible hosts, ingestion is
followed by a general paralysis leading to death within an hour. In the
majority of insects, only the gut is paralysed and death occurs in about 48 h
depending on dose.
Bt -endotoxins are part of a large family of homologous proteins. More
than 130 genes encoding -endotoxins have been identied to date. Differ-
ences in the nucleotide sequence of the cry genes cause variation in the tox-
icities of different crystals. These genes generate a rich source of biodiversity
and partly account for the host preferences expressed by different subspecies
of Bt. Bt is the most widely used microbial control agent and it is used always
as an inundative biopesticide. The bacterium is grown in fermentation tanks
up to the sporulation phase, after which the spores and the -endotoxin crys-
tals are harvested, cleaned, dried and formulated. The nal product is then
sold to growers and farmers. At the moment the available products use tox-
ins specic for caterpillars, beetles or haematophagous ies but new toxins
are being discovered against a wider array of targets including mites, cock-
roaches, grasshoppers and other species (van Frankenhuyzen, 2009). Bt is
very well documented as being safe to workers, benecial organisms and the
environment (Lacey and Siegel, 2000). After production, the bacterial spores
and crystals are processed to improve their shelf-life and handling character-
istics. They can be formulated for application as dusts, granules, wettable
powders, or as liquid emulsions, encapsulations or suspension concentrates.
Booster formulations are also available using semiochemical attractants or
phagostimulants (Brar et al., 2006).
At present, microbial Bt formulations are applied as foliar sprays for fruit
and vegetable crops (they have also been very important for the control of
insect vectors of human and animal disease including mosquitoes, blackies
and tsetse ies). Prior to the mid-1990s, Bt sprayable products were also sold
for use on broad-acre crops; however, these have now been superseded by
the development of Bt transgenic crops (see below). Nevertheless, Bt sprays
remain an important and growing tactic for horticultural crops where their
high level of selectivity and safety are considered desirable, and where there
are problems with resistance to conventional insecticides, such as apple pro-
duction. In the USA, for example, Bt foliar sprays are applied to about 10% of
the total area of cultivated apple trees. By comparison, the chemical insecti-
cide chlorpyrifos (an OP) is applied to 60% of the total area, imidacloprid (a
neonicotinoid) to 25% and Spinosad (a microbial) to 24% (NASS, 2008). Bt
foliar sprays cost about the same as modern chemical pesticides such as
Spinosad (van Driesche et al., 2008).
Expression of Bt d-endotoxins in genetically modied crops
While Bt sprays can be very effective products, their use has been eclipsed by
the development of GM crops that express Bt cry genes. These crops are com-
monly referred to as Bt crops and they have been adopted rapidly by farmers
around the world, with the exception of Europe where there has been wide-
spread reservation among consumers about GM crop technology. In 2009,
GM crops were being grown in 25 countries over 134 million ha, equivalent
to about 9% of the global area of cultivated land (International Service for the
Acquisition of Agri-Biotech Applications, 2010). These include six EU states
Spain, Czech Republic, Portugal, Poland, Slovakia and Romania although
the area of cultivation in these countries is generally less than 0.1 million ha.
Bt GM crops were developed to overcome some of the perceived short-
comings of using Bt sprays, specically the lack of systemic activity (which
meant that Bt sprays were not effective against insects that burrowed into
plant tissue), degradation by ultraviolet light and too narrow a host range
84 Chapter 3
(de Maagd et al., 1999). The crops that are currently available express cry
genes for -endotoxins that are specic for lepidopteran pests, particularly
those that are major pests of maize, such as European corn borer, Ostrinia
nubilalis, and pests of cotton such as the bollworm, Helicoverpa zea. Bt maize
with resistance to western corn rootworm, Diabtrotica virgifera (Coleoptera),
which is a highly damaging and invasive pest of maize in North America
and Europe, is also available, while the technology has been recommended
as the way forward for managing diamondback moth, Plutella xylostella,
which is a particularly severe pest of brassica production in Africa and South
Asia (Grzywacz et al., 2010). Truncated forms of Bt cry genes were expressed
in plants following Agrobacterium-mediated transformation. The nucleotide
composition of bacterial and plant genes varies signicantly. As a conse-
quence, the original cry sequences inserted into plants contained regions that
acted in the plant as mRNA instability motifs, as well as regions that were
interpreted by the plant as transcription termination sites, which meant that
expression levels were very low. In total, nearly 60% of the codons of the
inserted gene were altered, which increased expression levels 100-fold and
gave effective protection (de Maagd et al., 1999).
Since being made commercially available in the late 1990s to early 2000s,
Bt maize and cotton have become mainstays in many countries and are
grown on tens of millions of hectares. Surveys of farmers pesticide use
indicate that growing Bt crops can result in signicantly reduced spray appli-
cations of conventional insecticides, up to 70% in some cases (Shelton et al.,
2002.). Because -endotoxins are highly specic, this can result in signicant
environmental benets. Laboratory and eld studies done over multiple
years indicate that Bt crops have substantially lower impact on non-target
organisms than the broad-spectrum insecticides used previously, and have
shown either no impact or only a transient effect on arthropod natural ene-
mies (where a reduction has occurred, it has been caused by a reduction in
the number of target pests as prey for natural enemies and not by a direct
effect of the crop) (Romeis et al., 2006).
Despite this, there has been a very restricted uptake of Bt crops in Europe.
Why is this? It is undoubtedly the case that the development of policies on
GM crops in Europe has been affected by a lack of upstream engagement
between governments, regulators, farmers, pressure groups, industry, the
media and other members of civil society. In addition there has been a loss
of condence in scientic experts by the general public over issues of risk.
Governments have based much of their policy on evidence-based risk assess-
ment, forgetting perhaps that while scientic expertise and evidence can help
answer specic questions about GM crops, it cannot be the only tool for
developing policy. People entering the debate about GM have different points
of view and hence a resolution may not be possible. Agriculture in Europe
has its own distinctive social dimension and hence Europeans may well
have different concerns about GM compared with citizens elsewhere. The
ethical issues surrounding GM crops are many and complex, and include
general welfare (i.e. the responsibility of governments to protect the interests
of citizens), consumer choice and rights, principles of justice, and the
boundary between what is considered natural/unnatural (Nufeld Council
on Bioethics, 1999).
Those in favour of GM argue that transgenic crops can help increase
yields (e.g. by reducing losses due to pests), can have improved nutritional
content, require fewer inputs and have less postharvest spoilage and wast-
age. Arguments against GM crops include possible harm to human health,
concerns that the technology consolidates the industrialization of agricul-
ture, that it is not natural, and that it may damage the environment (e.g. by
having effects on natural enemies and other non-target species or by the
introgression of transgenes into wild plants). In Europe and elsewhere,
detailed environmental risk analysis of potential effects of GM crops, based
on laboratory and eld experiments, is made before licences to release the
technology are granted, and extensive farm-scale evaluations have been done
(Freckleton et al., 2003). Critics have argued that even farm-scale trials cannot
predict the effects of GM crops when grown at very large scales. However,
eight countries now grow more than 1 million ha of GM crops each (the USA,
Canada, China, India, South Africa, Paraguay, Argentina and Brazil) (Science
online, 2010) and hence if negative effects do occur from these crops, then
one might assume that they will become apparent in the next few years if
they have not done so already. For Bt crops, resistance management is a legit-
imate concern, as resistance has developed to Bt foliar sprays (Li et al., 2007).
A resistance management strategy has been devised based on the cultivation
of areas of non-Bt crops as refugia to maintain susceptible alleles within the
pest populations, and this has proved successful so far (Shelton et al., 2002).
The movement of Bt transgenes into landrace and wild populations of plants
is also an important area. This is not an issue in countries where the GM crop
species is not native and does not hybridize with native plants (e.g. Bt maize
in Europe), but it could be a different story where GM varieties are grown in
areas of the world that are centres of plant origin and harbour much of the
natural genetic variation in wild relatives of crop plants. The concern is that
transgenes, such as those conferring resistance to insect herbivores, could
increase the tness of wild relatives and thus would enhance their survival.
Determining the biological signicance of the dispersal of transgenes into
wild relatives or landraces is extremely challenging, because it requires a
detailed understanding of plant population dynamics over large spatial
scales and the information required cannot necessarily be obtained from
small plot experiments. In Mexico, which represents much of the natural
diversity of maize, the cultivation of GM maize varieties has not been
allowed since 1998. Nevertheless, a comprehensive recent study indicates
that 3% of seed lots of landrace maize in Mexico could express recombinant pro-
teins from Bt while 2% could express recombinant proteins for glyphosate
tolerance (Dyer et al., 2009). Transgene dispersal has probably occurred by
growing GM varieties that then hybridize with landraces, and hybrid seed is
passed from farmer to farmer as part of everyday business. The GM varieties
may have been planted prior to the moratorium in 1998, or illegally planted
by farmers, or they may have come from GM grain sent from the USA to
Mexico intended for food use.
86 Chapter 3
If we set the issue of unintended transgene dispersal aside, it is apparent
that Bt GM crops can provide benets for farmers, but we want to stress that
they are not a panacea for insect control, and if they are not used wisely then
side effects can and will occur. A good illustration of this concerns secondary
pest problems caused by mirid bugs (hemipteran pests with piercing
mouthparts that feed on plant sap), which have occurred on Bt cotton grown
in China (Lu et al., 2008). Broad-spectrum pesticides controlled the mirids
previously, but they are not controlled by Bt cotton, which is specic for cat-
erpillar pests. Problems with mirids in China did not occur until a few years
after the widespread uptake of Bt cotton (i.e. there was a time lag between
adoption of Bt cotton and the onset of secondary pest problems). The unfor-
tunate result is that some farmers growing Bt cotton in China are having to
make more pesticide applications than before in order to control mirid out-
breaks, with a net reduction in revenue compared with conventional cotton
(Wang et al., 2006). Secondary pest outbreaks are a well-known phenomenon
in agriculture, but without more evidence it is difcult to say whether this
particular problem could have been foreseen. There is no evidence that the
secondary pest outbreaks were caused by the Bt crops having a negative
effect on mirid natural enemies within the agro-ecosystem; rather it is because
broad-spectrum pesticides previously controlled these pests.
One lesson stands out clearly: if GM crops, or any other new technolo-
gies, are to be used to increase crop production, then they must be treated
on a case-by-case basis and utilized according to basic IPM and ecological
principles in order to make their use sustainable and environmentally
acceptable.
Insect pathogenic viruses
Insect pathogenic viruses are widespread in the natural world: over 1600
different viruses have been recorded from more than 1100 species of insects
(Tanada and Kaya, 1993). One group of insect pathogenic viruses, the bacu-
loviruses, have received particular attention as potential biological control
agents. The viruses in this group only cause infections in insects and other
closely related arthropods, and are biochemically and genetically very
distinct from any viruses recorded from vertebrates; thus they are consid-
ered inherently safe to people. All baculoviruses consist of the same basic
structure: an enveloped, rod-shaped nucleocapsid comprised of DNA and
protein, surrounded by a proteinaceous occlusion body that confers some
environmental protection to the virus. There are two baculovirus genera:
(i) nucleopolyhedroviruses (NPVs) infect over 400 insect species, mainly in
Lepidoptera (34 families) and to a lesser extent Hymenoptera and some
other orders (Diptera, Coleoptera, Neuroptera); and (ii) granuloviruses
(GVs) infect lepidopteran hosts, each GV species usually being specic for a
particular species of host.
Baculoviruses usually infect larval hosts that acquire virus particles during
feeding. The virus infects the cells of the midgut and then spreads to the rest of
the body. During infection the host becomes debilitated, resulting in reduction
of development, feeding and mobility and increasing exposure to predation.
Death occurs in 58 days depending on the amount of virus inoculum that
has been acquired, but it can be longer. Diseased and dead larvae serve as
inoculum for virus transmission. Virus particles can be spread by rain or by
other animals, including other insects.
Because they have such a narrow host range, which is well characterized
and documented, baculoviruses are considered to pose minimal environ-
mental risk when used in IPM (Huber, 1986; Groner, 1990). Baculoviruses
require living insect cells in order to reproduce and hence mass production
can only be done by growing the virus in host insects. This might appear
to be an expensive and cumbersome system, but in fact they can be mass-
produced economically in the larger lepidopteran species and some very ef-
cient factory mass-production systems have been developed. The harvested
viruses can also be formulated to improve their performance in the eld, and
they are usually applied as a spray on to plant foliage using conventional
spray apparatus.
In the USA, baculovirus products are available as inoculative biopesti-
cides for the control of forest pests such as Douglas r tussock moth and
gypsy moth, and as inundative biopesticides against pests of cotton such as
Helicoverpa and Spodoptera. In the USA and Europe the Cydia pomonella granu-
lovirus (CpGV) is used as an inundative biopesticide against codling moth
on apples. In Washington State, the USAs biggest apple producer, it is used
on 13% of the apple acreage (NASS, 2008). In Brazil, the NPV of Anticarsia
gemmatalis, the soybean caterpillar, was used in the mid-1990s on up to 4 million
ha (approximately 35%) of the soybean crop (Moscardi, 1999). The costs of
using this virus biopesticide are reportedly 2030% lower than using chemi-
cal pesticides; however, the technical challenges of mass-producing the virus
meant that supply could not meet with demand, and as a result the Brazilian
government has invested in new production technologies (Szewczyk et al.,
2006). It remains to be seen whether use of the virus is supplanted by the
imminent commercialization of Bt transgenic soybean (MacPherson and
MacRae, 2009). Elsewhere, the non-occluded baculovirus of the rhinoceros
beetle, Oryctes rhinoceros, has proved to be a valuable inoculative biopesticide
to protect coconut palms in the Pacic islands (Huger, 2005). An early
example of serendipitous classical control involving a baculovirus concerns
the European spruce sawy, Gilpinia hercyniae (Moscardi, 1999). This
hymenopteran insect was introduced into North America accidentally from
Europe during the early 1900s and occurred in outbreak proportions. It
became a serious problem in Canadian forests in the 1930s. A major pro-
gramme was begun in which predators and parasitoids were imported from
Europe and mass-reared for release into the forests. Initially the level of
release was low but expanded rapidly (2.5 million parasites released in 1935,
18 million in 1936, 47 million in 1937 and 22 million in 1940). Meanwhile the
sawy problem continued to get worse; in 1939, 73% of white spruce and
43% of black spruce in the original outbreak area were reported dead. By
1942, however, the larval population in all but a few areas had declined to
medium or light intensity and this was associated with a viral disease caused
by an insect pathogenic virus. The origin of the virus has never been traced
88 Chapter 3
but it was probably introduced unknowingly with one of the parasitoids
from Europe. Once introduced, the virus spread rapidly and, along with
other biological control agents, it kept the sawy population below the eco-
nomic threshold level. The success of this virus as a long-term control agent
is due to several factors. Transovum transmission (i.e. vertical transmission)
of the virus and contamination of foliage with virus by adult sawies have
been postulated as effective mechanisms of spread and transmission.
Entomopathogenic fungi
Most species of entomopathogenic fungi used for biological control occur
in two phyla, the Zygomycota and the Ascomycota. In the Zygomycota, most
entomopathogenic species occur within the class Entomophthorales. These
fungi show asexual reproduction on individual hosts during the summer
but often switch to sexual reproduction at the end of the year to produce
resting spores that survive over winter. The Ascomycota contain fungi that
show sexual reproduction as well as species that appear to have lost the
ability to reproduce sexually.
Entomopathogenic fungi attack all major groups of insects and mites.
They infect their hosts using spores that adhere to the outside of the hosts
body and germinate in response to biochemical and environmental cues. The
spores then grow through the cuticle using a combination of enzymatic
action and mechanical pressure. Usually the fungus grows into the hosts
haemocoel, the intercellular space that surrounds the major organs and is
bathed in a nutrient-rich uid. If the fungus is able to overcome the host
immune system operating within the haemocoel, it then goes on to prolifer-
ate and spread throughout the rest of the body, often in the form of yeast-like
cells that do not naturally survive outside the host. The host is killed by a
combination of mechanical damage, nutrient exhaustion and cell death
caused by fungal toxins. The relative importance of these mechanisms varies
with the specic fungal isolate or host. In many cases, a reduction of feeding
is one of the rst overt changes in an infected host. Death occurs within 47
days of infection, followed by the production of large numbers of spores on
the cadaver. Thousands or millions of spores may be produced on large
insects, such as locusts or caterpillars. The spores of many species of Ento-
mophthorales are actively discharged from the cadaver in order to transmit the
fungus to new hosts. They also show a range of other adaptations to increase
transmission including timing the release of spores to periods of the day
that are most favourable to infection and manipulating host behaviour so
that diseased insects die in exposed positions (Roy et al., 2006). The sexual
Ascomycetes show similar high-level adaptations to the life cycles of particu-
lar host insects; however, the asexual Ascomycetes appear to be more oppor-
tunistic.
The Entomophthorales contain some species that cause natural epizootics
in a range of agricultural pests, although many of these species cannot be
grown readily in vitro and so they are not yet used widely for commercial
biological control. However, these epizootics often reduce the pest below the
economic threshold (Lacey and Kaya, 2006) and some systems have been
developed to exploit them for crop protection. The best example concerns
epizootics of cotton aphids, Aphis gossypii, by N. fresenii in the southern USA.
This fungus causes epizootics that occur at the same times in summer over
large areas and which reduce aphid populations by 80% within 34 days. By
using a simple sampling method, the fungal outbreaks can be predicted up
to 10 days in advance and this gives the farmer the option to withhold insec-
ticide sprays. A Neozygites sampling and advice service is now run for cotton
farmers in ten US states and saves millions of dollars in reduced spray costs
every year (Hollingsworth et al., 1995; Pell et al., 2010).
Entomopathogenic fungi in the asexual Ascomycetes are associated less
commonly with natural epizootics, but they are popular choices for use as
inundative biopesticides because they can be mass-produced easily and
applied using the same equipment that is used to apply conventional chemi-
cal pesticides. Since the 1960s, at least 170 different fungal bioinsecticides
and bioacaricides have been developed (Faria and Wraight, 2007). About
three-quarters of these products are considered to be currently active
(commercially available, registered or undergoing registration). About 50%
have been developed in South and Central America, 20% in North America,
12% each in Europe and Asia, and 3% in Africa (Faria and Wraight, 2007).
These products are used against a wide range of target pests including spe-
cies within the Hemiptera, Coleoptera, Lepidoptera, Diptera, Orthoptera and
Acari. The majority of products are based on the ascomycetes Beauveria bassiana
or Metarhizium anisopliae, but mycopesticides are also available using Beau-
veria brongniartii and the ascomycete genera Lecanicillium, Isaria and others.
They have been used successfully as control agents of insect and mite pests
in glasshouse crops, fruit and eld vegetables. The largest single area of use
is in Brazil, where commercial biopesticides based on M. anisopliae are used
successfully against spittlebugs Mahanarva posticata and Mahanarva mbriolata,
which are major pests of sugarcane. Approximately 750,000 ha of sugarcane
were estimated to be treated with M. anisopliae in 2008, while the fungus
was also applied to 250,000 ha of grassland to control pasture spittlebugs
(Brachiaria spp.) (Li et al., 2010). The fungus is mass-produced on rice grains
and is sold to farmers as fungus-colonized substrate or as a puried spore
powder. The cost of using the fungus is put at US$1260/ha, depending on
the level of pest damage. Part of the reason for the success of Metarhizium
biopesticides is attributed to government support for research and develop-
ment together with the availability of low-cost substrates for mass produc-
tion, which keeps the price of the fungal biopesticide competitive with that
of chemical insecticides (Li et al., 2010). Different strains of M. anisopliae have
also been developed commercially for the control of locust and grasshopper
pests in Africa and Australia, including the desert locust Schistocerca gregaria,
which can cause vast amounts of devastation during outbreak years. These
pests are usually treated with conventional insecticides sprayed over very
large areas, particularly OPs, which raises concerns about environmental
and human safety. When mass-produced Metarhizium spores are sprayed in
an oil-based formulation they cause up to 90% locust and grasshopper
control in 1420 days. The fungus is specic for locusts and grasshoppers
90 Chapter 3
and does not affect non-target organisms. Reasons for its effectiveness
include not only high virulence but also persistence of fungal spores on
the soil and vegetation and the production of new spores on infected
cadavers, which then spread to uninfected insects. The fungus is approved
for use in several African countries and Australia (Lomer et al., 2001) and
the Food and Agriculture Organization (FAO) has recommended that
strategies are developed to bring it into use widely in desert locust control
programmes (FAO, 2007).
Sixty-seven introductions of entomopathogenic fungi have been made
for classical biological control, using 20 fungal species against a range of
invasive insects (Thysanoptera, Hemiptera, Orthoptera, Coleoptera, Diptera,
Lepidoptera) and Acari (Hajek and Delalibera, 2010). The success rate for
establishment of these introductions is estimated at around 60%. There have
been no documented cases where classical introduction of an entomopatho-
genic fungus has caused negative effects to the environment including
signicant mortality of non-target species (Hajek et al., 2007).
We will mention two examples of classical control with entomopathogenic
fungi here. First, the gypsy moth, Lymantria dispar, was introduced to the
USA from France in the 19th century (c.1869) and has caused highly signi-
cant damage to the forest ecosystem in the north-east USA, particularly to
oaks. Entomophaga maimaiga, an entomophthoralean fungus that is specic to
gypsy moth, was introduced from Japan in 1910, but it did not establish
(Hajek, 2004). However, outbreaks of the same species of fungus started to be
observed in 1989. It is not known if these outbreaks are caused by a different
strain of the fungus that was introduced by an unknown mechanism, or
whether they are caused by the strain released in 1910 and took nearly
80 years to establish. The fungus spreads using infective spores, which are
actively discharged from infected larval cadavers. The fungus has caused
repeated outbreaks since 1989 and is spreading, but its effects on gypsy
moth will only be gauged following long-term monitoring. Second, cassava
(Manihot esculenta) is the fourth most important carbohydrate source in the
tropics after rice, sugar and maize. Cassava is native to South America, but is
now grown widely in Africa and Asia. Two major pests were introduced to
Africa from South America: the cassava green mite, Mononychellus tanajoa,
and the cassava mealybug, Phenacoccus manihoti, causing yield losses of up to
85% (Bellotti et al., 1999). Application of synthetic pesticides against these
pests is not an option for low-income African farmers, but classical biological
control has proved successful. The phytoseiid predatory mite Typhlodromalus
aripo, sourced from Brazil, has proved successful against cassava green mite,
while cassava mealybug is being managed using the parasitoid Apoanagyrus
lopezi. Neozygites oridana, an entomophthoralean fungus that causes natural
epizootics in populations of cassava green mite in Brazil, is also being inves-
tigated as a potential biological control agent. Pathotypes of Neozygites from
South America, which suppress populations of M. tanajoa in areas of high
rainfall, are being assessed for release in Africa where native strains of N.
oridana do not cause regular epizootics (Delalibera et al., 1992; Hountondji
et al., 2007).
Pathogenic nematodes
As stated earlier, pathogenic nematodes are not classed as true biopesti-
cides by regulators, although they are used in identical ways to microbial
biopesticides. For this reason we shall mention them now briey. The nem-
atode families Steinernematidae and Heterorhabditidae (commonly termed
entomopathogenic nematodes or EPNs) are highly virulent, obligate para-
sites of insects and are the most important nematodes for biological pest
control. The infective stage is the third-stage nematode, known as a dauer
juvenile (Dauer is German for durability). Heterorhabditid nematodes are
hermaphrodites, and therefore only one dauer juvenile is needed to enter
the host for progeny production. In contrast, steinernematid nematodes are
either male or female and a member of each sex must infect a host for repro-
duction to occur. Host nding by infective juveniles can be an active pro-
cess in response to physical and chemical cues. Dauer juveniles of
steinernematid species infect their hosts by being ingested or enter through
the spiracles and penetrate the tracheae, whereas the heterorhabditids are
able to enter a host by actively burrowing through the cuticle. The EPNs
introduce symbiotic, pathogenic bacteria of the genera Xenorhabdus (in the
Steinernematidae) or Photorhabdus (Heterorhabditidae) into the haemocoel
of their hosts following penetration. Subsequent multiplication of the
bacteria leads to host death, which can occur within as little as 48 h of
infection. Insects infected with nematodes often have abnormal behaviour
compared with uninfected individuals. The nematode can kill its host
without its associated bacterium but is unable to reproduce without it.
After the host has died, the dauer juvenile nematodes mature into adults
and may undergo successive rounds of reproduction depending on the size
of the host, but ultimately the infection cycle terminates with the produc-
tion of large numbers of progeny dauer juveniles. If adequate moisture is
present, the next generation of dauer juveniles leave their hosts through
rents in the cuticle. In the laboratory, they exit from the host 814 days after
infection. The dauer juveniles can remain active for a long period of time
and, under laboratory conditions, some will live for 1 year (Koppenhofer,
2006).
Infection by EPNs requires the presence of free water. Nematodes show
many adaptations to the soil environment and hence they tend to be used for
biocontrol of soil-dwelling pests. They can be mass-produced in liquid sub-
strates on an industrial scale, formulated to improve storage and application
characteristics. They are usually applied to the soil as a drench but may also
be added to crop irrigation pipes. Up to ten commercial EPN inundative
biopesticide products have been available in the UK and over 60 have been
available in Europe, mainly targeted against pestiferous Coleoptera, Lepi-
doptera and Diptera on horticultural crops. For example, a number of prod-
ucts are sold by different companies based on Steinernema feltiae and used for
the control of larvae of the black vine weevil, Otiorynchus sulcatus, a serious
pest of soft fruit and ornamental crops. They have also been used with com-
mercial success against citrus root weevil, against turf pests and on mush-
room crops (Georgis et al., 2006), and have even been shown to give some
92 Chapter 3
control against leaf miners when sprayed on to plant foliage (Hara et al.,
1993).
Phasmarhabditis hermaphrodita is a rhabditid nematode that is a virulent
parasite of a range of terrestrial molluscs, including many key pest species.
Its life cycle is very similar to that of the EPNs, although its association with
symbiotic bacteria is uncertain. It is mass-produced in the same way as EPNs
and is sold as a formulated product for control of slugs and snails. The prod-
uct is comprised of infective juvenile nematodes mixed with clay to make a
water-soluble formulation that kills the host in 421 days depending on the
dose and environmental conditions. It is used in commercial horticulture to
help in slug management on eld vegetable crops and is also sold to amateur
gardeners. It is currently available commercially in 14 countries in Europe. It
has been shown to be native to Chile, but it has not yet been conrmed as
occurring naturally in the USA or Canada and so it is prohibited from sale in
these countries (Rae et al., 2007).
Microbial control of plant pathogens
Plant pathogens are controlled naturally to some degree by a range of micro-
organisms, including fungi, bacteria and viruses. Some of these are being
used for biological control using augmentation, classical and conservation
strategies. The target plant pathogens include fungi, oomycetes, bacteria,
viruses and plant parasitic nematodes. The development of microbial bio-
pesticides of plant pathogens is being driven by the increasing withdrawal of
synthetic fungicides following government reviews of their safety, but
equally important is the worldwide ban on the use of methyl bromide, which
was used widely as a soil sterilant but is being withdrawn because it contrib-
utes to depletion of ozone in the atmosphere. The commercialization of
microbial biopesticides as control agents of plant pathogens and plant
parasitic nematodes is a relatively young endeavour; effective products for
disease control have only become commercially available to any extent since
the mid-1990s (Whipps and Davies, 2000). In 2000, around 80 products were
on sale or close to market (Whipps and Davies, 2000).
The microorganisms exploited for plant disease biocontrol have a wide
range of modes of action. There are two broad classes. Microbial antagonists
occupy the same ecological niche as the target plant pathogen and interact
directly with it. The mechanisms of interaction include parasitism, competi-
tion for space, water or food, or chemical warfare using antibiotics or other
secondary metabolites that harm the target pathogen. The second class
involves an indirect effect in which the control agent induces a resistance
response in the plant that gives it protection against virulent plant patho-
gens. The inducer for this form of control may use a particular strain of the
plant pathogen that has low virulence, a different species of microorganism
or a natural product, as well as the plant itself. This is very different from the
microbial control approach used against insects, which currently relies
exclusively on using virulent parasites to directly kill insect pests.
Many microbial antagonists of plant pathogens have more than one way
of restricting the development of a target pest. A number of species of the
fungal control agent Trichoderma, for example, are used against soil-borne
plant pathogenic fungi. Trichoderma species are able to parasitize plant
pathogenic fungi in the soil, they also produce antibiotics and fungal
cell-wall-degrading enzymes, they compete with soil-borne pathogens for
carbon, nitrogen and other factors, and they can also promote plant growth,
possibly by the production of auxin-like compounds (Verma et al., 2007;
Vinale et al., 2008). Trichoderma is a common soil fungus and naturally grows
in the rhizosphere. Multiple modes of action confer many benets in terms
of disease control, because Trichoderma gives good control in a range of
conditions. However, it can create problems for the authorities that have to
regulate its production and use. Many Trichoderma products have been sold
on the basis of their plant growth-promoting properties, rather than as plant
protection products, and so have escaped scrutiny from regulators in terms
of their safety and efcacy.
At the microbial scale, plants present a very diverse set of environments
for the microorganisms that are associated with them. The environmental
conditions on the leaf surface are very different to those in the root zone, for
example. The leaf surface is devoid of many microorganisms as conditions
are not conducive to growth and survival. Water and nutrients are in scarce
supply, while low humidity and high levels of ultraviolet radiation limit the
germination of fungal and bacterial spores. In contrast, the root zone has
freely available water and is bathed in large amounts of readily utilizable
carbon secreted by root cells. As a result, there are large populations of taxo-
nomically diverse microorganisms inhabiting the root zone and competing
for resources. It is critical, therefore, that the ecology of the plant pathogen is
understood in detail if biocontrol is to be successful.
Microbial antagonists
A number of microbial antagonists are being used as commercial products
against plant pathogenic fungi and oomycetes (Table 3.1). Microbial control
products have been developed for use against soil-borne plant pathogens
and pathogens that infect the above-ground parts of plants. The most widely
used fungal control agents in the soil are species of Trichoderma, such as
Trichoderma harzianum, which is an antagonist of Rhizoctonia, Pythium,
Fusarium and other soil-borne pathogens (Harman, 2005). Trichoderma is a
parasite of a range of fungi and oomycetes in the soil, but it also inhibits
the growth of other organisms by the production of toxic metabolites and
cell-wall-degrading enzymes. Specic recognition reactions between para-
site and host mediate the release of antimicrobial metabolites by the parasite.
Other fungal parasites and antagonists include Gliocladium virens and Conio-
thyrium minitans. The latter is applied to the soil to kill Sclerotinia sclerotiorum,
an important disease of many agricultural and horticultural crops such as
oilseed rape, lettuce, carrots, beans and brassicas (Whipps et al., 2008).
Bacterial agents can also be used for control of soil-borne diseases. Crown
gall, caused by Agrobacterium tumefaciens, is a serious disease of a wide range
94 Chapter 3
of dicotyledonous plants including pome fruits, vines, ornamentals and veg-
etables. Bacterial infection causes the formation of tumours in root tissue.
Seed and seedlings can be treated with the K84 strain of the non-pathogenic
species Agrobacterium radiobacter. K84 colonizes root tissues and prevents
occupation by A. tumefaciens, using an antibiotic (Penalver et al., 1994).
Specic strains of Bacillus subtilis can also confer protection against some root
pathogens, while a number of Pseudomonas species, including Pseudomonas
uorescens and Pseudomonas aureofaciens, reduce damping off and soft rots
(Kloepper et al., 2004; Haas and Dfago, 2005; Choudhary and Johri, 2009).
Fungal antagonists used against pathogens that infect leaves and stems
include: Lecanicillium, which is primarily an insect pathogenic fungus, but
some strains have activity also against other fungi; Ampelomyces quisqualis,
which is used against mildews; and Nectria inventa and Gonatobotrys simplex,
which are parasites of Alternaria (Kiss et al., 2004). The fungus Phlebiopsis
gigantea is used to control Heterobasidion annosum, a fungal pathogen that
causes rots in freshly cut stumps of pine trees and which can spread subse-
quently to intact trees by root-to-root contact. Phlebiopsis spores are painted
on to tree stumps or are incorporated in the lubricating oil used in chain-
saws. The fungus occupies the same tissues as Heterobasidion and outcompetes
it, but causes no damage to the trees (Pratt et al., 1999).
There are also a number of bacterial species that are used as control
agents of plant pathogens infecting above-ground parts of plants. Species of
Bacillus, Pseudomonas and Streptomyces can prevent colonization of leaf and
stem tissue by plant pathogens (Berg, 2009). The activity of these agents is
often due to antibiosis brought about through the action of bacterial second-
ary metabolites. Usually, several kinds of secondary metabolites are pro-
duced. Production of metabolites is strain dependent, i.e. different strains of
the same species of bacterium can produce different types of metabolites
with different effects on target pathogens. Strain selection is therefore a
critical part of developing bacterial agents as biopesticides.
Microbial antagonists can be formulated as dusts, granules or liquid
suspensions for application to soil, either directly to the roots of plants or
in the soil ahead of planting. Antagonists used on leaves, stems or har-
vested fruit are usually applied as conventional sprays. However, novel
application systems are also being developed. Honeybees, used commer-
cially for pollination of blueberries, transport the plant pathogenic fungus
Monilinia vaccinii-corymbosi between blueberry owers, leading to berry dis-
ease. However, the risk of the disease can be reduced signicantly by using
the bees as ying doctors and treating them with the bacterial biopesticide
B. subtilis, which is dispensed from a device tted to the entrance of bee hives
and which the bees vector to blueberry owers (Dedej et al., 2004).
Microbial antagonists are also used as control agents of postharvest
diseases, mainly against the causal agents of rots in harvested fruits and veg-
etables. Yeasts, lamentous fungi and bacteria have all been used (Spadaro
and Gullino, 2004). Mode of action is not always clear, although competition
with the pathogen for space and nutrients is thought to be important,
alongside antibiosis. Sharma et al. (2009) list over 40 species of microbial
antagonists that have been demonstrated in experiments to give successful
control of postharvest disease of fruits and vegetables. Common target patho-
gens in these experimental programmes included Botrytis cinerea, Penicillium
species (e.g. Penicillium digitatum, Penicillium expansum, Penicillium italicum)
and Mucor piriformis. At present, however, only nine products are available
commercially across the world (Sharma et al., 2009). Of these, the most widely
used are based on A. quisqualis and B. subtilis. Application of the control agent
may be made preharvest, to combat latent infections acquired in the eld,
although it is not considered a commercially viable strategy. Postharvest
application is more practical, and the inoculum is usually applied as sprays
or as a dip.
Developers of microbial biopesticides of plant pathogens have tended,
quite understandably, to concentrate on species of microbial antagonists that
are easy to culture and mass-produce, although it has been pointed out
(Whipps and Davies, 2000; Alabouvette et al., 2006) that if commercialization
of these agents is done according to a chemical pesticide model, without
proper consideration of the ecological interactions involving the control
agent, the target pathogen, the crop plant and the environment, then poor or
inconsistent levels of control are certain to occur, which would be damaging
to the whole concept of biological control.
Microbial control of plant parasitic nematodes
Plant parasitic nematodes are susceptible to fungal and bacterial pathogens,
a small number of which are available as commercial biopesticides. Nema-
tophagous fungi include species that trap motile nematodes in the rhizo-
sphere using specialized hyphal organs, such as Arthrobotrys oligospora and
Arthrobotrys dactyloides. Endoparasitic fungi, such as Pochonia chlamydosporia
(= Verticillium chlamydosporium) are able to infect female cyst nematodes and
their eggs (Kerry, 2000). Pochonia chlamydosporia can be mass-produced in
vitro, and some strains are able to grow saprotrophically within the rhizo-
sphere, making it a potentially valuable augmentation biopesticide. How-
ever, the development of microbial control agents of plant parasitic nematodes
appears to be relatively slow. Dong and Zhang (2006) list only nine products
that have been commercialized, based on six different fungal or bacterial spe-
cies. They attribute this lack of products partly to inconsistent performance
in the eld, and it is likely that product development is being held back by a
lack of knowledge of the complex interactions that occur between nematode,
control agent, the plant and the soil, and in particular the rhizosphere.
Using microbes to induce plant defence responses against pathogens
Plants have both constitutive and inducible forms of defence against plant
herbivores and pathogens. When a plant is infected by a pathogen, it is often
able to detect it and mount a defence by producing a range of antimicrobial
compounds. Such induced responses are thought to have a selective advan-
tage over constitutive defences because they reduce trade-offs between the
allocation of resources for defence and other processes, such as growth and
reproduction. Induced defences are initiated by elicitor molecules from the
96 Chapter 3
pathogen, which include substances such as pathogen toxins, proteins
and cell-wall constituents, such as glycopeptides, chitin and glucans. Binding
of the elicitors to receptor molecules located on plant cell membranes initi-
ates a biochemical cascade that results in the up-regulation of genes control-
ling the production of a range of defence chemicals, such as phytoalexins and
antimicrobial proteins. Basal-level induced immunity to virulent pathogens
is afforded by a non-specic pathogen recognition system that utilizes
surface receptors (so-called pathogen-associated molecular pattern (PAMP)-
triggered immunity, PTI) (Vlot et al., 2009). Plants also exhibit induced
responses that are specic to particular pathogens, known as effector-triggered
immunity (Vlot et al., 2009). These specic responses are rapid and often take
the form of a hypersensitive reaction, in which reactive oxygen species and
pathogenesis-related defence proteins are synthesized by the plant at the site
of infection, while the plant also causes the death of infected cells in order to
contain the pathogen and prevent the disease spreading. The hypersensitive
response only occurs in specic hostpathogen combinations and requires
that a particular host resistance protein recognizes a matching avirulence
protein from the pathogen.
Two key discoveries about plant inducible defences have enabled them
to be exploited for pest management (Walters et al., 2007): (i) inducible
defences can be triggered in plants by avirulent strains of a pathogen, by
non-pathogenic microbes or by chemicals; and (ii) inducible defences are not
just conned to the site of contact with the elicitor, but are also induced in
distal parts of the plant via a chemical message. This helps to protect the
plant against subsequent infection by other plant pathogens. Two different
types of plant inducible defence have been characterized based on differ-
ences in the chemical signalling pathways involved. They can both be
induced articially by treating the plant with microbial agents or with
chemical elicitors. Once induced, long-lasting partial resistance is conferred
against a wide range of diseases. Systemic acquired resistance is induced in
nature by necrotrophic pathogens. The resistance rst develops as a localized
hypersensitive response and is induced elsewhere in the plant by chemical
signals based on salicylic acid. Systemic acquired resistance can also be
induced using specic chemical agents, some of which are available on
a proprietary basis. In contrast, induced systemic resistance is triggered
in plants by non-pathogenic, plant growth-promoting rhizobacteria.
Induced systemic resistance is regulated by jasmonic acid and ethylene
pathways. Induced systemic resistance acts independently of systemic
acquired resistance although the two mechanisms share a common regula-
tory protein.
Both induced systemic resistance and systemic acquired resistance are
exploited commercially. For example, the synthetic compound probenazole
has been used in Asia since 1975 to manage the rice blast pathogen Magna-
porthe grisea using systemic acquired resistance (Walters and Fountaine,
2009). Probenazole is applied during seedling production or to rice elds
after planting, where it is absorbed by plant roots and translocated to the
rest of the plant, and can control rice blast for up to 70 days (Iwata, 2001).
Other systemic acquired resistance products include acibenzolar-S-methyl
(ASM) and chitosan, a polymer present in insect cuticle and fungal cell
walls (Walters and Fountaine, 2009). In practice, the level of disease protec-
tion conferred by these products can vary widely, and is believed to be
dependent upon a broad range of complex, interacting factors including
plant genotype, environmental conditions, crop nutrition and whether the
plant has already been induced by naturally occurring biotic and abiotic
factors in the eld prior to the application of the compound (Walters and
Fountaine, 2009).
Symbiotic associations between arbuscular mycorrhizal fungi and
plant roots are widespread in nature and improve plant nutrition, drought
tolerance and pest resistance (Bending et al., 2008). Many agricultural
crops are mycorrhizal and there is widespread if equivocal evidence that
crops benet from the association by induced resistance to plant diseases
(Gosling et al., 2006). Intensively managed agro-ecosystems are generally
impoverished in arbuscular mycorrhizal fungi. However, new approaches
could be developed to reverse this, such as changes to farm management
practices or applications of fungal inoculum to the soil. This could be a
very practical way of boosting the ability of crop plants to withstand
disease.
Microbial control of weeds
Plant pathogens can be exploited as microbial control agents of weeds.
Biological weed control has been done successfully using the augmentation
strategy (where the agents are referred to as bioherbicides) and classical
biological control. However, only a small number of examples have been put
into practice to date. Synthetic chemical herbicides are inexpensive, effective
and widely available, which makes it difcult for bioherbicides to compete
unless they can nd a niche market. Between 1980 and 2001, only eight
bioherbicides were registered worldwide (Charudattan, 2001). However,
although the market is small, it has been argued that biological weed control
must be considered alongside all other potential management tools given
the diversity and extent of weed problems (Charudattan, 2001), and it has a
particular role for key weed species that have evolved herbicide resistance,
such as blackgrass Alopecurus myosuropides in Europe and annual ryegrass
Lolium rigidum in Australia (Hallett, 2005). Part of the reason for the lack of
commercial bioherbicide products may be the fact that there are few aca-
demic or commercial organizations in the world with the critical mass of
scientic expertise necessary to go all the way from basic research to product
development (Ash, 2010).
No bioherbicide products are currently available in Europe, but two
products, Collego and DeVine, have been used in the USA since the 1980s.
These are based on strains of the fungus Colletotrichum gloeosporioides and the
oomycete Phytophthora palmivora (Charudattan, 1990). Collego has been sold
since 1982 as a bioherbicide of northern jointvetch, Aeschynomene virginica, in
98 Chapter 3
soybeans and rice (te Beest et al., 1992). Northern jointvetch causes seed
contamination at harvest; it reduces rice yields by up to 20% and causes
around 10% of the crop to be rejected because of low quality. The strain of C.
gloeosporioides used in Collego has high virulence, is able to kill seedlings
within several weeks and the commercial product gives over 90% control
when used correctly by growers. It is integrated into rice IPM systems, which
includes proper timing of fungicide applications to ensure that they do not
inhibit the bioherbicide. Phytophthora palmivora has been used for nearly
30 years to control stranglervine (also known as milkweed vine), Morrenia
odorata, in Florida citrus groves. Stranglervine is an alien, invasive species
that was introduced to Florida from South America as an ornamental plant.
It climbs up citrus trees and competes with them for water, light and
nutrients. DeVine uses a highly virulent strain of P. palmivora isolated from
diseased stranglervines in Florida (te Beest et al., 1992). It is not specic to
stranglervine, and in glasshouse experiments it was found also to infect a
range of crop plants including pea, squash, watermelon, tomato and potato
when applied at high inoculum levels in sterile soil. However, it was argued
that these represented an extreme case and that in the eld these plant
species would not be exposed to direct applications at the same concentra-
tions of inoculum. DeVine is highly effective; an application provides
95100% control that persists for at least 1 year (Kenney, 1986; te Beest et al.,
1992).
One of the rst notable examples of using a pathogen for classical weed
control concerns the rust fungus Puccinia chondrillina for control of skeleton
weed Chondrilla juncea, a serious invasive weed of agriculture in south-east
Australia (te Beest et al., 1992). There is a very high degree of specicity
between the weed host and the pathogen, so that each strain of the weed is
susceptible only to a particular co-evolved strain of fungus. An Italian strain
of the fungus that was highly virulent to the weed was released in 1971,
and it spread rapidly after release. Two Italian strains were also released in
California and Oregon in the USA for control of skeleton weed there. These
pathogen strains have now colonized the entire Pacic north-west. Pathogen
infection reduces plant biomass and seed production, and 90% weed mortal-
ity can occur when conditions are favourable (te Beest et al., 1992). Another
rust fungus, Uromycladium tepperianaum, was introduced to control the
Australian acacia tree, Acacia saligna, a serious invasive weed in the Cape
Fynbos in South Africa, a region with a unique and particularly diverse
native ora. The fungus was introduced in the late 1980s and reduced tree
density by 95% in 9 years (Charudattan, 2001). Classical control of weeds has
also proved benecial in Hawaii, where ve major biological control projects
against weeds have been done since the late 1960s (Trujillo, 2005). The
economic and ecological benets of these programmes have been consider-
able. For example, control of just one weed species, Senna surattensis, with a
bioherbicide based on the fungus Acremonium, is reported to have saved the
Hawaiian cattle industry from collapse in the 1970s, and the total economic
benet of the Hawaiian weed biocontrol programme is valued at greater than
US$100 million (Trujillo, 2005).
Natural Compounds
Animals, plants and microorganisms synthesize a wide array of chemical
compounds that have adaptive signicance in terms of defence against pred-
ators, locating sources of food, nding mates, etc. The importance of some of
these compounds to the ecology of plants, pests and their natural enemies is
now relatively well characterized, and methods for exploiting them within
IPM are being developed.
Botanicals: direct chemical defences used by plants against herbivores
Plants produce a wide variety of secondary metabolites that deter herbi-
vores from feeding on them. These chemicals include terpenoids (for exam-
ple volatile oils such as limonene), phenolic compounds (such as tannins),
alkaloids (such as nicotine) and glucosinolates (such as mustard oil). When
extracted and concentrated, some of these plant compounds can be used as
pesticides. About 50 different botanical active substances are registered as
plant protection products in the USA, but only 11 are registered in the EU
(Table 3.1).
We have mentioned previously that one of the rst commercial pesti-
cides to be introduced was nicotine. Nicotine is a potent non-specic insecti-
cide that is synthesized by plants from the genus Nicotiana (including the
commercial tobacco plant Nicotiana tabacum) as a defence against insect her-
bivores. It binds to acetylcholine receptors and affects neurotransmission. At
normal concentrations in Nicotiana plants it acts as a feeding deterrent, but is
insecticidal at the higher concentrations found in Nicotiana plant extract. Nic-
otine is also a potent mammalian toxin, which goes to illustrate that just
because a pesticide is natural, it does not necessarily mean that it is safe.
However, there are other phytochemical insecticides which are safe to use
and which are exploited commercially. They are often referred to as botani-
cals. The market for botanical pesticides is currently limited, probably
because of the low efcacy of the products and the expense of mass produc-
tion compared with synthetic chemical pesticides. In developed countries,
they tend to be used most in organic farming. The most widely used
botanical compound is neem oil, extracted from seeds of the neem tree,
Azadirachta indica, which is native to the Indian subcontinent (Schmutterer,
1990). Neem oil contains two components with insecticidal activity,
azadirachtin and salannin. They function both as an insect feeding deterrent
and a growth regulator, preventing moulting in immature insects that ingest
them (Atawodi and Atawodi, 2009). Neem oil has been used as a traditional
insecticide in India for over 4000 years. Neem oil has a low mammalian toxic-
ity and has some systemic activity when applied to plants. A number of neem
oil insecticidal products are used in India and elsewhere. However, neem oil
is expensive to mass-produce compared with synthetic chemical pesticides,
and it has a low efcacy. Koul (2008) estimates that 1030 kg of neem seeds
are needed to treat 1 ha of land, at a cost of US$520/ha. Elsewhere, research
100 Chapter 3
on the effectiveness of low-molecular-weight volatile plant oils, also known
as essential oils, against insect and mite pests has been done with oils from
over ten different plant species. For example, essential oil from Chenopodium
ambrosioides was shown to be effective at controlling fungus gnats, Bradysia
coprophila, on ornamental plants (Cloyd and Chiasson, 2007). The efcacy of
commercially available products against arthropod pests can vary depend-
ing upon the active ingredient, and while some products can give high levels
of control, others may have low efcacy or be phytotoxic (Cloyd et al., 2009).
It is important therefore that independent evaluations are made of the
effectiveness of these products including phytotoxicity.
Other botanical compounds included the pyrethrins, which are the active
compounds of pyrethrum, a powder produced from owers of Chrysanthe-
mum cinerariaefolium. Pyrethrins kill most insect species, are active at low
concentrations and give a rapid knockdown effect (Silverio et al., 2009). The
product has a low mammalian toxicity, but as we have mentioned previously
it is toxic to aquatic animals and it also degrades rapidly after application.
While this is an attractive property from an environmental point of view,
as it reduces the chances of non-target organisms being affected, it does
lower the overall effectiveness against target insects. The poor persistence of
pyrethrum was the main driver for the development of synthetic forms of the
chemical with better environmental performance. Rotenone is a avonoid
insecticide active against leaf-feeding insects and extracted from tropical
legumes in the genera Derris and Lonchocarpus (Guleria and Tiku, 2009).
Rotenone works as a contact and stomach-acting insecticide. However, it is
moderately toxic to mammals and very toxic to sh.
Pesticides based on microbial products
Two highly active pesticides are available based on microbial products.
Strictly speaking they fall within our denition of a biopesticide; however, the
regulatory authorities have evaluated and approved them as conventional
chemical pesticides. Spinosad is a mixture of two macrolide compounds, spi-
nosyn A and D, that are synthesized by a soil actinomycete, Saccharopolyspora
spinosa, which was collected from a rum still in the Caribbean (Mertz and Yao,
1990). The level of insecticidal activity is comparable to that of synthetic pyre-
thrins, it has a very low mammalian toxicity and residues degrade rapidly in
the eld. A review of studies of the impact of Spinosad on natural enemies
showed that it is not harmful to predators but that it can be moderately harm-
ful to parasitoids (Williams et al., 2003). Spinosad kills insects by causing
hyperexcitation of the central nervous system (Sparks et al., 2001). Farmers
and growers used it widely against western ower thrips, lepidopteran and
dipteran pests following its introduction in 1997, but unfortunately resistance
has already developed in some of these pests (Herron and James, 2005; Bielza
et al., 2007). In the diamondback moth, one of the most important pests of
brassicas worldwide, resistance is determined by an incompletely recessive
gene mutation (Baxter et al., 2010).
Abamectin belongs to a class of macrocyclic lactone compounds, the
avermectins, that are synthesized by the soil actinomycete Streptomyces
avermitilis strain MA-4860 isolated from Japan in 1976 (Lasota and Dybas,
1991). These compounds affect sodium-gated membrane channels in nerve
cells that utilize -aminobutyric acid as a neurotransmitter. Abamectin is
degraded rapidly in the environment, including in the soil, in water and on
plant surfaces, it is not bioaccumulated in the food chain and therefore is
considered not to represent an environmental hazard. It is active against a
range of pest species but it has particularly good activity against mites,
including many species, such as the two-spotted spider mite and the citrus
rust mite, which could not be controlled with conventional acaricides because
of resistance. Unfortunately, resistance has developed now also to abamectin
(Sato et al., 2005; He et al., 2009).
Semiochemicals
A semiochemical is a chemical signal produced by an organism that evokes a
change in the behaviour of an individual of the same or a different species.
Semiochemicals are divided into two broad classes, allelochemicals and
phero mones. Allelochemicals are substances produced by one species and
which cause a response in individuals of another species. They are catego-
rized according to the effects they have on the emitter and the receiver: (i)
allomones are allelochemicals that are benecial to the organism that has
emitted them, but are detrimental to the receiving organism; (ii) in contrast,
kairomones are benecial to the receiver and detrimental to the emitter; while
(iii) synomones are attractive to both emitter and receiver. Pheromones are
chemicals released by an organism that affect individuals of the same species.
Both pheromones and allelochemicals are being used for pest management.
Exploitation of allelochemicals against invertebrate pests
Plants produce volatile allelochemicals in response to feeding or egg laying
by insect herbivores (for this reason they are often referred to as herbivore-
induced plant volatiles, HIPVs). They include methyl jasmonate, methyl
salicylate and hexenyl acetate. Note that both the jasmonate and salicylate
compounds were discussed earlier in this chapter in relation to plant defence
against pathogens. These signalling molecules are produced by a taxonomic-
ally diverse range of plant species, which suggests that they constitute an
evolutionarily ancient form of plant defence. In the same way that they act
as a messenger to prime distal parts of the plant against pathogen infection,
they also spread systemically from wound sites induced by invertebrate
feeding, stimulating the synthesis of phytochemicals that deter feeding
and oviposition in other parts of the plant. They also stimulate the production
of deterrent compounds in neighbouring plants (Thaler, 1999; Reddy and
Guerrero, 2004). They are also able to recruit natural enemies as bodyguards
when under attack: insect predators and parasitoids have evolved the ability
to detect HIPVs and use them to detect prey. Different plant species produce
102 Chapter 3
different blends of volatiles according to the type of herbivore that feeds
upon them.
This knowledge can be exploited for pest control. For example, James et al.
(2005) showed that stick traps baited with hexenyl acetate, methyl jasmonate
or methyl salicylate increased the abundance of natural enemies on the crop.
The precise mechanism by which natural enemies are attracted has yet to be
elucidated, but it is hypothesized that crop plants respond to a general warn-
ing signal from the HIPV and emit their own specic blends of volatiles to
attract in natural enemies.
Insect pheromones
There are three main functional types of insect pheromone: (i) sex phero-
mones, produced by one sex to attract the other; (ii) aggregation pheromones,
which cause individuals to group together for the purposes of reproduction,
feeding or hibernation; and (iii) alarm pheromones, such as the sesquiter-
pene -farnesene, which is produced by aphids when attacked by predators
or parasitoids and causes the dispersal of other aphids in the vicinity (Kunert
et al., 2005). Nowadays, it is possible to synthesize a wide range of insect
pheromones and use them for crop protection. These synthetic molecules are
chemically identical to the ones found in nature. Each insect species has its
own particular blend of sex pheromones; so considerable research effort may
be required to produce exactly the right blend of synthetic pheromones for
use in the eld. Sex pheromones are used for both monitoring and pest
control. For monitoring, a small number of lures are deployed in the eld,
each comprising a pheromone dispenser with a sticky trap. The numbers of
trapped insects provide information on ight activity, dispersal, population
size and so on. The data are used to inform the timing of applications of
pesticide sprays or other therapeutic agents. Sex pheromones are also used
for pest control. This can take the form of mass trapping, where pheromone
dispensers attract insects to physical traps. Mass trapping is used, for exam-
ple, to control banana weevil in commercial banana plantations (Reddy et al,
2009). Sex pheromones can also be utilized in lure-and-kill systems, in which
the pheromone is used to attract the insect to a device containing a pesticide
(El-Sayed et al., 2009). The advantage of this system is that the amount of
pesticide used is signicantly less than in conventional spraying, and keep-
ing the pesticide within the lure means that there are no issues of contamina-
tion of the crop plant. There are also lure-and-infect systems, in which the
pest is treated with a microbial pathogen such as a baculovirus or a fungus.
However, the most highly developed and widely used strategy for using sex
pheromones is mating disruption. Large numbers of female sex pheromone
dispensers are deployed within a eld to disorientate males and disrupt their
ability to nd females for mating. Worldwide, mating disruption is used on
over 660,000 ha (Witzgall et al., 2008). One of the most successful examples is
the use in apple orchards of the codling moth female sex pheromone, (E,E)-
8,10-dodecadienol (known as codlemone), which is used on about 160,000 ha
worldwide. Because there is a low threshold for economic damage to the
apple crop, the pheromone is most effective at low to medium population
levels. If the moth population exceeds 1000 overwintering larvae per hectare
then the pheromone needs to be combined with other management tools,
such as the codling moth baculovirus biopesticide (Witzgall et al., 2008).
Insect pheromone formulations are non-toxic to mammals and are recog-
nized as low-risk products by regulatory authorities. The US EPA, for exam-
ple, does not require toxicological testing for straight-chain lepidopteran
pheromones (SCLPs) if applied at less that 150 g/acre (Weatherston and
Stewart, 2002). Not all insects produce pheromones that can be utilized for
pest management, and even if a pheromone is available there may only be
limited opportunities to control a pest due to agronomic factors or the pests
behavioural ecology. However, sex pheromones clearly have much to offer in
terms of making crop protection more sustainable.
Use of Biopesticides in Integrated Pest Management
Modern IPM is an ecologically based discipline. Successful IPM programmes
should take into account the following: the biological characteristics of the
pest; the causes of the pest outbreak; the presence of other pests; the attributes
of the available control agents including their safety, efcacy, environmental
impact and compatibility with other IPM tools; the characteristics of the crop
and its environment; the nancial costs of the available pest control tactics;
and social factors (for example, are the available control strategies acceptable
to society?). It must be remembered that the number and diversity of species
that make up the pest community on a particular crop are critically impor-
tant in determining the overall pest management strategy. Writing about
the use of microbial biopesticides in IPM, Lacey and Shapiro-Ilan (2008) point
out that pest management agents tend to be considered as stand-alone treat-
ments and that the ways in which they interact with the rest of the agro-
ecosystem are often overlooked. This would appear to be a hangover from
the industrial approach to crop protection. Some biopesticides work well as
stand-alone treatments, such as M. anisopliae used for control of locusts and
grasshoppers (Lomer et al., 2001). But many biopesticides, by their nature,
are unlikely to work effectively as stand-alone treatments; however, their
selectivity and safety mean that they can contribute meaningfully to incre-
mental improvements in pest control in ways that make agriculture more
sustainable (Lacey and Shapiro-Ilan, 2008). The development of systems that
integrate biopesticides with other control measures is essential for the future
of IPM. This vital work is complex, challenging and long term, but it is also
true to say that it is unglamorous and does not receive the attention it deserves
from governments and other research funders.
We have already seen that sophisticated IPM systems are used widely in
protected crops, particularly for the control of insect and mite pests. In
Europe, the industry is supported by about 25 biological control companies
including the worlds three largest that supply natural enemies and technical
support (van Lenteren, 2000). The costs of IPM are reported to be competitive
with chemically based control (van Lenteren, 2000). Fungal and nematode
104 Chapter 3
biopesticides are incorporated into these systems. As an illustration, a lead-
ing grower of glasshouse ornamental crops in the UK routinely uses 11
different biocontrol agents including parasitoids (Aphidius, Dacnusa, Diglyphus,
Encarsia) and predators (Aphidoletes, Amblyseius, Hypoaspis, Phytoseiulus) as
well as entomopathogenic nematodes and the insect pathogenic fungus
Lecanicillium. The system is based on routine, detailed monitoring of pest
abundance, and a computerized system is employed to keep a check on the
amount and cost of biocontrol used per week, month and year for each crop
grown. Where possible, mechanized systems of biocontrol application are
used to save costs. The whole system keeps application of chemical pesticides
to a minimum and works out at about three pence per plant (M. Holmes,
personal communication).
Research has shown that biopesticides can be used as an effective second
line of defence with predators against western ower thrips and spider mites
on greenhouse crops ( Jacobson et al., 2001; Chandler et al., 2005). These pests
are routinely managed using trickle release applications of predatory mites.
However, there are invariably periods in the production season when the
pest population starts to outstrip the ability of the predator to control it. This
may be caused by a change in environmental conditions such as tempera-
ture, the application of a chemical pesticide, or because some crops such as
tomato (which has leaves covered in thick, glandular trichomes) are not
very conducive to easy predator movement. In the past, synthetic chemical
pesticides have been used in such situations, but their use has become
severely restricted through the evolution of resistance. However, this gap can
be replaced by using biopesticides in some cases. For example, the entomo-
pathogenic fungus B. bassiana applied as a supplement to the predatory
mite Phytoseiulus persimilis against spider mites, T. urticae, can give up to 97%
control of eggs, nymphs and adults seven days after spraying (Chandler
et al., 2005). Growers in countries where Beauveria is available commercially
are now adopting this strategy. The ability to use fast-acting, supplementary
treatments such as Beauveria can make the difference between success and
failure in greenhouse IPM (R. Jacobson, personal communication).
Perhaps the key point to make about IPM in greenhouse crops is that
multiple management tactics, including biopesticides, are integrated across a
wide range of different groups of pests and are also integrated with agro-
nomic practice. This makes for a highly advanced system. For other crop
sectors, IPM where it is practised at all is still at the stage of integrating
different pest control tactics for the same pest or group of pests. Getting
biopesticides to work effectively for crops grown outdoors is signicantly
more of a challenge than for crops grown under protection. An important
area for future activity is going to be making biopesticide products avail-
able for eld crops to be used in IPM. In Chapter 2 we saw how Bt has been
incorporated into a biocontrol-based IPM system for outdoor tomato pro-
duction in the USA. Bt can also be a valuable tool for growers against cater-
pillar pests on a range of other eld vegetable crops including brassicas,
sweetcorn, pepper, aubergine and potato (Rowell and Bessin, 2005). The fact
that the Bt products used have no negative effect on the predator and
parasitoid natural enemies of caterpillar pests is an important plus point
for IPM. The mycoparasitic fungus C. minitans is used as a biopesticide of
sclerotinia disease caused by S. sclerotiorum, which affects a wide range of
crops. At present the mycoparasite is used mainly in greenhouses, but the
future aim of the various biopesticide companies involved with it is to
market it also for outdoor use including on oilseed rape, for which sclerotinia
can be a major problem. Integrating Coniothyrium into IPM will be essential.
Its effectiveness can be improved in IPM, for example by combining its appli-
cation with organic amendments such as lignin or with reduced fungicide
applications (van Beneden et al., 2010).
There are encouraging prospects for the incorporation of biopesticides
into IPM systems in orchard and soft fruit crops. Because these crops are
eaten raw and unprocessed, there is considerable demand from retailers
and consumers for reduced use of chemical pesticides. On the supply side,
a range of reliable products is becoming increasingly available. Bt, baculo-
viruses and entomopathogenic nematodes are being used against a range
of lepidopteran pests of pome and stone fruits such as tortrix moths and
fruit borers. The entomopathogenic nematodes Steinernema carpocapsae,
Steinernema riobrave and Heterorhabditis indica are being used for manage-
ment of citrus root weevils (Coleoptera) in the USA. Granulosis virus-based
biopesticides have been available since the 1980s against codling moth,
C. pomonella (Lepidoptera), which is the most important pest of apples
worldwide (Lacey and Shapiro-Ilan, 2008). Codling moth larvae burrow
into developing apples to feed, causing signicant economic damage to the
crop if left uncontrolled. The CpGV virus is applied against neonate larvae
before they have entered the fruit. It is highly virulent and has a rapid speed
of kill, although some cosmetic damage may still occur from larvae that
burrow into the fruit surface before death. Commercial CpGV products are
available in most European countries, in North and South America, as well
as in South Africa, Australia and New Zealand ( Jehle, 2008). Resistance
management is required as some codling moth populations have been
reported in Europe following repeated applications over many years
(Asser- Kaiser et al., 2007). Integrated systems are being used successfully
against resistant moths using a combination of CpGV with pheromones for
mating disruption. This can be reinforced by the application of entomopatho-
genic nematodes to soil, leaf litter, etc. to control overwintering diapausing
pupae (Lacey and Shapiro-Ilan, 2008).
Biopesticides are not being used much at all on broad-acre crops in
industrialized countries, as in general they cannot yet compete with cheaper,
more effective synthetic pesticides. Pest management in broad-acre crops
in these countries is based largely on stand-alone tactics for each pest,
and hence the lack of a pre-existing IPM framework is likely to be a signi-
cant barrier to biopesticide uptake. However, where pesticide use becomes
untenable, then biologically based IPM is adopted. As an example, alterna-
tive control mechanisms play an important role in Colorado potato beetle
management in North America. The most widely used natural enemies
are the entomopathogenic fungus B. bassiana and sprays of Bt, and there is
106 Chapter 3
evidence that the two entomopathogens work synergistically when applied
together (Wraight and Ramos, 2005). The egg parasitoid Edovum puttleri,
used according to an augmentation strategy, can give about 50% parasitism
in the eld. Because overwintering adults disperse to the crop by walking,
and hence do not cover large distances, crop rotation can be a viable form of
cultural control (Hare, 1990). Despite considerable work on breeding for
resistance, no conventionally bred resistant crops are available. Crops engi-
neered to express Bt endotoxin were made commercially available in the
USA in 1995 but were withdrawn from use in 2000 because of consumer
concerns about GM crops (Romeis et al., 2006). Research is under way to
characterize wild relatives of the cultivated potato that have Colorado potato
beetle resistance and which could be used in a crop breeding programme.
One promising nding has been that resistance to Colorado potato beetle is
associated with particular taxonomic groups of Solanum, which should make
it more cost effective in future to screen the large number of candidate plant
accessions available ( Jansky et al., 2009). Resistant species tend to produce
foliage with high levels of glycoalkaloids and a high density of glandular
trichomes. However, there remains a signicant challenge of how to achieve
introgression of resistance genes from wild relatives into cultivated potato
lines. Since high levels of glycoalkaloids can cause bitterness in potato tubers,
it has also been suggested that Bt genetic modication technology is com-
bined with conventional breeding. This may reduce the selection pressure for
resistance to Bt genes and allow the deployment of breeding lines with levels
of glycoalkaloids in the foliage that do not affect the palatability of potato
tubers (Cooper et al., 2004).
Probably the best-known example of implementing an integrated
approach to biological control on a large scale concerns Cuba. A detailed
examination of the Cuban agricultural crisis including the development of
the national IPM system has been written by Nicholls et al. (2002). In the early
1990s, a sudden collapse of trade with the former Soviet countries (which
were supplying Cuba with chemical pesticides, fertilizers and petroleum),
plus problems with pesticide resistance, resurgence and secondary pests,
forced the abandonment of chemical-based agriculture and a large-scale shift
to semi-organic production in order to prevent widespread starvation. To
give some scale to the Cuban agricultural crisis, in just 3 years from 1989,
petrol imports fell by 53%, fertilizer imports by 77% and pesticide imports by
63%. During the same period, the per capita food intake fell from 12.17 to
7.79 MJ/day (2908 to 1863 kcal/day); however, by 2000 this had been brought
back up to 10.82 MJ/day (2585 kcal/day) the recommended daily intake is
8.37 MJ (2000 kcal) for women and 10.46 MJ (2500 kcal) for men. Reduced
access to oil for road transport as a result of the US trade embargo resulted in
signicant amounts of food being grown in urban areas. Urban farmers
are trained in IPM and thus biologically based IPM is used both in cities and
in rural areas. The new agricultural production system that was developed is
characterized by low inputs of chemical pesticides, the use of resistant variet-
ies, growing crops that are best suited to local environmental conditions, use
of crop rotations and mixed cropping, and integrated crop and livestock
systems. Habitat manipulations are put in place to make the environment
less favourable to pest populations and more favourable to natural enemies.
Natural enemies, including microbial biopesticides, are used very widely.
These are produced locally using a network of state-run mass-rearing facili-
ties. There are around 280 biocontrol agent production centres, most of which
provide parasitoids, predators and microbial agents at low cost to local farm-
ers. In addition there are one industrial and 29 semi-industrial scale factories
providing commercial quality products for use on export crops. Biological
control is based on inundative applications of local strains of biocontrol
agents, including the release of 10,000 million Trichogramma parasitoids per
year. Production of microbial agents including Bt, entomopathogenic nem-
atodes and ve different genera of entomopathogenic fungi amounts to
about 2000 t/year applied to 600,000 ha. In general, the Cubans use low-dose
applications of microbial biopesticides, which by itself gives only partial pest
control but is considered to be cost effective and efcacious when combined
with other IPM components. Bt is sprayed against lepidopteran pests, such
as diamondback moth, cassava hornworm and tobacco budworm. Beauveria
bassiana is used against banana root borer, sweet potato weevil, sugarcane
borer and rice weevil. Metarhizium anisopliae is targeted against banana root
borer, diamondback moth and wax moth, while Lecanicillium species are
sprayed against whiteies and aphids. The IPM system is carefully matched
to the particular characteristics of each type of crop. Thus IPM in sugarcane
is based around use of resistant varieties and releases of predators and para-
sitoids, whereas banana IPM makes high use of cultural pest control and
microbial biopesticides. While it has been successful in preventing nation-
wide starvation, the Cuban agricultural system clearly does not provide the
range and abundance of food that consumers are used to in industrialized
countries, and the high levels of farm labour that are required are probably
untenable in modern market-driven economies. However, it must not be dis-
missed out of hand. The key elements of the Cuban system biocontrol with
local strains of natural enemies, the use of resistant plant varieties, careful
attention paid to crop nutrition and rotation, plus state support including
training for growers is a prime example of sustainable IPM that is not
reliant on high inputs of fossil-fuel-based pesticides and fertilizers.
As we have alluded to earlier in this book, there are complex interactions
between insects, plants and phytochemicals. For example, some groups of
herbivorous insects have evolved the ability to utilize phytochemicals for
their own benet. Some species of Lepidoptera, Coleoptera and Orthoptera
sequester toxic pyrrolizidine alkaloids (PAs) from their host plant. Enzymes
within the insect haemocoel oxidize the alkaloid to a non-toxic state. PA
sequestered during the larval stage remains within the insect after
metamorph osis into the adult stage and is even passed on to eggs. The
sequestered compound acts as a deterrent to invertebrate and vertebrate
predators; when ingested, it is reduced in the gut and absorbed in its toxic
state (Reddy and Guerrero, 2004). Some insect species also exploit phyto-
chemicals to ensure that eggs are laid on suitable host plants. Volatile phyto-
chemicals acquired when an adult contacts a host plant can trigger the
108 Chapter 3
production of sex pheromone to attract mates (e.g. in Helicoverpa spp., cotton
boll weevil, Anthomonus grandis, and African palm weevil, Rynchophorus
phoenicus) (Raina et al., 1992). Some insect species even use phytochemicals as
sex pheromones or pheromone precursors (Nishida, 2002). In other cases,
there is a synergistic interaction between a pheromone emitted by an insect
herbivore and the volatile compounds produced by its host plant.
This knowledge can be exploited for improved, integrated pest control.
For example, chemical baits used against African palm weevil are made of a
mixture of host plant esters and insect sex pheromone (Reddy and Guerrero,
2004). The complex interactions between plants, herbivores, natural enemies
and semiochemicals are starting to be exploited in the so-called pushpull
strategy (Cook et al., 2007; Khan et al., 2008) which uses behavioural modica-
tion to make a crop unattractive to pests (the push) while simultaneously
luring it away from the eld to other, more attractive plants that are grown as
traps/baits (the pull). Once the pests are on the trap crop they can be
removed. The methods used for the push part of the strategy are based on
making the crop plants repellent or masking their apparency to pests. They
can include use of non-host-plant volatiles, anti-aggregation pheromones,
alarm pheromones, feeding and ovipositional deterring chemicals, and dis-
torting the visual ability of pests to locate host plants using intercropping or
undersowing with non-host plants. The trap crop can be treated with a range
of semiochemicals such as host plant volatiles, pheromones, ovipositional
and feeding stimulants, etc. Each individual component may have only a
small effect on pest behaviour, but the overall aim is for the combined effect to
be as efcacious as using a broad-spectrum chemical pesticide. The strategy is
appealing from an IPM perspective, since it minimizes the use of synthetic
chemical pesticides and conserves natural enemies. The pushpull approach
is currently being used by African farmers to control stem-boring caterpillars
in maize and sorghum. Stands of sorghum or maize are intercropped with
molasses grass, which produces volatile compounds that repel ovipositing
adults and also increases the presence of insect parasitoids. Plantings of trap
crops consist of Napier grass or Sudan grass. Napier grass appears to be par-
ticularly suitable as not only is it attractive to ovipositing females, when its
tissues are penetrated by boring larvae it also secretes a gum that coats the
larvae and kills them. To date, however, there is little evidence that the push
pull strategy is being used consistently in commercial crops elsewhere. This
may be because the system requires a high level of detailed knowledge in
order to develop it, can be disrupted by changing the crop cultivar grown, or
because the high level of species specicity is a cost-limiting factor.
Regulating Biopesticides
Many governments have regulations in place for biopesticides. Only author-
ized biopesticide products can be used legally for crop protection. Biopesti-
cide companies have to apply for state authorization of a product; they are
then required to submit detailed information in the form of a dossier, which
is assessed by the government-appointed regulatory authority. The data
requirements used now by most OECD countries for microbial biopesticides,
pheromones and other semiochemicals are summarized in Tables 3.3 and 3.4.
Usually these data requirements have been modied from those used for the
registration of conventional synthetic chemical pesticides. Until about the
mid-2000s, government regulators particularly in Europe were unfamiliar
Information, test or study R or CR EU USA Canada Japan Australia
Point 1: Identity of the MPCA
Applicant R

Producer R

Scientic name R

Composition of technical grade
of MPCA/active substance
Concentration of microorganism R

Composition of microbial material
used for manufacture of end use
products. Identity and maximum
content of microbial impurities
R

Quality criteria for the production
and storage of the MPCA
R

Quality control data R

Theoretical discussion regarding
impurities. Physical and chemical
properties if produced as
manufacturing product.
International regulatory status.
Comprehensive data summary.
Sample of MPCA, analytical
standard of metabolite
R

Patent status R

Point 2: Biological properties
of the MPCA
Origin, isolation, maintenance
and history of the isolate
R

Natural occurrence of
microorganism
R

Description of target organisms R

Available information on host specicity R

Life cycle of microorganism R

Information on closely related
species. Physiological properties.
Description of plasmids. Genetic
stability. Resistance to antibiotics
R

Point 3: Information on the MPCA
(function, mode of action, handling)
Function R

Fields of use R

Continued
Table 3.3. Types of registration information required for microbial pest control agents (MPCAs)
in OECD countries. (From OECD, 2003.)
110 Chapter 3
Details of existing and
intended uses
R

Details of harmful organisms against
which protection is afforded
R

Effects achieved R

Mode of action in terms of
biochemical and physiological
mechanism and biochemical
pathways
R

Details of active metabolites and
degradation products
R

Information on formation of active
metabolites and degradation
products
R

Information on possible resistance
developing
R

Material safety data sheet for
microbial active substance
R

Detailed instructions for safe disposal R

Decontamination of water
procedures in case of an accident
R

Other/special studies CR

Crops or products to be protected or
treated
R

Measures to render microorganism
harmless, in case of an accident
R

Point 4: Analytical methods
Methods to preserve and maintain
master seed stock
R

Production process for technical
grade of MPCA
R

Quality control and post-registration
monitoring methods
R

Storage stability test, data and
determination of shelf-life
R

Post-registration monitoring methods
to determine and quantify residues
and metabolites on food, feed,
animal tissue, soil, water and air
CR

Point 5: Toxicological and exposure
data and information on the MPCA
Summary of potential of hazards
to humans
R

Occupational health surveillance
report on workers during production
and testing of MPCA
R

Acute oral infectivity and toxicity R

Continued
Acute intratracheal/inhalation
infectivity and toxicity
R

Acute intravenous/intraperitoneal
infectivity
R

Cell culture study for viruses and viroids
or specic bacteria or protozoa
R

Genotoxic potential, especially for
fungi and actinomycetes
R

Toxicity studies on metabolites CR

Published reports on adverse effects.
Short-term toxicity. First aid
measures
R


Summary of mammalian toxicity
and overall evaluation
R

Point 6: Metabolism and residue
studies on the MPCA
Summary of residue behaviour and
rationale for waiver of residue data
R

Point 7: Fate and behaviour studies
on the MPCA in the environment
Information on origin, properties,
survival and residual metabolites
to assess fate in environment
EU R
USA CR
Japan CR
Canada CR


Point 8: Ecotoxicological studies
on the MPCA
Effects on non-targets R

Birds R

Fish R

Aquatic invertebrates R

Effects on algal growth R EU only

Effects on aquatic or terrestrial plants CR

Bees R

Non-target terrestrial arthropods R

Other terrestrial invertebrates CR

In EU effects on earthworms required R

In EU effects on non-target soil
microorganisms required
R


Point 9: Summary information
for the MPCA
Summary and evaluation of
environmental impact and assess risk
R

R, the data submission is in principle necessary; CR, the data submission is necessary when the microbial
pesticide meets a certain criterion.
112 Chapter 3
Information, test or study R or CR
Mode of action
Function, handling and label information
Information on function, directions of use, formulations, eld of use and
use sites, pests controlled, application rate, method and timing,
preharvest interval, precautionary and emergency measures, procedures
to clean equipment and spills, disposal of unused product
R
Labelling requirements regarding hazard classication and risk identication R
Chemistry
Technical grade of active ingredient (TGAI)
Composition R
Identity by spectral conrmation R
Description of starting materials, production process and potential impurities R
Analytical data and methodology R
Analytical methodology and data for impurities of toxicological concern CR
Analytical methods for residues CR
Colour, odour, physical state, relative density or specic gravity, stability R
For each known active ingredient (AI) component of the TGAI
Description of starting materials and manufacturing process R
Physical properties: melting point, boiling point, solubility in water
and other solvents, colour, odour
R
Ultraviolet/visible absorption R
Vapour pressure R
Volatility (Henrys law constant) R
Dissociation constants R
Octanol/water partition coefcient R
Submission of analytical standards (samples) R
End-use product (EP)
Formulation process and starting materials R
Composition R
Analytical methodology (AI) for post-registration monitoring R
Physical properties: colour, odour, physical state, specic gravity, pH,
formulation type, container type, explosivity, viscosity,
technical characteristics
R
Corrosion characteristics and stability of formulation during storage R
Data for assessment of health risk
Summary R
Toxicology
Acute oral toxicity: TGAI and EP R
Acute dermal toxicity: TGAI and EP R
Primary eye irritation: TGAI and EP R
Primary dermal irritation: TGAI and EP R
Dermal sensitization/reporting of hypersensitivity incidents: TGAI and EP R
Mutagenicity (gene mutation in microbes and mammalian cell systems
and chromosome aberration): TGAI
R
Medical data, available information: TGAI and EP R
Short-term study by appropriate route: TGAI CR/R
Teratogenicity/developmental toxicity/one species: TGAI CR/R
Continued
Table 3.4. Guidance for registration requirements for pheromones and other semiochemicals
used for arthropod pest control. (From OECD, 2001.)
Information, test or study R or CR
Long-term toxicity (chronic) and carcinogenicity CR
Multigeneration reproduction, teratogenicity (in second species),
animal metabolism, neurotoxicity, immunotoxicity
CR
Occupational or bystander exposure (using the EP)
Use description/scenario (application and post-application) R
Passive dosimetry (mixer/loader/applicator and/or post-application)
or biological monitoring
CR
Dislodgeable residues CR
Ambient air samples CR
Biological monitoring CR
Dermal absorption CR
Clothing penetration, epidemiology, package integrity CR
Metabolism studies and residue analysis of food, feed and tobacco
Metabolism/toxicokinetics study on animals and plants which
may be directly exposed to semiochemicals through use
CR
Analytical residue methodology for food crops CR
Crop residue data CR
Meat, milk, poultry and egg residue data CR
Freezer storage stability, produce quality CR
Data for assessment of environmental risk (using EP unless otherwise specied)
Summary R
Effects on non-target organisms
Birds dietary toxicity CR
Bees: prefer EP CR/R
Other terrestrial arthropods (crop-specic benecial, related species): prefer EP CR/R
Freshwater invertebrate acute toxicity: prefer EP CR/R
Freshwater sh acute toxicity: prefer EP CR/R
Algae: prefer EP R
Earthworms R
Soil microorganisms R
Long-term laboratory or eld testing on: aquatic animals, terrestrial animals,
non-target plants, non-target insects
CR
Environmental fate
Assessment based on available information R
Experimental studies in compartments of possible concern: hydrolysis
(TGAI), phototransformation on soil and/or in water (TGAI), stability in air, per-
sistence of volatiles (TGAI), biotransformation (aerobic soil and/or aerobic aquatic,
TGAI), adsorptiondesorption (TGAI), leaching of each AIC from
dispenser by water (EP), volatilization from dispenser, release rate (EP)
CR
Efcacy (for the EP)
Efcacy summary R
Description of pest problem and AIs mode of action R
Efcacy trials of product, used as directed on the label, including reporting of adverse
effects to site (e.g. phytotoxicity)
R
Sustainability considerations (compatibility with integrated pest management; contri-
bution to risk reduction)
R
R, required data, surrogate data or a rationale to waive data; CR, required only under certain conditions;
CR/R, the information is required only under certain conditions in Canada, the USA and Switzerland but is
required in the EU, with the understanding that there is an appropriate basis for waiver rationale.
114 Chapter 3
with biologically based pest management and were therefore slow to appre-
ciate the need to adapt the regulations to make them appropriate for the
features and characteristics of biopesticides. The questions, information and
procedures required to effectively evaluate the environmental fate and
behaviour of a living, microbial biopesticide are very different from those
for a chemical pesticide, for example. Often the data required by regulators
during this period were excessive and incurred large nancial costs on the
applicant that were out of proportion to the prot that was set to be made
from biopesticide sales. Evaluating biopesticides using an inappropriate set
of regulations has had the unintended consequence of deterring companies
from commercializing biopesticide products. However, when the regulations
are tailored appropriately, it is possible to achieve effective governance that
does not impede the commercial development of products. Thus regulators
have made a consistent effort in the last 5 years to adapt the data require-
ments to make them suitable for biopesticides. Usually the amount of data
required now is much less than that for a conventional synthetic pesticide.
Of course, the drivers behind regulation vary according to the circumstances
of each country. As we have seen in the case of Cuba, the collapse of the
countrys conventional, industrial agriculture forced the authorities to be
proactive in getting biopesticides into the hands of growers as part of the
drive to develop an alternative agricultural system. Countries in the Global
North clearly do not yet face the perilous and acute situation suffered by the
Cubans. But policies put in place in the EU, North America and elsewhere to
restrict the use of conventional pesticides, combined with the realization that
agricultural production has to increase signicantly in the next 20 years and
at the same time become more sustainable, means that governments are hav-
ing to think long and hard about biopesticides and other alternative agents
as part of a new effort with IPM.
There are a number of good reasons why the sale and use of biopesticides
need to be regulated. First, if a product is being sold with the express inten-
tion of controlling a pest, then it goes without saying that its effectiveness
needs to be demonstrated to the people who will buy it. The EU requires
that efcacy be proven as a condition for ofcial registration, whereas other
countries such as the USA tend to let the market decide whether a product is
effective or not. Biopesticides are valuable components of IPM but they often
have lower levels of efcacy than conventional pesticides, and hence regula-
tors are now tending to alter their data requirements so that a biopesticide
does not have to show 100% efcacy in trials in order to be granted approval.
Biopesticides respond to environmental conditions signicantly more than
conventional pesticides and thus the level of pest control is likely to vary at
different times. Systems of using biopesticides need to be developed that
allow for some performance variation but which still contribute in a mean-
ingful way to pest control. This also needs to be reected in the advice and
information given by biopesticide companies to their customers so that
expectations are reasonably managed. Obviously, if a biopesticide product is
not effective then farmers and growers are unlikely to use it, but customer
condence can also be damaged if a product is over-sold.
Second, regulatory authorities need to determine whether a biopesticide has
potential to cause negative effects on humans and the environment. They then
need to decide whether any risk is associated with the biopesticide and, if so,
is it acceptable? This brings us on to the third, related reason for regulation: the
need to be able to characterize biopesticide products. Regulators have to ensure
that biopesticide companies are selling products that contain the ingredients
that are stated on the product label and are free from harmful contaminants.
So what potential hazards could be presented by biopesticides? To begin
with, if the biopesticide had a toxic mode of action, it could offer a toxicity
hazard to people (farm workers, production plant operatives or the general
public) as well as to animals, plants and other non-target organisms. For
microbial biopesticides, there are three additional potential hazards (Cook
et al., 1996): (i) ecological displacement of non-target microorganisms; (ii)
causing an infection in non-target organisms; and (iii) causing an allergic
reaction in humans or other animals. Points (i) and (ii) result from the ability
of a microbial natural enemy to grow and reproduce in its environment
and are features that are important for the effectiveness of many microbial
biopesticides against their target pest (Cook et al., 1996).
At least as far as the OECD countries are concerned (and also probably for
most other countries), the regulations are set up so that biopesticides are only
being approved for use if they pose minimal or zero risk. For example, the basic
requirements of most OECD countries for microbial biopesticides are that:
the microorganism and its metabolites pose no concerns of pathogenicity or
toxicity to mammals and other non-target organisms which will likely be
exposed to the microbial product; the microorganism does not produce a
known genotoxin; all additives in the microbial manufacturing product and in
end-use formulations are of low toxicity and suggest little potential for human
health or environmental hazard.
(OECD, 2003)
Thus, of the 218 biopesticide active substances approved by the US EPA, 206
are classed as having no expected health risk to humans. Of the remainder:
nine are classed as having potential to cause eye and/or skin irritation; one
is classed as having dermal and oral toxicity at high concentrations; one is
slightly toxic; and one is classed as having a very small potential risk to
human health (United States Environmental Protection Agency, 2010). These
evaluations are based on experimental investigations using toxicological and
eco-toxicological tests, host range testing, as well as basic information about
the biopesticide agent, such as its mode of action, which are combined into
an overall risk assessment.
The risk (i.e. probability) of a negative effect happening is a combination
of the hazard and the exposure. With conventional pesticides, products that
are toxic to humans and other non-target animals are still authorized for use
if it can be shown that the risk can be managed effectively by controlling
the level of exposure, for example through the application method, by
using protective equipment, by formulating and packaging the product and
so forth. Because most biopesticides are deemed by regulators to present low
116 Chapter 3
or minimal hazard, this has the considerable advantage that less stringent
precautions are required over exposure. For example, because many biopes-
ticides leave no chemical residue, they are granted a short harvest interval
(the time allowed between when the product is applied and the crop is
harvested). This means that pests can continue to be managed right up until
the last moment. Similarly, because biopesticides normally have zero
mammalian toxicity, farm workers and other operatives can handle the crop
a very short time after it has been treated. This can be a vital consideration for
crops grown under protection, which tend to require a high level of main-
tenance and handling. With conventional pesticides, workers have to be
excluded from the crop for many hours or even days after spraying. The
main hazard from authorized biopesticides is the development of an allergy
in people working in microbial biopesticide production plants who could be
regularly exposed to high amounts of microbial spores or farm workers who
handle the product in concentrated form (Cook et al., 1996). Only a very small
fraction of microbial species produce spores that cause an allergic reaction
(Latge and Paris, 1991) but nevertheless it makes sense, as part of good
operating practice, to prevent exposure during production or biopesticide
application by using remote-controlled machinery and by wearing personal
protective equipment during spray application, although often only basic
protective equipment is required.
This is not to say that all agents that could be used as a biopesticide
present no hazard. Just because something is natural does not mean that it
is safe. It is important, therefore, that biopesticides continue to be evaluated
for their human and environmental safety. Let us consider microbial natural
enemies as an example. We have seen earlier in this book that some plant
pathogens, such as Aspergillus and Claviceps species, produce metabolites
that are toxic to people and animals. Obviously, these species would never be
considered as bioherbicides according to OECD guidelines as there is a risk
of the toxins entering the food chain from fungus-infected weed material
accidentally harvested with the crop. Likewise, there are members of the
bacterial genus Rickettsiella that are pathogens of arthropods (Larsson, 1978).
Although they are not related antigenically to rickettsial pathogens of verte-
brates, some can cause infection in the lungs of mammals if inhaled (Tanada
and Kaya, 1993). Consequently, these bacteria would not be considered suit-
able for use as bioinsecticides as they pose a danger to spray operatives and
other farm workers. There is an important role here for using basic scientic
knowledge and common sense to select candidate agents for biopesticide
development that are known to offer minimal hazard. From our knowledge
of the biopesticides industry, there is a clear drive to identify and commer-
cialize agents that are known to have minimal hazard.
Safety considerations for microbial biopesticides
We do not have space in this book to provide a detailed account of the
potential health and safety issues for all microorganisms used as biopesticides.
We have made reference in previous sections to the safety of some agents,
such as Bt and entomopathogenic viruses. For more information the reader is
referred to Burges (1981) and the EU REBECA (Regulation of Environmental
Biological Control Agents) website (www.rebeca-net.de). Here we will focus
on a small number of illustrative examples.
We have just seen that the biopesticides that are approved for use are
considered to present no hazard to human health. It is important at this junc-
ture to put concerns about the safety of microorganisms used as biopesticides
into context. Humans coexist with thousands of different microbial species
as part of normal life. These include microbial natural enemies of arthropods,
plant pathogens and weeds. The vast majority of these bacteria, fungi, oomy-
cetes, viruses and protozoans are harmless to us. This is not to say that all
candidate microbial agents are safe. Regulators need hard evidence on the
risks of microbial biopesticides, but the problem for many biopesticide com-
panies is that the costs of generating the required data are very high com-
pared with the market size. There is relevant information on microorganism
safety from the scientic literature that is in the public domain and could be
used to support a data registration package, but it is highly specialized and
can be difcult for the companies which tend to be small enterprises to
track down and synthesize. For this reason, researchers at academic institu-
tions can play a very important role by writing independent systematic
literature reviews on microorganism safety and putting them into the public
domain so that regulators, commercial operations and others in the policy
network can use them. Historical experience with microbial biopesticides is
also important. For example, commercial products of Bt have been authorized
in the USA since the early 1960s, and a large number of studies since then
have shown them to have a rst-rate safety record (Siegel, 2001). This should
give condence to regulators when asked to evaluate new Bt products.
The main concern about the risks of microbial biopesticides to human
health is whether the microorganism produces compounds that are toxic.
Fungi, for example, produce a wide range of bioactive metabolites, some of
which are toxic, although others are used as pharmaceutical medicines.
Metabolites that are toxic have been characterized for a number of fungi used
as microbial biopesticides, and the safety concern is that these could cause
harm to people if they enter the food chain. Strasser et al. (2000) reviewed
the toxic metabolites produced by species of the entomopathogenic fungi
Metarhizium, Tolypocladium and Beauveria. Some of the compounds are impor-
tant for the pathogenicity of the fungi to insects, although the function of
others remains to be elucidated. The levels of these metabolites produced in
vivo are usually much lower than those produced in laboratory culture, and
studies have shown that negligible amounts of metabolite are released into
the environment from formulated biopesticide product or from fungus-killed
insects. The authors concluded that the use of fungal bioinsecticides would
not result in harmful toxin levels in the environment and posed no serious
risk to humans. Similarly, Zimmerman reviewed the safety of B. bassiana and
B. brongniartii (Zimmerman, 2007a) and M. anisopliae (Zimmerman, 2007b)
including comprehensive analysis of biological properties (including toxin
118 Chapter 3
production), analytical methods for residues, fate and behaviour in the envir-
onment, effects on non-target organisms, vertebrates, mammals and human
health. On the basis of the available published information he concluded that
these fungi should be considered safe to use as biopesticides. The US EPA
concurs, and classify the M. anisopliae and B. bassiana strains registered as
biopesticides in the USA as presenting no toxicity risk to human health.
Indeed, there could even be benets for human health: Beauveria, in the form
of its teleomorph (sexually reproducing phase) Cordyceps sinensis, collected
from naturally infected ghost moth caterpillars, has been used as a tradi-
tional medicine in China and Tibet for hundreds of years (Muller-Kogler,
1965, cited in Zimmerman, 2007a). The fungus is highly valuable and is a
signicant source of export income to the region.
The other concern for microbial biopesticides is their risk to wildlife.
Effective methodologies need to be in place to determine the impact on non-
target organisms. Such methodologies should be informed by ecological
theory, including insights made in recent years in community ecology and
invasion biology (Pearson and Callaway, 2003, 2005). Impacts on non-target
organisms can be direct or indirect (e.g. competition between introduced and
indigenous natural enemies). A microbial biopesticide with a high level of
selectivity means that unwanted direct effects on non-target organisms are
likely to be rare. However, even host-specic biological control agents can
have impacts on non-target organisms through indirect effects (Pearson and
Callaway, 2005).
Augmentative applications of microbial biopesticides use natural enemies
that are endemic, i.e. that already occur naturally in the country or region
of use. They are not aimed at permanent establishment and the population of
the released agent is expected to decline to background levels post-application.
Therefore, any negative effects on non-target species should be temporary.
Cook et al. (1996) state that, there is nothing inherent in the strategy itself
(inoculative, augmentative, or inundative) that raises a safety issue. Practical
experience with agents such as entomopathogenic fungi used for augmen-
tation biological control backs this up, with no detectable detrimental envi-
ronmental impact (Goettel et al., 2001; Vestergaard et al., 2003). Such
experience has an important bearing on the risk evaluation of new products,
but as outlined above this is not to say that evaluation of new products
is not required. To start with, augmentative applications alter interaction in
space and time between the microbial agent, its hosts and the environment
( Jackson, 2003). If microbial biopesticides become used more widely, then
the amount of environmental perturbation might increase. Biopesticide
manufacturers are under commercial pressures to develop products with a
relatively wide host range and this increases the risk of a negative environ-
mental effect. Potentially, there could be unintended effects, for example,
on the diversity and function of other microbial natural enemies. Host
range evaluation is important for microbial biopesticides, although proce-
dures here have been criticized for concentrating on the physiological host
range of agents (i.e. the potential host range as determined through laboratory
bioassays) at the expense of studies of the ecological host range (i.e. the
actual host range in the agro-ecosystem, which tends to be much narrower)
( Jaronski et al., 2003).
Since classical control is based on the deliberate introduction of a non-
indigenous natural enemy with the aim of permanent establishment, deter-
mination of host specicity is critical to ensure that agents released do not
have negative effects on non-target organisms. There are now well-established
systems for risk assessment and host range testing (Andersen et al., 2005) that
tie in to the FAO code of conduct on the import and release of biological
control agents (FAO, 1996). But it has been argued that there is still a lack of
long-term, quantitative and objective monitoring of classical control pro-
grammes (Thomas and Reid, 2007). This may be because few apparent prob-
lems have been encountered with classical control (van Lenteren et al., 2006;
Hajek and Delalibera, 2010). However, where pre-release risk evaluation pro-
cedures are inadequate or ignored, environmental damage can occur. It
should not be forgotten that early introductions of alien generalist predators,
such as cane toads in Australia and coccinellids in Hawaii, were done with-
out proper consideration of the risks and with a poor understanding of eco-
logical principles, resulting in unacceptable environmental consequences
(Thomas and Willis, 1998; Barratt et al., 2010). And a prominent recent exam-
ple in Western Europe concerns the harlequin ladybird, Harmonia axyridis.
This species is native to Asia and has been used as a control agent of aphids
in glasshouses in Europe and North America. It has been intentionally intro-
duced in nine European countries since 1982 (Brown et al., 2008), although a
retrospective analysis identied it as having high environmental risk (van
Lenteren et al., 2003) and thus it should not have been released (van Lenteren
et al., 2008). It is now established in 13 European countries from Denmark to
southern France and is predicted to spread further. It is able to outcompete
native ladybirds, will predate on some benecial insects, and there is evi-
dence that it has a signicant negative impact on other native arthropod
species. This episode has undoubtedly cast a shadow over classical biologi-
cal control in Europe. This is unfortunate, because it remains the only method
for permanent ecological management of many alien invasive species. It has
been proposed that legislation is enacted within the EU in line with the
Convention on Biological Diversity to enable releases of classical control
agents based on EPPO (European and Mediterranean Plant Protection
Organization) standards (Sheppard et al., 2006). In the future there is likely to
be an even greater drive to reconcile biocontrol efcacy with biosafety,
with the focus being on selecting biological control agents that are effective
at controlling the target pest but which are highly selective and present no
risk to non-target species (Barratt et al., 2010).
There is a related issue that crosses the divide between classical and
augmentative biocontrol, namely whether an entity of a microbial natural
enemy intended for use in augmentation biocontrol is endemic or not. For
example, many fungal species that have been classied taxonomically on
the basis of morphological criteria are said to have worldwide distribu-
tions. However, studies using molecular tools indicate that in reality
these individual morphological species may consist of an assemblage of
120 Chapter 3
genetically distinct cryptic or hidden species, each with its own charac-
teristics and with differing geographical distributions (Desprez-Loustau
et al., 2007). If this were to apply to a fungal species being considered as a
microbial biopesticide, there could be a chance of unknowingly introdu-
cing a non-native, cryptic species to a new country. There is a clear role
here for research on the diversity and biogeography of microbial natural
enemies to underpin environmental risk evaluation of microbial biopesti-
cides. For example, a molecular phylogenetic study of the entomopatho-
genic fungus B. bassiana showed that a strain of the fungus isolated in the
USA, and now used in a commercial biopesticide sold in the USA and
Europe, is a member of a cryptic species that is indigenous to North
America and Europe (Rehner and Buckley, 2005). Such basic studies on
microbial phylogeny have an important role to play in the future regulation
of microbial biopesticides.
Safety considerations for botanicals and semiochemicals
If a botanical pesticide comprises just a single active ingredient then its
registration data requirements are relatively straightforward and it can be
assessed in much the same way as a conventional chemical pesticide. Reduced
data requirements are likely if there is well-established evidence, e.g. from
the scientic literature, European pharmacopoeia, etc., that the compound is
non-toxic to mammals and other non-targets and presents minimal risk.
Problems are likely to arise, however, if the botanical consists of a complex
plant extract that is difcult to characterize and is likely to vary between
production batches.
Semiochemicals are naturally occurring non-toxic molecular messengers
that work by chemically binding to receptor molecules that are located on the
cell membranes of the receiving organism. They are target specic: if an
organism does not possess the receptors for a particular semiochemical (e.g.
in the case of a human exposed to insect sex pheromones) then the semiochem-
ical will not bind to its cells. Therefore, there are sound biological reasons for
government regulators approaching semiochemicals intended for use as
biopesticides from the starting position that they are unlikely to be hazard-
ous to non-target organisms. The OECD regards semiochemicals used for
arthropod control as presenting minimal hazard to people or the environ-
ment, and it considers SCLPs, which form the majority of semiochemical-
based biopesticides, as particularly safe (OECD, 2001). This assessment was
based on the fact that they are non-toxic to humans, the rates at which they
are applied in the eld are very low and are typically similar to levels that
occur naturally, and that they dissipate and degrade rapidly in the environ-
ment. Moreover, many are applied in passive dispensers that prevent direct
contact between the semiochemical concentrate and humans or wildlife.
Most organisms are able to degrade SCLPs by normal metabolic processes,
and the OECD considers that they should present no problems with their
normal physiology if contamination does occur (OECD, 2001). The OECD
recommends that the high safety factors:
justify substantial reductions in health and environmental data requirements,
especially for SCLPs, a well-dened chemical group for which considerable data
are available. Also for other classes of semiochemicals, it may be justied to
waive certain required studies if the registrant can provide an adequate rationale.
(OECD, 2001)
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4
The Economics of Making the
Switch in Technologies
So far in this book we have seen that IPM, to date, is used to varying degrees
of intensity in nearly all annual protected and unprotected crop systems.
However, this is far from a universal picture since not all growers have
adopted this approach. Furthermore, for the majority of production systems,
particularly in broad-acre agriculture, adoption and impact (as measured by
reductions in use of conventional chemical pesticides) have been minimal.
This lack of commercial adoption appears to run counter to various asser-
tions by researchers of the appropriateness and even the superiority of these
new techniques over the incumbent technology.
In the wider technology adoption context, this apparently irrational
behaviour on the part of farmers has been the subject of a number of contri-
butions within the economics literature.
Typically, the producers decision of whether or not to adopt a novel
technology can be conceived as a simple comparison of the relative net
benets derived from the novel and the incumbent technologies. The
bene ts are usually dened as utility, which for the commercial producer
will relate primarily to prots. However, at least for the novel technology,
farmers will have imperfect information on the costs of implementing
and the benets gained from the novel technology. Therefore, the farmer
must make a judgement to form his expectation of the net benets of
using the new technology. Economists tend then to formalize the single
technology adoption/replacement decision as one where adoption occurs
if E(U
n
, z) > E(U
o
, z), where n refers to the novel and o to the old technology
and z is a range of farm characteristics and prices. This framework works
well when we consider the adoption of single independent innovations, a
good example of which could be the adoption of computerized record-
keeping. However, there are a number of characteristics of the IPM
adoption problem that are likely to considerably complicate our simple
technology adoption decision criteria.
132 Chapter 4
Several possible reasons are cited. These include:
1. Differential cost structures of pesticide and IPM technologies. The signicant
research database and the widespread practical use of chemical pesticide
technology ensure that what xed costs are required are both mitigated by
widely available information and diluted over many users. The xed costs
faced by users of this technology are a small fraction of the total costs of pest
control. It has been argued by many authors (e.g. Cowen, 1991; Cowen and
Gunby, 1996) that this situation is both an artefact of the technology (farmers
need only limited information to ensure that control is effective, if not eco-
nomical) and a product of past dynamic gains from adoption. In contrast,
existing biocontrol and other alternative pest management technologies are
very information and skill dependent. This factor ensures that potential
adopters of this technology face signicantly large xed costs of adoption.
However, these xed costs are likely to diminish as these technologies gain
more widespread use and, as such, dynamic gains are likely to be increasing
albeit from a small base.
2. Differential risk of technologies and risk preferences of producers. The much
more limited body of research data and practical experience with biocontrol
and IPM adds to the degree of uncertainty surrounding the efcacy and eco-
nomic viability of the techniques (e.g. Cowen and Gunby, 1996; Abadi Ghabim
and Pannell, 1999; Pannell, 2003) and acts as a barrier to adoption. In addition,
the uncertain effects of scaling in alternative technologies also hinder the
adoption process (Grifths et al., 2008a). Furthermore, farmers heteroge-
neous, and potentially averse, risk preferences are likely to result in a less than
uniform, and probably suboptimal, adoption pattern of uncertain technolo-
gies (e.g. Antle, 1987; Yaron et al., 1992; Cowen and Gunby, 1996). Potential risk
aversion adds to the problem if expectations of the efcacy of alternative strat-
egies based on biocontrol are skewed towards the downside (Antle, 1987).
3. Jointness caused by allocatable xed factors (Shumway et al., 1984) (the
sprayer machine). Jointness in the control of a range of pests, plant pathogens
and weeds using conventional chemical control techniques, caused by use of
common shared xed assets, presents a further potential barrier to the adop-
tion of alternative biocontrol techniques. The broader the range of biocontrol
approaches integrated into alternative strategies the greater the potential
gains to adopters. As such, a more integrated approach to biocontrol research,
development and extension is likely to be important.
4. Portfolio economies in IPM adoption. While some substitution possibilities
may exist between component techniques with IPM, there will probably exist
some strong yield-enhancing or cost-reducing complementary relationships.
These are often highlighted by ecologists working with biocontrol evalua-
tion. Practical examples include ying biocontrol organisms that predate or
act in the upper crop canopy and those ground-moving organisms that act
lower down the plant being spatially additive. Likewise, biocontrol organ-
isms that are active at different times of the cropped season can be consid-
ered as temporally additive. Therefore, IPM adaptations to systems and
land-use practices which promote these different biocontrol agents will be
functional complements. However, where the presence of one IPM technique
in a system results in improved performance in a second technique, where
complementary techniques are super-additive, then there will be economies
of adoption intensity, or portfolio economies. Grifths et al. (2008b) have
quantied some of these effects in the context of the rate of pest control
provided by control agent assemblage complexity. If these intra-species
effects scale up to the level of IPM component pest management technolo-
gies, then they will reinforce portfolio economies. Therefore, farmers must
consider the potential benets of adopting a specic IPM technique in the
light of their currently adopted portfolio of technologies since e
n
= f(t
n
,T),
where e
n
and t
n
are respectively the efcacy and intensity of adoption of the
nth technique and (T = t
1
, t
2
, . . . , t
n1
) is the intensities of the set of currently
used technologies or practices.
All of these factors will probably contribute towards an advantage of the
incumbent technology. As Cowen and Gunby (1996) point out, in the compe-
tition between technologies which perform similar roles, history matters
when one or both technologies possess increasing returns to scale in either
production or use. For the user, the farmer, scale economies could arise from
learning by doing, falling information costs of implementation and scale or
size economies relating to subsequent and sequential application cost. In
addition, external scale economies (and diseconomies) in the pest control
process itself, associated with possibly reduced pest pressure (and dimin-
ished population of benecial organisms) derived from the use of pesticides
on neighbouring farms, can complicate the issue. If so, the incumbent tech-
nology, in this case chemical pest control, will probably benet from positive
feedback as scale economies increase the returns to both current users and
new adopters. Even if the alternative, IPM, technologies also possess econo-
mies of scale, and really are superior to the incumbent, farmers will nd it
extremely costly to switch technologies in the medium term and potential
gains will remain unrealized. Subsequent technology choice will probably
then be path dependent and chemical pest control will remain locked in to
the system until such a time when the incumbent technology fails, as resis-
tance is encountered and new toxicity pathways are exhausted or society
deems that the use of particular chemical pesticides is unacceptable.
All of these issues probably compound to make the adoption decision
process cognitively complex. Furthermore, the issue of path dependency in
both the incumbent and novel technologies probably promotes inertia.
A number of researchers have attempted to model the decision to adopt
multiple, potentially interdependent, farming technologies. Examples in
agriculture include Feder (1982), who considers the adoption of two tech-
nologies under uncertainty and where one technology has scale economies,
and Dorfman (1996). These approaches consider the decisions of farmers
faced with the options to not adopt or to adopt technology i, technology j or
some combination of technologies i, j, . . . , S.
Dorfman models the portfolio adoption process by considering each
alternative adoption decision, for a two technology decision as either (0,0),
134 Chapter 4
(0,1), (1,0) or (1,1), a problem with four potential technology bundles or
portfolios. Dorfman then applies a multinomial logistic regression model to
explain adoption patterns of IPM and improved irrigation technologies in
US apple farms. Clearly, the number of technology bundles to consider
increases rapidly the more distinct technologies we consider. With three
technologies the number of unique bundles increases to seven, with four
technologies to 11, and so on. At this level of technology disaggregation,
econometric identication of key parameters is near impossible since model
likelihood functions are quite at. Moreover, since the farmer must develop
an expectation of the utility he could derive from each bundle, his cognitive
burden is considerable. The farmer may nd it quite easy to develop an
expectation for bundles such as (0,0,0) or (0,1,0). However, any bundle includ-
ing more than one technology will require the farmer to assess whether the
expected utility from (1,1,0), never mind (1,1,1), is greater than or less than
the sum of its parts. The potential for IPM portfolio economies to promote a
positive path dependency resulting in the sequential adoption of IPM
techniques could be strong if the technical incrementalism referred to in
Chapter 3 is signicant.
Feder considers the decision facing a farmer with the option to adopt
two interrelated technologies which differ in cost structure, one with con-
stant average and marginal cost (Feder considers high-yielding crop variet-
ies) and the other with a lump-sum start-up cost and therefore a declining
average cost (the example used is irrigation tube wells). The technologies
considered by Feder are interrelated in two ways. First, the adoption of both
technologies together produces higher average yields than achieved when
adopting only one of the technologies, a yield complementarity. Second, the
adoption of the declining cost technology affects the perceived risk of the
constant cost technology. In Feders example, perceived risk of adopting
higher-yielding crop varieties might be reduced by adopting irrigation tech-
nologies. It is then shown that an increase in the xed cost of adopting irriga-
tion, a smaller perceived risk complementary effect, a higher perceived risk
of using improved crop varieties and increasing farm size (if farmers are risk
averse as is often the case) can all reduce the adoption of higher-yield variet-
ies. These results remind us that we must consider a broader denition of
technological complementarity, than simple yield complementarity, in our
assessment of IPM approaches and that scientic evaluation work on the
interrelated risk effects of joint adoption could prove highly inuential in the
portfolio adoption decisions of farmers.
Faced with these types of adoption problems, it seems reasonable to
assume that farms will probably retreat into a tactic of trialling, and subse-
quently adopting or dropping, individual technologies in a sequential man-
ner. This approach may generate some benecial portfolio approaches;
however, it is likely that the choice of the rst technology will condition the
shape of the resulting technology portfolio. Equally, since we would expect
that the expected utility derived from any technology, or set of technologies,
would be conditional on farm characteristics, including geography, crop
combinations and farmer skill sets, it would be quite difcult to make
specic portfolio recommendations, although the science community could
help here by identifying key technology complements for general situations
or specic pest problems.
Pragmatic Promotion of Integrated Pest Management Adoption
Many authors who consider both the science and the economics of the IPM
adoption process recognize the importance of the public good aspect of
alternative forms of pest control. This may be the case where the adoption of
IPM reduces the potential external effects associated with pesticide use, such
as effects on non-target organisms and the contamination of watercourses,
whose costs are borne by society at large. Additionally, the adoption of IPM
on one farm may enhance the benets of IPM on neighbouring farms. The
presence of external effects can justify calls for government action to equalize
private incentives with the costs or benets to society. Cowen and Gunby
(1996) argue that path dependency suggests that farmers are not necessarily
irrational in choosing to continue to use an entrenched but suboptimal tech-
nology. However, society as a whole may be considered to be irrational if the
public policy provision required to change to a socially more optimal path is
not committed. Elsewhere in this book we consider the role of contracts in
the food supply chain in this regard (see Chapter 7). While private contrac-
tual arrangements have been shown to be effective in inducing a switch away
from pesticides to IPM in some production systems, this cannot be consid-
ered an option for systems which produce primarily for spot market sale.
Here, government action remains the primary hope for breaking pesticide
dependence. Agri-environmental policy (AEP) may then help to improve the
nancial return of IPM to farmers and close the technology gap opened up
by scale economies in the incumbent chemical control technology.
Other government action may also help the process of adoption. As
extensively discussed elsewhere in this book, the regulation of chemical pes-
ticides provides an interesting case. The action of the regulator (the PSD, now
CRD, as competent authority for Directive 91/414/EEC replaced by Regula-
tion 1007/2009 in the UK case) may have the effect of slowing up the supply
of newly approved compounds, by the application of stringent safety and
testing requirements and the removal of existing compounds considered
unsafe given new knowledge and standards. Much is written on these forces
elsewhere in this book. Either mechanism could provide the demand pull
that promotes an increased adoption of IPM technologies.
Thus, while there are many drivers acting to reduce the use of pesticides,
and there are many alternative pest management strategies in development,
adoption of these alternatives remains limited to date (particularly in the
arable sector).
Lohr and Park (2002) considered the mix, or number, of insect manage-
ment technologies adopted by organic farmers in the USA. Their data
showed that over 30% of their sample of 1027 farms used more than ve
distinct technologies within their IPM portfolio. Lohr and Park subsequently
136 Chapter 4
used a count data model to consider how the number of technologies
adopted, or the diversity of a farms IPM portfolio, was inuenced by vari-
ous farm- specic characteristics. On the whole, highly educated and more
experienced organic full-time farmers who operated on smaller farm areas
producing a high proportion of horticultural crops adopted a wider range in
insect pest-specic IPM technologies. IPM complexity, and by extension
IPM success, then appears to hinge on scouting, information and an ability
to understand complex systems. How IPM rolls out into more extensive
crop systems, where human capital must be spread thinly, is of great inter-
est. Public policy is likely to be important in the adoption of IPM in broad-
acre agriculture.
Agricultural and agri-environmental policy
AEP can, in principle, give rise to landscapes that can support a large num-
ber of arthropods such as pests and their enemies and can help to overcome
some of the problems of path dependence described by Cowen and Gunby
(1996). Indeed, the types of habitat manipulation available via the AEP
should, in principle, give rise to the provision of many natural predators of
value to cereal producers. Holland and Oakley (2007) even identify those
manipulations most likely to yield the preferred outcomes (i.e. hedgerows,
eld margin strips, beetle banks). They also note that within-eld activities
such as non-inversion tillage need to be considered given the growing imple-
mentation of this method in practice.
Currently, there are a number of strong drivers in the agricultural policy
domain to suggest that farmers will adopt a number of different strategies,
both consciously and unconsciously, towards pest management. In the UK
and the EU more generally agricultural policy has undergone signicant
modications in recent years. These changes have resulted in farmers being
targeted by two strands of nancial aid or incentives. First, the reform of the
Common Agricultural Policy has seen the introduction of the Single Farm
Payment Scheme and Cross Compliance. The Single Farm Payment is a pay-
ment made to farmers which is decoupled (partially in many cases) from
current production. The Single Farm Payment is meant to replace all previ-
ous forms of commodity support so that the EU can move towards compli-
ance with the demands placed on agricultural policy as a result of the General
Agreement on Tariffs and Trade/World Trade Organization trade negotia-
tions. The UK Department for Environment, Food and Rural Affairs (DEFRA,
2007) reports that the Single Farm Payment attracted 2.4 billion in expendi-
ture in 2006. This compares with 346 million for AEP.
Initially, the Single Farm Payment is based on an agreed benchmark
anchored to each farms historic policy receipts; however, a phased shift
towards a at-rate payment system, differentiated only by region, is under
way. In order to qualify for receipt of the Single Farm Payment, farmers need
to satisfy the Cross Compliance standards and requirements (DEFRA, 2004)
of which there are two types.
1. Good Agricultural and Environmental Conditions (GAEC): maintain land in
appropriate condition includes requirements such as protection of hedges,
stone walls and watercourses. Dened by each member state in order to pro-
tect soils and ensure minimum level of maintenance and avoid deterioration of
habitats (especially for non-cultivated land, i.e. pasture) (Kirkham et al., 2004).
2. Statutory Management Requirements (SMRs): secure compliance with vari-
ous EU Regulations and Directives 18 in total.
Second, there has been a signicant reform and reconguration of AEP.
From early 2005 the UK introduced the Environmental Stewardship scheme:
ES is a new agri-environment scheme which provides funding to farmers and
other land managers in England who deliver effective environmental manage-
ment on their land. The scheme is intended to build on the recognized success
of the ESA and CSS and its primary objectives are to:
1. Conserve wildlife (biodiversity)
2. Maintain and enhance landscape quality and character
3. Protect the historic environment and natural resources
4. Promote public access and understanding of the countryside
Within the primary objectives, it also has the secondary objectives of: Genetic
conservation; and Flood management.
(DEFRA, 2005: 2)
Environmental Stewardship is composed of the Entry Level Stewardship
scheme (ELS), the Organic Entry Level Stewardship scheme (OELS) and the
Higher Level Stewardship scheme (HLS). These schemes replace existing
AEP such as Environmentally Sensitive Areas scheme (ESA), the Country-
side Stewardship Scheme (CSS), the Organic Farming Scheme (OFS) and the
Wildlife Enhancement Scheme (WES).
In terms of pest management activities, both the ELS and OELS are
highly relevant. Beginning with the ELS, this scheme is open to all land man-
agers in England with entry guaranteed providing scheme requirements are
met. This requires the land manager to select a number of environmental
commitments which earn points that are explicitly stated as part of the
scheme and, once the threshold of 30 points/ha is attained, entry is assured.
Entry is currently for 10 years with a contract initially for 5 years, which can
then be extended. Management options include things such as protection
and management of boundary features, woodland edges, the conservation of
soils and historic and landscape features. The ELS is designed to be simple
with little need for expert knowledge in terms of the form to be completed
other than that held by a competent farmer. The intention of the ELS is to
secure basic-level environmental management over as large a territory as
possible. Currently, the nancial payment is set at 30/ha per annum. The
OELS is very similar in terms of how it is intended to operate albeit with
slightly modied objectives and management options. The OELS attracts
slightly higher payments at 60/ha per annum.
Currently, ELS and OELS farm management requirement go beyond
Cross Compliance. However, the management options selected will comple-
ment, but not remove, obligations arising from Cross Compliance.
138 Chapter 4
Concurrent with these changes to agricultural policy there have also been
efforts in the UK to minimize the negative externalities associated with pesti-
cide use. Specically, there has been an industry initiative/programme called
the Voluntary Initiative on pesticides. The Voluntary Initiative has attempted
to bring about best practice in pesticide use by initiating research, training
and communication, and stewardship (www.voluntaryinitiative.org.uk). The
Voluntary Initiative was introduced in April 2001 after a long debate about
the appropriate policy mechanism to employ to deal with pesticide externali-
ties. The Voluntary Initiative was initially meant to last 5 years but it has
recently been extended on a 2-year rolling basis. However, there are still strong
reasons to assume that a pesticide tax will be considered again, given the Vol-
untary Initiatives 2-year rolling window of continued operation.
The Voluntary Initiative, as its name suggests, consists of a set of volun-
tary industry actions with the aim to reduce the impact of pesticides on the
environment. Examples of the types of programmes in the Voluntary Initia-
tive include research, training, communication and stewardship. The pack-
age of measures was devised by the Crop Protection Association in
collaboration with various industry bodies such as the National Farmers
Union. It has been estimated that the cost of the programme over the 6 years
it has been in operation is approximately 45 million (Voluntary Initiative
Steering Group, 2006).
The signicance of the Voluntary Initiative can be seen in the impact it
has had on the development of land options as part of the ELS. In particular,
the Voluntary Initiative supported a research project demonstrating that
skylark plots, which attract points for the ELS, can signicantly increase sky-
lark edgling survival. Also the Voluntary Initiative introduced Crop Protec-
tion Management Plans (CPMPs). These plans are a self-audit of farm-level
crop protection activities. The CPMPs were included in the ELS and at pres-
ent it is estimated that some 1.5 million ha are covered by approved plans.
Controversially, however, DEFRA have now removed this option from the
scheme.
The inclusion of the CPMP in the ELS provided a farmer with 2 points/ha.
The CPMP requirements were reasonably general, covering aspects of pesti-
cide use such as storage, handling and application. There was also an empha-
sis on the choice of pesticide product as well as the adoption of non-chemical
pest management options. Those practices considered here included the use
of deliberate crop rotations, cultivations practice and timing, the planting of
resistant crop varieties and the use of natural predators via habitat enhance-
ments such as beetle banks and eld margins.
In an effort to understand what farmers are currently doing with respect
to pest management we can consider what types of actions and activities
have been adopted as part of the ELS. Boatman et al. (2007) have examined
the uptake of the ELS to date and their results provide an interesting insight
into how this scheme has inuenced pest management strategies on farms.
Currently some 27,000 farmers participate in the various Environmental
Stewardship schemes compared with some 170,000 non-participants. As we
might expect, farmers adopt management and land-use practices that make
least change to current farming practices. Boatman et al. (2007) estimate that
60% of ELS activities entered into the scheme were already being done in the
desired manner, which raises questions regarding over-compensation. How-
ever, there has been a large increase in the land area and number of agree-
ments under AEP since 2005 and the introduction of the Environmental
Stewardship scheme.
In terms of land area the ELS agreements cover some 3.5 million ha with
the highest proportion being in eastern regions. Cereal farmers are the larg-
est group of participants by type, both in terms of number and area. It is also
the case that cereal/cropping farms have adopted the largest number of
options in the ELS per farm: on average, 8.6 options for cereals and 9.0 for
general cropping. If a farm has adopted a large number of practices it is pos-
sible that they have adopted some of the options that proved less popular
overall. The reason given by farmers for the adoption of particular options
was the points gained. This may have been particularly acute in the case of
arable farms since, for these farm types, gaining points was difcult because
of the existing farming systems, landscape and land-use patterns.
So what practices and options have proved popular? Again as might be
imagined, those options which require little in the way of systems changes,
little signicant land-use change or those which alter land use on marginally
productive areas have proved popular. These include hedge and ditch man-
agement, eld corner management on arable farms (popular in the east), and
4 m and 6 m buffer strips on cultivated land.
Those options which have proved far less popular can be summarized as
those which require additional effort, signicant investment or land-use
change on more productive land. These include the use of buffer strips on
intensive grassland, wild bird seed mix or pollen and nectar mix on set-aside,
beetle banks, skylark plots, conservation headlands and uncropped culti-
vated margins on arable land, and all options to encourage a broader range
of crop types on farms.
As we have already noted, the CPMP from the Voluntary Initiative had
been included as a management option within the ELS. From the most recent
data available we can see that this option was adopted by 10,164 farms or
39.5% of all farms in the ELS. As might be expected, many of the farms adopt-
ing CPMPs are cropping dominated farms (see Table 1.16 in Boatman et al.,
2007: 28), some 69.3% of cereals farms and 76.1% for general cropping farms.
The average area entered into CPMPs is 195.1 ha. However, we cannot be sure
as to whether the ELS has helped to pump-prime the Voluntary Initiative or
whether the ELS essentially over-compensates existing activities here.
We can also consider the extent to which nancial incentives have encour-
aged farmers to adopt non-pesticide disease and pest management practices.
From the data we can see that the adoption of practices that may provide
non-chemical pest control is relatively low. Some important incentives built
into the ELS are summarized in Table 4.1 and here we note the relatively poor
take-up of those options of potential benet to conservation biocontrol,
namely beetle banks, pollen and nectar mix on set-aside and conservation
headlands.
140 Chapter 4
If we turn to the OELS, 167,000 ha were entered into the scheme mostly
located in the south-west. The area of uptake is greatest by lowland grazing
livestock farms and mixed and dairy farms. The percentage of cereals and
general cropping farms entering the scheme is very low; although cereal
farmers have enrolled the largest total area, the proportion of all cereal farm-
ers is much lower than for dairy or mixed. Even so, it is noteworthy that very
few organic farmers have adopted either IPM benecial beetle banks or sky-
lark plots, which might surprise some readers.
Research supported by RELU grant RES-224-25-0093, using a similar
approach as used by Lohr and Park (2002), presents an interesting picture of
current (2007) IPM adoption in UK arable agriculture. Data include observa-
tion on 547 farms. While the data set used in this case includes conventional
farms (92.6%), organic (5.4%) and farms with both conventional and organic
activity (1.9%), a high proportion of the sample does report adoption of a rela-
tively large number of IPM technologies on their farms. Respondents were
asked to report their use and interest in a prescribed set of IPM technologies.
For each technology considered, respondents were asked to indicate whether
they currently use, have discontinued using, will consider using in the near
future or will not use each technology. The results of this question for the 17
pesticide alternative practices are reported in Fig. 4.1.
The results reported in Fig. 4.1 show a strong gradient of differential
adoption among the pest management practices considered, with some quite
widely adopted and others that are far less prevalent. Many of these results
are unsurprising a priori. An interesting (if less than surprising) result, how-
ever, is the relatively large number of farmers using improvements in eld
margins. This type of eld management requirement is part of many of the
AEP contracts and requires only a marginal addition to a land management
practice to that required by the Single Farm Payment scheme.
It is interesting to note that very few of the technologies appear to have
been discontinued following a trial phase. The highest level of discontinua-
tion of a technology is 15% for both pheromone monitoring and disease- or
Table 4.1. Financial incentives to encourage pest management in the Entry Level Stewardship
scheme. (From DEFRA, 2005; Boatman et al., 2007.)
Option
Cereal farms
(%)
Cropping farms
(%) Points attained
EF2 (Wild bird seed mix) 17.7 21.0 450
b
EF3 (Wild bird seed mix on set-aside) 2.6 3.25 85
b
EF4 (Pollen and nectar mix) 11.3 13.1 450
b
EF5 (Pollen and nectar mix on set-aside) 0.9 0.9 85
b
EF7 (Beetle banks)
a
2.2 2.6 580
b
EF8 (Skylark plots) 3.6 3.4 5
c
EF9 (Conservation headlands in cereals) 0.4 0.7 100
b
a
This equates on average to 0.2 ha or 1 km 2 m wide.
b
Points per hectare.
c
Points per plot.
T
h
e

E
c
o
n
o
m
i
c
s

o
f

S
w
i
t
c
h
i
n
g

T
e
c
h
n
o
l
o
g
i
e
s

1
4
1
Fig. 4.1. Adoption of pest control methods. (From Bailey et al., 2009.)
0 10 20 30 40 50 60 70 80
Other options
Using a trap crop
Pheromone control
Introducing predators
Using mixed varieties within field
Pheromone monitoring
Using beetle banks
Floristic strips to encourage beneficials
Cultivation to control weeds
Spot spray
Rotating pesticide classes
Different varieties in different fields
Hand roguing
Disease- or insect-resistant varieties
Adjusting time of operations
Treating seeds
Improving field margins
Planned crop rotation
T
e
c
h
n
i
q
u
e
s
% of respondents
Discontinued
Consider for future
Currently used
142 Chapter 4
insect-resistant varieties. This would suggest that, if farmers do trial a
practice, then they are highly likely to continue to use, or to fully adopt, that
practice. Of the technologies being considered there would also appear to be
a degree of resistance to even trying some of them, in particular planned
rotations, treating seeds and hand roguing, although there appears to be a
reasonable likelihood that some of the currently less popular technologies
might be considered for adoption at some point in the future.
The data report that some 61% of farmers are using more than ve IPM
technologies within their pest management portfolios. Many of these tech-
nologies were probably adopted by farmers in order to comply with AEP
contracts. However, these data do suggest that broad-acre farmers are
employing diverse and complex IPM portfolios and that reliance on chemical
methods alone is rare. More specically, just 6% of these farmers reported
that they currently use introductions, within which we can consider biopes-
ticides an option. However, a further 51% of the sample expressed an interest
to trial these technologies in the near future. More generally, those technolo-
gies which can be considered in some way embodied in capital or material
goods are considered positively by 55% of the sample while 63% of the
respondent farmers consider the more disembodied techniques positively.
While arable farmers appear to favour IPM interventions which they can
provide from their own resources of land and labour, they do appear willing
to purchase IPM products.
The adoption data collected in this project were used to uncover the dif-
ferent types of IPM portfolios farmers use in the wider pest management
context. A principal components analysis revealed that the 17 pest manage-
ment techniques could be summarized by four distinct portfolio approaches.
This approach was used by Rauniyar and Goode (1992) when they consid-
ered the adoption of seven technologies by maize farmers in Swaziland.
These portfolios are described in Table 4.2.
It would appear that the specic problems faced by farmers in their crop
systems have a signicant bearing on portfolio choice and the portfolio
names suggest this. Regression analysis was then used to investigate further
Table 4.2. Distinct integrated pest management portfolios in UK arable crops. (From Bailey
et al., 2009.)
Portfolio 1:
Intra-crop
biocontrollers
Portfolio 2:
Chemical users/conservers
Portfolio 3:
Extra-crop
conservation
biocontrollers
Portfolio 4:
Weed-focused farmers
Trap crops Pheromones Field margins Cultivate weeds
Mixed varieties Different varieties Floral strips Crop rotation
Introductions Resistant varieties Beetle bank Timing of operations
Pheromones Spot spraying Hand roguing
Different varieties Treated seeds
Rotate pesticide classes
determinants of portfolio choice by farms. This analysis sheds very little light
on the Intra-crop biocontrollers. However, there appeared to be some sig-
nicant relationships in the other three cases. Factor scores for the second
portfolio, Chemical users/conservers, appeared to be associated with
increasing cropped areas (larger arable operations), with higher frequency of
insecticide application, and involvement in the ESA and membership of the
Voluntary Initiative. Organic status, perhaps not surprisingly, was negatively
related to this portfolio approach.
For Extra-crop conservation biocontrollers there appeared to be a statis-
tically signicant negative relationship with the number of insecticidal appli-
cations per crop; on the other hand, a positive statistically signicant
relationship with the proportion of land with tenant rights and membership
of the Voluntary Initiative. Certainly, the absence of tenant rights would
probably form a barrier to the adoption of habitat manipulations that require
some signicant investment, beetle banks for example. There were four stat-
istically signicant relationships between farm characteristics and scores of
Weed-focused farmers. Here, livestock farms with high levels of tenant
rights and those engaged in the HLS were less likely to opt for Portfolio 4,
while organic farms appeared to be more likely to adopt Portfolio 4.
One further regression model employed these data, alongside a range of
farm characteristics, to assess the impact of portfolio choice on differential
rates of insecticide application intensity (number of insecticide applications
per crop) across farms.
Results suggested that arable farmers who rely on independent crop
consultants for their spray advice, are members of the ELS and have adopted
Portfolio 2, Chemical users/conservers, tended to spray for insect pests
more frequently. The results also suggested that farmers who follow prac-
tices described by IPM Portfolio 1, the Intra-crop biocontrollers, appeared
to have applied chemical insecticides in a less intensive manner than did
their peers. Two further nearly signicant relationships were those for
membership of the Voluntary Initiative and the proportion of land farmed
conventionally. Both of these results tentatively suggested a positive effect on
applications, albeit at a condence level of only 89.3% and 87.0%, respect-
ively. The two statistically signicant relationships for Portfolios 1 and 2
conrmed prior expectation in terms of sign since it seems reasonable to
assume that intra-crop biocontrol strategies should reduce reliance on chem-
ical pesticides while practices aimed at reducing selection pressure on pesti-
cides might still result in a signicant reliance on pesticides. Furthermore,
while it is not surprising that efforts to control weed problems have little
impact on insecticide use, as found for Portfolio 4, it is surprising, if not dis-
appointing, to nd no evidence of an impact of using Portfolio 3, Intra-crop
conservation biocontrol practices, on insecticide use. Moreover, it is interest-
ing to note that this research found that membership of the ELS, with its
focus on environmental land-use change and CPMPs, was counter- intuitively
correlated with a greater intensity of insecticide applications. Likewise, while
statistical power was lacking, the positive effect of the Voluntary Initiative on
insecticide spray intensity was also striking. Such results call for further
144 Chapter 4
work to uncover in more detail the impact of the Voluntary Initiative on
pesticide use, given the UK Governments current reliance on this policy for
pesticide use and impact reduction.
Recently the potential scaling impacts of IPM and biodiversity have been
considered by the scientic (Grifths et al., 2008a) and policy-making (Franks
and McGloin, 2007) communities. The potential for farmers to create, at least
local, network external benets in the provision of biocontrol and other con-
servation goals is now being considered. To this end, coordinated or coop-
erative bids submitted by groups of neighbouring farmers for collective AEP
funding could provide the key to gaining otherwise elusive scale and network
benets from agro-ecosystem services.
The picture we see of a rather passive adoption of IPM portfolio prac-
tice, induced in no small measure by AEP, is likely to require farmers to
employ extensive crop-walking if benets from adoption are to be gained.
Since farmers are unlikely to have chosen ELS options in a conscious effort
to limit their reliance on chemical pesticide, we cannot expect farmers to
subsequently modify their pest control strategies unless they already spray
reactively in response to economic damage thresholds. While economic
damage thresholds are relatively simple to understand and apply when
considering chemical control alone, the cognitive process of assessing the
benets from spraying becomes excessive in an IPM context. The identica-
tion of the presence of a damage agent is not enough. The farmer needs to
consider what other practices or pest control mechanisms are present in a
given site, how quickly and effectively they might be expected to act, and
the risk of their failure, before an intervention, which could be chemical
pesticide, a biopesticide or a pheromone, can be decided upon. Such com-
plexity of decision calls for a decision support tool preferably one that
includes economic price information alongside pest control response func-
tions. Our current state of IPM knowledge is some way off the level needed
to produce such a set of rules.
Key Challenges for Further Research and Development in Integrated
Pest Management
Research and development activity is typically split into separate activities.
Traditionally, the public sector funds fundamental research that discovers
new technologies through the acquisition of new knowledge. It is widely
believed that the public sector should do this since private individuals and
rms will not ll this role, although examples of fundamental science in the
private sector do exist. The product of this fundamental science is then left to
the private sector to develop in the form of patentable products which
embody the new technology. Patent holders can then exclude other produ-
cers from producing, and non-purchasers from using, their technology while
recovering their developmental costs through the price of the product.
There exists a split, then, between the research and developmental
phases of technology innovation and delivery, which potentially suits
patentable new technologies but leaves others forms of technology behind.
Further, if farmers adopt portfolios rather than individual IPM compo -
nents separately, then the commercial exploitation of IPM could easily suffer.
Either private innovators need to recognize that the success of their
product-based technology requires the parallel development of system-based
portfolio partner technologies and fund development of both, or government
needs to take up the challenge of funding the development of systems, or
disembodied, IPM components.
Future research is required in two areas.
1. Further research to understand the role different technologies play within
alternative IPM portfolios in terms of both yield and cost and risk comple-
mentarity. We need to understand the type of relationship between IPM com-
ponents such that we can prescribe portfolio mixes of techniques which build
both improved efcacy and sufcient resilience into portfolios.
2. Research and evaluation must be conducted on an extensive scale. This
is unlikely to be affordable if conducted by the public sector and especially if
conducted using conventional experimental control approaches. This work
must also consider the dynamic time frame of problem identication, action
and outcome of IPM portfolios. As Grifths et al. (2008a) point out, we do not
know the effect of scaling up individual IPM component technologies, let
alone know whether IPM portfolios exhibit increasing, constant or decreas-
ing returns to scale. Given obvious budget constraints and the need to con-
sider the performance of diverse technology sets in complex environmental
settings, the logical approach will probably follow the approach used in the
farm-scale evaluation of herbicide-tolerant transgenic crops in the UK (e.g.
Firbank et al., 2003; Perry et al., 2003).
Both of these strands of research are required in order to:
1. Redesign AEP policy so as to promote a more appropriate set of IPM
portfolios that do reduce the commercial use of chemical pesticides in farm-
ing systems.
2. Consider the reintroduction of CPMPs redesigned to explicitly pro-
mote IPM.
3. Persuade farmers of the efcacy, resilience and compatibility of IPM
portfolios in their farming systems and encourage them to rely upon the
action of the portfolio mix before reaching for chemical remediation.
4. Generate IPM portfolio specic decision support protocols, allowing
farmers to select the practices available at, and other key features of, each
site, for crop protection interventions.
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148 (A. Bailey et al.)
5
The Regulation of Biopesticides:
an International Analysis
The regulation of biopesticides takes place within a regulatory system that
was designed for the regulation of synthetic (chemical) pesticides. Hence, the
system has a number of features that did not make it amenable to the regis-
tration of biological pesticides and a number of adjustments have had to be
made to the system to facilitate their registration. In this chapter there is a
discussion of the Biopesticides Scheme in the UK and the equivalent Genoeg
Scheme in the Netherlands. The chapter concludes by drawing on the lessons
learned from experience in a range of countries to set out design principles
for a better regulatory system for biopesticides.
Within the EU, the registration of pesticides involves both member states
and the European Commission. In the USA, regulation is principally under-
taken at the federal level by the EPA but there is some involvement of the
individual states. The OECD and the World Health Organization (WHO)
also have an inuence on pesticides regulation and their role is discussed
more fully later in the chapter.
Limitations of the Current Regulatory Model
The system of pesticides regulation was established to deal with chemical
pesticides, which remain the predominant type of plant protection product.
As Waage notes (1997: 11), Biopesticides, being living organisms, have
properties which make their design, production and use potentially very
different from that of chemical pesticides. However, present and planned
development, production and delivery of biopesticides usually follows a
chemical pesticide model. Thus, The pesticide regulation system has been
developed for regulating conventional chemical sprays developed by
large companies and several aspects of it do seem to act as barriers to the
further development and commercialization of alternative control methods
The Regulation of Biopesticides 149
(ACP, 2004: 34). One of the objections made by those opposed to pesticides is
how pesticides are spread directly into nature, unlike industrial chemicals
(Blok et al., 2006: 321). Given that biopesticides come from nature, these
objections do not apply in the same way, but this has not been fully recog-
nized by the regulatory system, which has taken insufcient account of the
specic benets of biopesticides.
Waage argued (1997: 16): [It] is not the industry alone, but the entire
pesticide regulatory process which has not adapted itself to the new oppor-
tunities which biopesticides provide. Biopesticide development found
itself locked into an inexible and unimaginative chemical pesticide
model (Waage, 1997: 14). In the years since Waages article was written,
considerable progress has been made towards the reduction of the regula-
tory barriers to biopesticide availability, not least through initiatives such
as the UK Biopesticide Scheme discussed later in this chapter.
Pesticide Registration in the UK
The UK operates within an EU regulatory system for pesticides that, as one
would expect in a system based on multi-level governance, is made up of a
two-tier system of registration. The regulatory regime is currently in a transi-
tional period where some major pieces of national legislation are being
replaced by new, harmonizing EU legislation, a process that is discussed
more fully later in the chapter. Pesticides are composed of specic com-
pounds designed to adversely affect a pest and are combined with inert
substances to improve their handling, application and effectiveness. Active
ingredients are assessed at a Community level for inclusion on a positive list
(known as Annex 1). Products containing chemicals listed on Annex 1 must
then be assessed and registered by member states. Active ingredients in exist-
ing plant protection products are reviewed as part of a rolling programme
that is focused on products that were already on the market before the mid-
1990s. The maximum permitted residue levels for pesticides in crops (MRLs)
are laid out in legislation. These are not safety levels, although they may be
perceived as such by consumers, but are based on the maximum residue that
should be present if a pesticide has been used according to its approval.
Within the UK, what was the PSD but became in April 2009 the CRD,
constituted as a directorate of the Health and Safety Executive (HSE), has
been the agency responsible for the registration of agricultural pesticides.
In response to the Hampton Review of the regulatory sector, PSD became
a distinct entity within the HSE in April 2008. The merger is based on PSD
maintaining its identity, structure and current business (PSD, 2008a: 3).
Before April 2009 other pesticides known as biocides were dealt with by
the HSE from an ofce in Bootle. Biocides are now also dealt with by the
CRD, still from the Bootle ofce, while what was PSD continues to operate
from York. How these geographical arrangements will develop in the lon-
ger term remains to be seen, but as a bureaucratic joke what was PSD is
sometimes referred to as Bootle East. In this chapter, we shall continue to
150 Chapter 5
refer to PSD in relation to events before April 2009, but use CRD to refer to
current practice.
The basic framework for PSDs (and CRDs) activities is set out in the
Food and Environment Protection Act 1985 and the Control of Pesticides
Regulations 1986. The Plant Protection Regulations 1995 implement the
European Directive (91/414/EEC), which regulated plant protection prod-
ucts. Within the EUs mutual-recognition framework for regulatory approval
and licensing, it sought to be the market leader and took an active part in
pesticides standard-setting (Hood et al., 2003: 126). PSD was originally part
of the Ministry of Agriculture, Fisheries and Food (MAFF), but was consti-
tuted as a quasi-independent executive agency in 1993. After the dissolution
of MAFF, it subsequently reported to the Department for Environment, Food
and Rural Affairs (DEFRA) where it also advises ministers on pesticide
issues. It had a staff of 178 in 2008, 115 of whom are scientists.
CRDs policy work is funded by a grant from DEFRA. Its approvals and
registration work is undertaken on a cost recovery basis, through charges to
the rms seeking registration and a levy on approval holders. The levy is
designed to cover the cost of reviewing older pesticides and monitoring
pesticides use and residues in food. It is based on a percentage of annual
turnover arising from sales of approved pesticides. In 2006/7 out of a PSD
total income of just over 13m, 5.3m came from the policy grant, 3.8m from
the levy and 3.2m for fees, the balance being made up by incidental income.
Before granting marketing approval to a product conferring plant
protection, the CRD evaluates data on human toxicity, environmental toxi-
city, pest control efciency and potential to leave a residue on treated food
crops. Recommendations for approval by the CRD are then forwarded to the
ACP, a committee of independent experts. PSD and HSE provided the secre-
tariat for the ACP but we are separate from, and independent of, these
organisations (ACP, 2005: 21). It would not be practical for the ACP to deal
with every minor amendment to an approval so the Committee deals directly
with the most important decisions, e.g. rst commercial level approval of
active ingredients new to the UK or any applications which appear to raise
new concerns about safety. The nal approval decision is taken by the respon-
sible minister acting on the advice of a civil servant, but the minister is
unlikely to overturn a recommendation made by the ACP. Advice from
the ACP comes forward in written form from the Secretariat of the ACP to
ofcials in Departments Once received, the advice is acted on directly
by ofcials on behalf of Ministers this is the case for technical issues and
routine regulatory decisions (RCEP, 2005: 79).
The Royal Commission on Environmental Pollution (RCEP) report on
Crop Spraying and the Health of Residents and Bystanders was critical of the ACP,
arguing in particular that its present approach may be conservative and pro-
tective in its treatment of targets (RCEP, 2005: 59). The RCEP report drew a
robust response from the ACP which sought to draw attention to various
errors of fact and logic in their report. We note that several of its important
conclusions appear to have been reached after what we consider to be an
incomplete consideration of the relevant evidence (ACP, 2005: 4). In its
response, the RCEP claimed that We do not set out to criticise the ACP or sug-
gest that UK practice is in any way less rigorous than elsewhere (RCEP, 2006:
5). Nevertheless, we remain concerned that the ACP seems unable or unwill-
ing to accept that most of its advice to Ministers is based on an implicit judge-
ment, in a context of scientic uncertainty, about the relative importance of
public concerns about human health and well being (RCEP, 2006: 78).
Minor use crops: commercially signicant but lacking protection
The term minor uses is in many ways an unfortunate one as it encompasses
eld vegetable crops and fruit that are of some signicance, such as carrots
and peas. A minor use is dened in terms of one that occupies less than 50,000
ha so that potatoes and sugarbeet are above this dividing line in the UK.
Brassicas are below this line, but, on the whole, there are very few crops in
the 15,00050,000 ha bracket. What is characteristic of minor uses is that the
minor crops typically have available to them, given the relatively small size
of the market, a small number of plant protection products that do not cover
all the pest, disease and weed problems of that crop, or fail to provide choice
between products to minimize the development of resistance to single pesti-
cides. The loss of one active substance or its availability for use on minor
crops could cause major difculties and ultimately a situation could arise in
which the crop could not be grown economically.
Carrots and parsnips provide an illustration of the problems that can
arise. For carrot y control, there is a now a diminishing range of active ingre-
dients available that can deal with the problem. The Commission proposals
under the revision of Directive 91/414/EEC could remove further substances
which are important for the protection of carrots and parsnips with a poten-
tial for the loss of all yield. [The] majority of the currently approved herbi-
cides would no longer be available, and the control of some major weed
species (e.g. mayweeds) would not be possible. This could have signicant
commercial consequences. Weeds affect quality in terms of size, grade and
uniformity. This is particularly important for baby carrots for quick-freezing
or canning and fresh market. Failure to meet specications can result in crop
rejections or no sales (PSD, 2008b: 36).
In 2003 PSD set up the Minor Uses Network to provide information and
advise it on issues affecting the minor use sector. The coverage of the group
was actually wider than minor crops to ensure that niche pest problems on
major crops are adequately covered. This Network was not operating in 2009,
but there was discussion about resurrecting it. The existence of the UK Minor
Uses Network stimulated the Commission to set up the Minor Users Steering
Group. This represented all member states, but in practice there were a rela-
tively small number of member states who are very active. Like the UK Minor
Uses Network, a primary function was information exchange. A participant
commented in interview: Looks at common problems and solutions, gets
companies to develop actives on [a] broader range of crops and situations
Helped get more authorisations, enables much better co-operation, help to
152 Chapter 5
share, exchange or even sell data. However, by 2009 the Network had faded
due to a lack of funding. Several member states wrote to the Commission to
express their concerns. The new plant protection Regulation passed in 2009
obliges the Commission to report on the scope for a minor uses fund by the
end of 2011.
Off-label approvals
Off-label approval provides a mechanism to make available approved plant
protection products to deal with an economically damaging level of pests in
a minor crop for which there is not a current on-label approval. One route has
been the Long Term Arrangements for Extension of Use (LTAEU), introduced
as a temporary measure in the late 1980s, which in effect allowed the use of
pesticides on a minor crop providing that an approval exists for use of the
same pesticide on a major crop. These arrangements did not t in with the
EU regime where specic approvals are required for all uses. PSD concluded
that the LTAEU could not be maintained and those relating to edible crops
were no longer valid from January 2007.
Growers or their representative organizations can apply for the approval
of a pesticide on a specic crop under a Specic Off-Label Approval (SOLA).
Such applications have to be supported by a reasoned case that covers the
nature of the problem which must include reference to a named pest. Details
must also be provided of the scale of the problem including its severity and
scope and the potential for economic damage. One retailer argued in inter-
view that more use should be made of the off-label approval route, stating
You could use the retailer muscle to move that forward. Thats where PSD
and DEFRA should be looking.
Maximum residue limits
MRLs are in effect a parallel system of regulation. The purpose of them is to
ensure that residue levels do not pose unacceptable risks to consumers. It is
important to emphasize that the MRL is not a health-based exposure limit,
and exposure to residues in excess of an MRL does not necessarily imply a
risk to health. Use of a pesticide would not be permitted in the rst place if it
led to exposure to pesticide residues above safety limits.
MRLs are established on the basis of the highest residue expected when
a pesticide is applied in accordance with the approved conditions of use.
MRLs applicable to UK trade are decided primarily at an EU level. However,
although there are already more than 25,000 limits in force across the whole
EU, member states also had the right to x individual caps where the EU
statute book is silent, and created over 100,000 according to European
Commission estimates.
EC Regulation 396/2005 came into effect on 1 September 2008 to harmo-
nize member state caps on pesticide levels. At the centre of the new rules is a
phased-in harmonization of all MRLs specic to individual member states.
All MRLs will either be substantive or temporary Community levels. The
Commission will handle risk management, working on the basis of risk
assessments from the European Food Safety Authority (EFSA). Member
states will keep responsibility for enforcement, although the Commission
will attempt to coordinate their efforts. A PSD ofcial commented in 2008:
MRLs will be harmonised, but it will be slow. It will get worse before it
gets better.
In the UK the Pesticides Residue Committee is an independent commit-
tee that supervises a programme of pesticide residues surveillance in food
and drink at the point of sale with the work carried out on its behalf by the
PSD. Generally very small numbers of samples are found to contain residues
in excess of the MRLs. In the third quarter of 2007, 537 (71.7%) of 749 samples
of 13 different foods had no detectable residues and 207 contained residues
below the MRL level. The results showed that ve samples (0.7%) contained
residues in excess of the legal levels.
The practical difculties that can arise from MRLs for growers can be
illustrated by the case of dieldrin and courgettes. The use of dieldrin ceased
in the mid-1970s, but it is still persistent in the soil. It can be extracted from
the soil and concentrated in courgettes, pumpkins and water squashes, with
uptake higher when the soil is particularly dry. Levels of uptake can vary
signicantly within one eld. The residue issue is not one related to use, as
there is no acute toxicology risk, but to environmental contamination and
movement through watercourses. In 2006 the MRL level of 0.05 ppm was
reduced to 0.02 ppm. In practice a number of plants are on or just above
0.02 ppm with a maximum of 0.03 ppm. From the growers perspective, this
created a situation in which the only way in which courgettes could be grown
without breaching an MRL was hydroponically.
PSD reassured the grower that they would not take enforcement action,
but the grower was concerned about the reputational damage resulting from
adverse publicity. EFSA was to carry out a review of the toxicology of increas-
ing the MRL. However, a PSD ofcial commented: EFSA approach it in a very
purist way. This was the separation of risk assessment and management. It
goes back to the whole BSE story. A more positive view of EFSA from within
PSD was that EFSA is transparent, [it] forced [the] pace on transparency,
getting Draft Assessment Reports into [the] public domain.
In our interviews with retailers, some expressed the view that consumer
misunderstanding of MRLs could lead to commercial damage. Retailers hire
technical experts to check a sample of their produce to see if MRLs have been
exceeded and take follow-up action with suppliers if this does happen. A
number of retailers commented that problems were more likely to arise with
imported produce, especially exotic fruit. One retailer commented: Growers
are using far less chemicals than they have ever done, food has never been
safer if only the public would realise that. Another commented: Europe,
dominated by green parties, focus[es] on MRLs. Have had a number of MRLs
raised in recent years without any justication about whether it is right or
wrong. We need to think about what we mean by residues.
154 Chapter 5
Enforcement and the black market
Chemicals are among the most strictly regulated of substances because of
their hazardous and toxic properties, and Pesticides are among the most
strictly regulated of all chemicals (House of Commons, 2005: 6). Pesticides
emerge as a special risk regulation domain, characterized in terms of
toxicological attributes, comparative strict regulatory controls and social
benets (Blok et al., 2006: 321). [The] data requirements that were xed for
pesticides greatly exceed those required for any other class of substance
including pharmaceuticals, food additives and commodity chemicals
(European Commission, 2001: 3). When one has a strict system of regulation,
a black market invariably appears. In the following discussion, a distinction
is made between the black market of illegally marketed products and the
grey market of products that fall outside the regulations but are competitors
to biopesticides.
It has been estimated by the European Crop Protection Association
(ECPA) that 57% of Europes supply of crop protection products is fake.
Criminal organizations are involved in this trade and [t]he use of fake or
illegal substances to treat crops is growing at an alarming rate (Bounds,
2008). About 90% of the fakes come from China, with India being another
source. At the British Crop Protection Council congress in 2005, lawyers
acting for agrochemical companies served 37 injunctions on 19 separate
Chinese companies. At the 2006 congress, one Indian and 23 Chinese compan-
ies were given legal warnings and three were ordered to cease commercial
activity, after illegally promoting products. Ukraine has become an impor-
tant crossroads in this trade. Differences in packaging may be very small and
the rst the grower may know that the product is not genuine is when the
spray nozzle jams or the crop fails to respond in the expected way. Some of
these sales may be made through the Internet, in other cases farmers have been
targeted by text messages and in some cases the product comes from other-
wise reliable distributors who have unknowingly purchased the material.
In late 2006 German authorities found isofenphos methyl, an illegal
pesticide, in peppers from southern Spain. Raids led to the arrest of the pres-
ident of the local cooperative and the seizure of 4000 kg of illegal pesticides
among the greenhouses of Almeira, the centre of Spains fruit and vegetable
industry. However, the difculties of dealing with such problems were
emphasized by a retailer who discussed the Spanish case in interview:
Technical managers y out and try to get the bottom of it, more often you
cant. Someones touting an illegal, dealing with a central pack house with
hundreds of growers in Almeira. One consequence of these events was that
pepper orders fell by a fth as purchasers sourced elsewhere and prices halved.
These economic effects had an impact on Spanish regional governments who
encouraged more extensive use of biopesticides. Spain wants to transfer 38,000
ha of its vegetable production area to IPM with a focus on biocontrol by 2010
and is prepared to offer nancial support of ?1000/ha (Ehlers, 2007).
In 2008 PSD warned growers to watch out for a counterfeit herbicide
labelled as Emrald Wotsit. Nearly 3000 l of the counterfeit material had been
identied, which had been manufactured on a different formulation from the
approved Emrald Wotsit formulation. The formulation has been manufac-
tured in Yorkshire and appeared to be originally intended for export, on
which there are no controls. But the formulation had then been labelled as
Emrald Wotsit for use in the UK, making it illegal to sell or use it, as well as
constituting a breach of cross-compliance regulations.
Within the UK, PSD considers that the evidence points towards a small
number of well-organized and persistent offenders, perhaps ve or six. What
makes things more complex is that not all the sales made are counterfeit pro-
ducts. The products targeted vary but are more likely to be older chemicals,
which farmers are familiar with, but have had recent restrictions. An impor-
tant feature is that they are usually for common pest and disease problems
with high demand and high potential prots (Abram, 2006). Prosecutions are
very difcult and expensive because of the technical complexity of the cases.
However, effective enforcement does not always require prosecution. PSD
can issue enforcement notices which require remedial action to be taken. These
can include monitored disposal of illegal products at the owners expense.
The grey market of biostimulants, foliar feeds and plant strengtheners
is of particular concern to biopesticides manufacturers. Marketing products
in this way is entirely legal so long as these products make no claim on their
labels to control pests. Some of them are actually registered elsewhere as
pesticides. It was estimated that as many 30 products were being sold as bio-
stimulants in the UK in 2007, creating a way of going round the system of
regulation. A manufacturer expressed the dilemma in the following terms:
Because of the grey area around biostimulants and physical products, the
grower does not feel condent of using biopesticides because of products
sold with a wink and a nod. [If] the grower spends a couple of years using
the product, then nd[s] it doesnt work, [it] undermine[s] condence in
biopesticides. Muck and mystery products. There is a lot of passing off going
on; this product is as good as that one. The whole biopesticide product range
is brought into disrepute.
In a 2009 paper the International Biocontrol Manufacturers Association
(IBMA) noted that some of its members were becoming increasingly aware
that there are some products in the market place that are being described as
biopesticides but which are not registered. What is not clear is whether
these products comply with the legal requirements (IBMA, 2009).
The IBMA saw the issue as falling into ve categories.
1. Products containing microorganism active substances listed on Annex 1
(the main list of active ingredients for inclusion in plant protection products),
being sold in the UK without national approval. While the regulations are
isolate specic, the situation for additional examples of products of the same
species is unclear.
2. Products containing active substances not included in the current EU
review, with unproven efcacy, making claims of direct pesticidal activity.
3. Some products, particularly microorganisms, have both plant protection
qualities and plant growth stimulant properties.
156 Chapter 5
4. Products containing active substances, with known pesticidal activity,
being sold without national approval as plant tonics, foliar feeds or other
nutritional supplements.
5. Products incorporated into growing media, composts or as amendments
that may include Annex 1 active substances or be considered as biopesticides.
In the Netherlands, a claim about plant strengthening falls under regula-
tions involving indirect effect. All substances inuencing plants are considered
plant protection products. However, in Spain some 700 products are regis-
tered as phyto-forticants. Biopesticide producers consider that it is too
easy to get under the radar with some products, but some grey market pro-
ducers argue that they are unfairly targeted and are an important source of
innovation.
Efcacy testing
The key efcacy issue is whether the product provides a measurable benet
when used according to its label recommendations. Efcacy testing raises a
series of issues in relation to biopesticides. In the USA applicants for registra-
tion of biopesticides are not required to submit efcacy data, although they
must have it available; but the USA is rather unusual in this respect in terms
of national systems of regulation. Efcacy testing presents a number of chal-
lenges for biological products. With chemical products if a product works in
the laboratory, it usually works in the eld. Chemicals can be tested using
quite small treatment plots but biologicals need larger plots to get statisti-
cally signicant results because individual replicates are more variable: there
is greater complexity and variation because they are living organisms. For
the small and medium enterprises (SMEs) that produce biopesticides, the
cost of efcacy trials can be a signicant consideration. For a major crop or
pest, ten trials are normally required, with three trials for a minor crop or
pest. These would normally be undertaken over 2 years across a range of
locations. A survey of 21 companies conducted for the REBECA project found
that, across the EU, the average overall cost to achieve EU Annex 1 inclusion
was ?1.89 million, of which 21% was accounted for by efcacy tests (Hokkanen
and Menzler-Hokkanen, 2007). One UK respondent claimed that efcacy
testing could account for 50% of the registration costs for biopesticides as
against 10% for chemicals. This gure is at the high end of the range, but
another respondent suggested that costs in the UK of generating data were
particularly high.
Why not let the market decide whether a product is efcacious? As a
grower commented in interview, If a product was safe but we didnt know it
would work wed have a look at it. PSD starts from the position that the
Food and Environment Protection Act requires it to ensure that methods of
controlling pests are efcient. It is therefore important to authenticate the
claims made on the label about the product. This is a means of protecting
users from deceptive claims about snake oil products. A product must meet
the EPPO Principles of Acceptable Efcacy so that it is signicantly superior
to the untreated control. In terms of Directive 93/71/EEC, efcacy data need
to cover the justication of pest status of targets, the minimum effective dose
and the use of ofcially recognized testing organizations. Firms developing
biopesticides are not generally themselves ofcially recognized to carry out
their own efcacy trials. It is therefore important that they listen to advice
from the ofcially recognized contractor and not insist on their own trial
designs, which may be scientically interesting but not necessarily what is
required for registration purposes. A further category was recently introduced
to the UK Ofcial Recognition Scheme for Biologicals and Semiochemicals
Trials/Tests. This will allow organizations conducting work on microorgan-
isms or semiochemicals to apply for ofcial recognition in a more limited and
specialized category of work than was previously possible.
Apart from the need to meet statutory requirements, PSD would argue
that regulation can be seen as a costbenet analysis with the consideration
of product efciency being the benet analysis. In its view efcacy is not an
additional regulatory burden: the questions that PSD are asking are ques-
tions that applicants would be asking anyway to ensure that they have a
marketable product. PSD would argue that it is exible and pragmatic
about sources of evidence, primary data, mode of action, resistance, dose
response and glasshouse screening. There are no preconceived levels of
effectiveness required for registration of a biological product. PSD can
accept something with lower efcacy if it provides other benets such as
toxicological and environmental. If a worthwhile benet can be shown,
then a claim can be approved with an appropriately worded label to reect
the underlying data.
There is an issue about whether it is necessary to destroy crops used for
trials. High-value crops can be worth up to a million pounds. The PSD view
is that it cannot compromise safety by allowing products to go into the
supply chain, but there may be further scope for exibility on this issue.
Biopesticides Scheme
Concern about the lack of availability of biopesticides in the UK led to the
introduction of the Pilot Project in June 2003 to facilitate their registration. Its
aim was to increase the availability of biological pesticides in the UK by
improving knowledge and raising awareness of PSD requirements and how
to meet them. Prior to the introduction of the scheme, three active substances
and four products were approved between 1985 and 1997. In April 2006
the Pilot Project was replaced by a Biopesticides Scheme. This covered four
categories of products: (i) semiochemicals; (ii) microorganisms (bacteria,
fungi, protozoa, viruses); (iii) natural plant extracts; and (iv) other novel
products on a case-by-case basis (no such cases had arisen by 2008). Since the
introduction of the Pilot Project, seven products have been guided to
approval. In April 2007 ve products were at various stages of evaluation
and several other companies were discussing possible applications with
158 Chapter 5
PSD. Two products were approved in 2009 and several were at various stages
of the registration process.
In order to operate the scheme PSD developed an internal biopesticides
group made up of a team of specialists, including an assigned Biopesticides
Champion, who understand the issues, have received specialist training and
are continuing to learn. PSD thought it was desirable to involve as many
people in an Approvals Group for this work as possible, rather than having
a dedicated unit that would probably have insufcient work. These staff
members are able to participate in pre-submission meetings with applicants.
Particularly if they are held early in the process, they can help applicants to
plan the acquisition of the data they need for registration and also avoid the
compilation of any material which would be superuous. In particular, it is
helpful to hold a pre-submission meeting before efcacy trials take place.
A number of such meetings were observed on a non-participant basis as
part of the research. A typical meeting might last for 3 or 4 hours with differ-
ent experts from PSD joining the meeting as required. The meetings enabled
the identication of gaps in the application dossier and mutually helpful
discussions of how these could be lled, for example, through published
data.
Reduced fees are charged for biological control agents: 22,500 for bio-
pesticides; 13,000 for pheromones; and 7500 for taking either through
EFSA procedures. These fees were not increased in March 2007 when other
fees went up. Before the introduction of the Pilot Project, there was a stan-
dard fee of 40,000 for everything termed a biological. In comparison, the
cost of core dossier evaluation, provisional approval and EFSA review for a
synthetic would be between 120,000 and 180,000 from March 2007. CRD
intends to continue to operate the Biopesticides Scheme with reduced fees.
The scheme has had to face a number of challenges. It has involved PSD
reaching out to non-traditional customers who may be suspicious of the
regulatory authority because they have no experience of working with it. As
a consultant commented, Pre-submission is a key element because registra-
tion is still an unknown, a lot of fear, people want me to hold their hands,
introduce them to PSD. For their part, applicants need to have realistic
expectations. Putting an application in too quickly in the hope that the prod-
uct will be available for the next harvest may reduce its quality. From a PSD
perspective, the hope is that submissions will be of higher quality, needing
less work and taking less time to process, thereby reducing the costs
involved. An underpinning element of the PSDs work on biopesticides
could be interpreted as giving it rst mover advantage as the preferred
registration authority for such products within the EU. It was claimed that
Our biopesticides scheme is now a pathnder in Europe (Davis, 2008).
The European System of Regulation
This section explains the EU system of regulation as it operated in 2009,
including a consideration of the way in which the review of actives is
reducing their availability. Major criticisms of the EU system in terms of
timeliness are considered.
It considers the problem of mutual recognition and possible solutions to
it. The major revisions to the EU legislation which took place in terms of the
review of Directive 91/414/EEC, its repeal with Directive 79/117/EEC and
its replacement in 2009 by Regulation 1107/2009, along with the thematic
uses strategy for pesticides and the framework directive on sustainable use
are considered with particular reference to biopesticides. Reference is also
made to the possible implications of the Water Framework Directive
(2000/60/EEC) for which the implementing legislation came into force in
2004. There is then a consideration of two member states with very different
systems of regulation, Denmark and the Netherlands.
The 91/414 European system
Directive 91/414 was a new departure for the Community in several respects.
It was one of the rst major items of legislation to anticipate not only the
principle of subsidiarity, but also the precautionary principle (European
Commission, 2001: 3). Its basic procedures remain intact in 2006/0136 (COD),
but with some important modications. The registration process is divided
into two parts: Annex 1 inclusion of active substances and the authorization
of plant protection products by member states. An extensive dossier is
submitted by a company. It contains all the relevant information on the active
substance and at least one representative product. It is submitted to a
Rapporteur Member State selected by the company. The pesticide authority
in that member state carries out a risk assessment and distributes the Draft
Assessment Report (DAR) with a recommendation to the applicant and the
other member states. In practice, a signicant degree of variation became
apparent between review practices among individual Rapporteur Member
States. This problem had to be corrected by the development and adoption of
a series of guidance documents (European Commission, 2001: 5).
Since 2002 the EFSA has been responsible for risk assessment which it
carries out through a scientic peer review by EFSA scientists and experts
from the member states. This leads to the production of a guidance docu-
ment which goes to the Working Group (legislation) of the European
Commissions Standing Committee on the Food Chain and Animal Health.
Member state civil servants decide whether to approve the active substance
and, if successful, it would be added to Annex 1 of Directive 91/414. Product
authorizations are considered at a national level using harmonized criteria
for data requirements laid down in EU legislation (94/89/EC, Mammalian
toxicology, including human exposure; 96/68/EC, Residues, including con-
sumer exposure; 94/37/EC, Physical/chemical properties; 95/36/EC, Fate
and behaviour; 96/12/EC, Ecotoxicology; 93/71/EEC, Efcacy). However,
as one respondent commented, You have data requirements, member states
can interpret them how you wish. It should be noted that while microbials
have a specic and uniform set of data requirements at EU level, there has
160 Chapter 5
been no specic set of data requirements for plant extracts, pheromones and
semiochemicals. Chemical data requirements have been used, but cases
could be made for not presenting part of the data.
Loss of active substances through the EU review programme
Many older substances are being removed from the market under the 91/414
review programme, either because they fail to meet the standards of the
review or because companies decide for commercial reasons not to support
them, which could include a consideration of the costs of re-registration. The
MRL programme is likely to reduce the range of available uses. The EU
review programme is having a signicant impact on the availability of crop
protection products. In some cases, there are no effective chemical solutions,
as exemplied by the loss of all products for the control of root y on swedes
and turnips in the UK (Richardson, 2005: 237). This does, of course, provide
a new opportunity for biopesticides, but biological substitutes are not avail-
able for all the withdrawn products and, if they are, may be less efcacious.
The pesticide review was a protracted process and a new developed
database nally came on stream in March 2009. About 1000 active substances
on the market before 1993 were subjected to a detailed risk evaluation in
terms of their effects on human health and the environment. Two hundred
and fty achieved the harmonized EU safety assessment and 70 substances
failed it and were removed from the market. The others were eliminated as
dossiers either were not submitted or were withdrawn by industry.
Shortcomings in the EU system of registration
The length of time it takes to complete registrations is a major consideration
for SMEs as they wish to generate a cash ow as soon as possible and start to
recoup the costs of research and development. The industry complains that
the current registration period for [microbial biological control agents] in the
EU is costly and time-consuming. Long registration periods are a severe
problem, because they delay the onset of the returns for the investments
made during research and development (REBECA, 2008: 19). Seven exam-
ples of biological control agents considered by the REBECA project showed
that the time period from the month of dossier submission to the month of
inclusion on Annex 1 or granting of national registration was a mean of 87.7
months with a range of 57121 months (REBECA, 2008: 19). The mean time
for registration in the EU was 75 months compared with 28 months in the
USA (Hokkanen and Menzler-Hokkanen, 2008). There was also considerable
variation in reported registration times between member states. Britain and
Germany were regarded by our respondents as having relatively efcient
registration agencies. A number of complaints were made about Spain,
one respondent commenting, waiting two years from submission, such a
backlog of products.
In an internal market, one would hope that once a product was approved
in one member state, it could then easily be registered in other member states.
As one manufacturer commented, Hopefully, once done a registration in
one country, just a rollout to other European countries. Everyone is looking
for mutual recognition routes. Have a lot of trouble with mutual recognition.
The Commission accepts that Mutual recognition does not function well and
national authorisations of products leads to duplication of work in Member
States and to differences in the availability of plant protection products across
the European Union (European Commission, 2005).
Some of these problems have arisen because of the existence of 27 regula-
tory authorities across the EU with varying and often inadequate levels of
resources available to them and following their own particular procedures.
Some member states are uneasy about the principle of mutual recognition. A
Danish Environmental Protection Agency (EPA) ofcial commented in inter-
view: Mutual recognition would seek to undermine standards. We really feel
that. The slowness of getting Annex 1 listings has also been a factor and the
drive to speed things up led to substances being approved for single rather
than multiple uses. A more underlying tension is, as one respondent put it,
Regulators united in commitment to carrying on regulation on a member
state basis, policy makers likely to favour a more harmonised approach.
To some extent, regulators have been developing their own informal
links, both through EU and OECD committees and on a bilateral basis.
One participant in the EU expert meetings noted that Belgium, Denmark,
Germany, the Netherlands, Sweden and the UK were regular in attendance
with France and Hungary coming occasionally. These links can be used as a
basis for information exchange and have led to work sharing of the Rappor-
teur role. A PSD ofcial commented, Try to get an air of pragmatism, work
sharing, where we can support each other, where we can support each other
to cut down on data requirements. We used to know frighteningly little about
how others did efcacy. PSD sees itself as trying to push pragmatism into
Europe. [We are] trying to push pragmatism into other member states.
One available mechanism for harmonization is to make use of the
EPPO. Founded in 1951, EPPO is an intergovernmental organization with
50 members and a secretariat of 12 based in Paris, funded by contributions
from the member governments. In the plant protection area, EPPO has
developed a number of standards for use by national registration authori-
ties. PSD has taken certain UK procedures and has turned them into EPPO
ones, particularly in the efcacy area, for example trials guidelines and
minimum effective dose. One respondent suggested that EPPO had more
effective dissemination mechanisms than the EU.
Although the EU is supposedly an internal market, it is geographically
diverse and pesticides that work in one set of climate conditions will not
necessarily work in another or at least not as well. A proposed solution has
been to devise climatic zones in which mutual recognition could occur. This
idea originated with a paper by the UK Crop Protection Association that out-
lined a northern European region with a climate comparable to the UK. This
paper was accepted by the ACP and provided an opportunity for companies
162 Chapter 5
to use northern European data in regulatory submissions without the need
to provide for each trial a specic justication that climate conditions were
relevant to the UK (Richardson, 2005: 235). More generally, The climate
within a zone can be considered comparable for the purposes of effectiveness
data, and should aid the acceptance of efcacy data between countries within
a zone (Richardson, 2005: 235). However, as will be evident from the fol-
lowing discussion of EU reform proposals, zoning met with considerable
political resistance and many problems connected with its implementation
have to be resolved.
The reform of the EU regulatory system
This revolves around three main proposals: the amendment of Directive
91/414; the EU Thematic Strategy; and the Sustainable Use Directive, but also
discusses the Water Framework Directive. In this section the main elements of
each proposal are considered and then their progress through the co-decision
process of the EU. There is also a draft regulation on the collection of data on
pesticides sale and use, but that is not considered further here.
The amendment of Directive 91/414
A steer for the revision of the directive was provided by the 2001 report to the
Parliament and the Council on how the directive was working. It was admit-
ted that Decision-making was slow between 1993, when the Directive
entered into force, and 1999 An already complex piece of legislation
became progressively more complex in application as expectations mounted
on all sides, ensuring that standards and criteria were not only maintained at
a high level but were effectively raised (European Commission, 2001: 8). It
took another 5 years for the Commission to produce a set of proposals for
amendment. Part of the reason for the delay was no doubt the extensive
consultations held with a range of stakeholders, including the IBMA. The
other principal stakeholder groups consulted were: agriculture and food
organizations, six; agrochemical and chemical organizations, four; environ-
mental organizations, four; animal welfare organizations, two; retailers, one;
consumers, one. This gives the indication of the range of conicting interests
involved and helps to explain why it was so difcult to get the proposals
through the Parliament. Despite the time taken in the preparation of the
proposal, one regulator commented, It is not the best thought out proposal.
Born of frustration that mutual recognition has not taken off.
A central consideration for the Commission was that The large difference
in authorisation of existing active substances shows that without further har-
monisation the protection levels in Member States may vary a lot (European
Commission, 2006a: 9). The whole approach of the document was informed
by the application of the precautionary principle to ensure that industry
demonstrates that substances or products produced or placed on the market
do not adversely affect human health or the environment (European
Commission, 2006a: 14). The document also endorsed the principle of IPM,
but recognized that it would require a transition period of unspecied length
before it could be applied, although the accompanying Thematic Strategy
targeted 2014.
The main proposals included provisions to encourage a move from national
to zonal-level authorizations with obligatory mutual recognition between
member states of the same zone. This solution to the mutual recognition prob-
lem had proved particularly controversial during the stakeholder consultations
and continued to be so subsequently. Some stakeholders opposed any further
harmonization, while others favoured full centralization. The proposed
system is a compromise between the current situation and a fully centralised
authorisation (European Commission, 2006a: 7). Like many compromises, it
pleased relatively few with only Austria and the UK being clear supporters
among the member states with France and Germany opposed. One consider-
ation was that states with national testing systems, such as France, did not
want the job losses associated with greater centralization.
A key plank of the proposals was risk-based comparative assessment and
substitution to encourage the replacement of more hazardous substances
and/or products with alternatives. This was good news for advocates of
biopesticides, and has been called for by the IBMA in its 2005 white paper on
the regulation of biologicals, but the inuential ECPA was opposed in princi-
ple to regulatory substitution at any level. Farmer organizations were also
opposed because they were concerned about the reduced availability of prod-
ucts. Hazard triggers would be used to exclude from Annex 1 carcinogens,
mutagens or reproductive toxins.
The Commission proposed bringing to an end the system whereby
member states could grant provisional national authorizations for new active
substances pending a decision on Annex 1 listing. This was thought to pro-
vide a welcome element of exibility in the system, but the Commissions
view was that it was incompatible with a harmonized system for establishing
MRLs and would be offset by strict deadlines for assessing an active sub-
stance. Whether deadlines such as completing the DAR within 12 months of
notication of the completeness check are achievable is another matter.
Resource constraints and the availability of specialized personnel have been
a continuing constraint for the European pesticides regulation regime.
The Thematic Strategy for Pesticides and the Sustainable Uses Directive
This arose from the 6th Environmental Action Programme, which called for
a reduction in the impact of pesticides on human health and the environment
and the need to achieve a more sustainable use of pesticides. However, the
strategy document acknowledged that The potential risks associated with
their use are accepted to a certain extent by society given the related economic
benets since inter alia plant protection products contribute to ensuring
supplies of affordable and healthy agricultural products of high quality
(European Commission, 2006b: 3). The Commission noted with concern that
Despite the increasing costs involved in [the registration] process and the
decreasing number of active substances on the market, actual consumption
and use of pesticides in the EU have not decreased in the last ten years. At the
164 Chapter 5
same time, the percentage of food and feed samples where residues of pesti-
cides exceed maximum regulatory limits is not declining, but remains around
5% (European Commission, 2006c: 3). As with the proposal to amend Directive
91/414, the Commission expressed its concern about policy variability
between member states, which in their view required harmonizing action
at EU level: Over the last fteen years, signicant but uneven changes in
pesticide use have been observed amongst Member States. Whilst pesticide
use declines in some Member States, a sharp increase has been observed in
others (European Commission, 2006c: 3).
The Commission declared its support for forms of agriculture that
restricted or better targeted the use of plant protection products, such as
organic farming, integrated pest management or the use of less susceptible
varieties (European Commission, 2006b: 6). No mention is made of biopest-
icides, reecting their low prole at EU level. This is evident in internal
SANCO documents which examine extensively the reaction of the ECPA to
proposals, but make no mention of the IBMA. During the debates in the
Parliament, lobbying efforts by the IBMA raised the prole of biological
solutions, but the toehold they obtained in the legislation was subsequently
removed.
The preparation of the Thematic Strategy identied the need for a Sustain-
able Use Directive as several of the envisaged measures could not be integrated
into existing legislation or policies. This directive was passed in 2009 and will
be implemented by 2011. It was centred around the creation of National Action
Plans to identify areas of risk, the reduction of risk and use, the minimization
of impacts on human health and environment, responsible use and IPM. It
would set up systems of training for distributors and users, require member
states to set up systems for inspection of application equipment, and prohibit
aerial spraying.
The battle in the Parliament
In its plenary vote in November 2007, the Parliament substantially toughened
up the proposals put forward by the Commission. As they stood, the Com-
mission proposals on active substance approval criteria would remove the
main control for major diseases of wheat in the UK with potential yield losses
of 2030% and would have signicant implications for crops such as carrots,
parsnips and onions because the majority of approved herbicides might no
longer be available. The Parliament proposals would mean effectively no
herbicide options for control of weeds in horticultural crops; chemical con-
trol of black-grass in cereals would become virtually impossible with severe
economic impacts potatoes seed potato growing unlikely; ware potato
yields severely reduced many horticultural crops would be uneconomic to
grow (PSD, 2008b: 1112).
The discussion of the Parliamentary debate focuses on two proposals
that are particularly relevant to biopesticides: the zoning scheme and an
amendment proposing distinct regulatory arrangements for biopesticides.
The scheme to divide the EU into northern, southern and central zones
for mutual recognition purposes had attracted opposition as soon as it was
proposed. There were concerns that the proposed zones did not represent
homogeneous regions in terms of climate, pests or agricultural production
and practices, although truly homogeneous zones would be difcult to
devise. Hungary in particular pressed for a fourth zone which would pre-
sumably cover Eastern Europe. There was concern that products might be
withdrawn from the market unnecessarily because of a conservative assess-
ment by one member state. Denmark, which takes a relatively rigorous stance
on pesticide regulation, expressed concern that a plant protection product
approved in one Member State could have a highly adverse effect in other
Member States of the same zone (Anon., 2007). From a different perspective,
an industry spokesman commented that Introducing a zonal system often
takes away national exibility, instead of a lowest common denominator
system which is often talked about in Europe, going to end up with potential
for highest common denominator in granting an authorisation. Any member
state that has an issue with something imposes that condition.
It was always possible to criticize the arbitrary nature of the zones,
particularly given that it was not politically feasible to divide countries as
might have been climatically sensible for northern and southern France.
German Rapporteur Christa Klass complained that the scheme would lead
to the introduction of a zoning line which would, for example, place the
right and left banks of the Mosel in different legal areas. She therefore
suggested that instead of arbitrary zones, that the principle of mutual recog-
nition of national licensing should be retained, but that the Member States
should, in the spirit of the subsidiarity principle, be allowed to make national
or regional specications (European Parliament, 2007: 132). In other words,
there would be a completely discretionary system in which member states
could opt to make a regional ruling, although it is unclear how other member
states might then respond. The European Parliament subsequently rejected
the zonal authorization system and the linked compulsory recognition of
authorization within a zone. The Commission rebuffed this rejection: The
amendments have not been accepted as they would have considerably
undermined the Commission proposal and would have removed one of its
key elements (European Commission, 2008: 7). However, in an effort to reach
agreement the Commission put forward a compromise in the form of excep-
tional derogations in a bid to render the authorisation process more relevant
to realities on the ground such as climate conditions, soil types, crops
cultivated etc. (Anon., 2008).
The plant protection regulation created northern, central and southern
zones and a single zone for greenhouses, seed and post-treatments, empty
rooms and containers. Initial authorization will be undertaken by a member
state in the same zone, but application can be made in any member state for
greenhouses. In general the application is examined by the member state
proposed by the applicant. Other member states in the zone would normally
recognize the authorization decision, but if they have human or animal health
or environmental concerns, and there are no risk mitigation measures, they
can refuse to authorize. How mutual recognition will work in practice
remains to be seen. The whole procedure for the inclusion of an active
166 Chapter 5
substance should take 30 months, plus 15 additional months if additional
time periods and clock stops are used.
Rapporteur Christa Klass proposed a specic system of regulation for
biopesticides. In order to meet substitution objectives, the licensing of natural
biological control products such as micro-organisms and viral and pheromone
products should be facilitated. When the relevant research projects have been
completed, these substances should not fall within the scope of this regula-
tion, but be specically regulated (European Parliament, 2007: 132). In
Amendment 35, the European Parliament inserted language giving priority to
non-chemical alternatives for plant protection. The Commission deleted this
amendment, justifying its rejection in the following terms:
Amendment 35 aims to introduce a future limitation to the scope excluding
micro-organisms, viruses, pheromones and biological products once a specic
regulation related to these products will be adopted. The Commission retains
that there is no need for a specic regulation as specic data requirements and
criteria for authorisation are already in place and for some of these substances
the provisions concerning low risk substances could apply.
(European Commission, 2008: 5)
The new legislation does give a specic status to non-chemical and natural
alternatives and requires them to be given priority wherever possible. The
denition of non-chemical methods mentions in Article 3(8) physical,
mechanical or biological pest control. Biological controls should generally
qualify as low-risk active substances in Annex II, Section 5. They should
certainly satisfy the exclusion criteria in that they are not carcinogenic,
mutagenic, toxic to reproduction, toxic or very toxic, nor are they sensitiz-
ing chemicals, explosive, corrosive or deemed to be endocrine disruptors.
Problems may be caused by the requirement that they are not persistent in
the sense that their half-life in the soil is less than 60 days. This provision
will almost certainly require a guidance document as provided for in Arti-
cle 77 which permits the Commission to adopt or amend technical and
other guidance documents concerning micro-organisms, pheromones
and biological products, for the implementation of this regulation. EFSA
would normally undertake this work, but its schedule is full for 2010 and
probably for 2011 (Heilig, 2009).
Being classied as a low-risk active substance gives initial approval for
15 years rather than the standard 10 years. A fast track decision on authoriza-
tion should be taken within 120 days providing no data are missing. A
reduced dossier can be submitted for plant protection products containing
them, but this has to include a demonstration of sufcient efcacy. The prod-
ucts may be advertised as Authorised as low-risk PPP, but paradoxically no
such claim can be made on the label. It should also be noted that the nal
categorization of low-risk substances will depend on EFSA peer review.
The new European legislation does not give biological controls all they
might have hoped for, but it does give them legislative recognition and
opens up the potential for faster authorization processes and effective
mutual recognition.
The Water Framework Directive
The implementation of water quality legislation in the form of the Water
Framework Directive could also have important implications for the
availability of active substances which could go beyond those anticipated as
the result of the revision of 91/414. If certain pesticides were found to be
continually damaging water quality, they could be withdrawn. The active
substances that are most likely to be affected are those used on a large area
and/or at high rates. This is typical of herbicides used on combinable crops
where ten herbicides are causing some concern, in particular those used for
the control of grass weeds in oilseed rape. Many insecticides could also be at
risk, making options for control of some pesticides very limited. Metalde-
hyde is particularly at risk as it is being found in water and this could lead to
difculties in slug control.
Denmark: regulatory stringency
Scandinavian regulatory standards are widely believed to be stricter, less
favourably disposed to pesticide usage, than is the case in countries like
the UK and parts of Southern Europe (Blok et al., 2006: 313). In particular,
Denmark is seen by most experts, including the NGO respondent, as possess-
ing comparatively restrictive regulations, as opposed to countries such as
Italy where south of Rome normal rules do not apply (Blok et al., 2006: 319).
This was conrmed in interview by a Danish EPA ofcial, who stated: There
are some areas where we are more strict than other member states. For most
effects we use a high safety factor. Apart from a general green orientation, a
major specic driver for this stance is that Contrary to most other European
countries, Danish water supply companies use groundwater reserves for
drinking water, with no or minimal forms of prior purication (Blok et al.,
2006: 314). Denmark may, however, be less of a regulatory leader on pesticides
than it was. Following a change to a more conservative government in 2001,
concerns are raised that the content and style of environmental policy mak-
ing may be changing (Blok et al., 2006: 315). In particular, the Danish EPA
used to be populated by environmentally committed staff unwilling to
approve pesticides (Blok et al., 2006: 317), but this is no longer the case.
Denmark is particularly noted for its use of a pesticide tax, with Norway
being the only other European country to use such a policy instrument, In
1986 the Danish parliament approved a pesticide action that required a 50%
reduction in the use of pesticides by 1997. Use decreased less than had been
hoped for and in 1995 a tax was imposed equal to 37 per cent of the retail
price on insecticides and 15 per cent on fungicides, herbicides and crop-
regulating chemicals (Daugbjerg and Pedersen, 2004: 225). In 1998 the tax
was doubled but the government had to back down in the face of pressure
from agricultural interests and lower land taxes to compensate. In Denmark
[t]he combined sale/consumption of plant protection agents to/in agricul-
ture has fallen from 6,972 tonnes of active substance in 19811985 to 2,889
tonnes in 2000 The experience gained from pesticides taxation shows that
the tax in conjunction with a range of other measures does have an effect
(Larsen, 2004: 18). However, it should be noted that these gures take no
168 Chapter 5
account of the toxicity of active ingredients. In Britain the New Labour
government considered the use of a pesticide tax after it came into ofce in
1997 but decided to rely on the Voluntary Initiative to minimize the impact of
pesticides on the environment and on water quality in particular.
Does the Danish approach facilitate the wider use of biological controls?
The Bichel Committee, which was set up by the Danish Government in 1997
to provide an overview of the use of pesticides, devoted less than a page to
biological control and adopted a somewhat sceptical tone:
The utilisation of useful organisms and microbiological methods would
present a signicant risk of proliferation of alien organisms, which could
have a detrimental effect on the environment. Theoretically speaking, the
proliferation of local species could also disturb natural ecological balances.
The use of microbiological methods entails a risk of industrial injuries, in the
form of allergies or industrial diseases.
(Bichel Committee, 1998: 73)
Biopesticides are subject to the pesticides tax, but at a lower rate of 3%.
However, as there are no fees for authorizations and applications, the low tax
is intended to cover administrative costs instead of a fee. If Denmark is a
Rapporteur Member State and has to do an EU evaluation, a charge of
?100,000 is made for microbials compared with ?210,000 for chemicals.
Research is funded from the pesticides tax and, as far as is possible given the
quality of the applications received, one microbial project is funded each
year. For a time, the Danish EPA lacked an expert to deal with biological con-
trols: [The] person responsible stopped work at EPA and [products] were
put on the shelf for many years. Then another person came and not much
happened, then I got the job. This does not suggest a very high priority for
biological controls. The emphasis of Danish policy seems to have been on
reducing pesticide use rather than promoting alternatives.
The Netherlands: regulatory innovation
Denmark does not have a large protected crops sector, but its importance in
the Netherlands has created a favourable environment for the promotion of
biopesticides. Dutch Government policy is concerned with reduction of use,
but also covers the stimulation of the use of natural products. Dutch law has a
provision for products with a low toxicity prole (regulation exempted pesti-
cides, RUB). Genoeg is a series of schemes which have attracted nancial and
political support from the Ministry of Agriculture. Genoeg is the acronym for
Gwasbeschermingsmiddelen van Natuurlikje Oorsprong Effectief Gebruiken,
which translates as using plant protection products of natural origin more
effectively (or, more colloquially, the effective use of natural pesticides). It is
a functional equivalent of the UK Biopesticides Scheme, although in the
Netherlands companies receive a subsidy from public funds while in the UK
fees are lowered. In the Netherlands, the process was a more bottom-up one
than in the UK with a coalition of actors creating a new process.
The rst phase of the project from 2001 to 2002 was an exploratory one
concerned in particular with the development of an inventory of effective
natural pesticides. After a phase of issue management concerned with the
dissemination of knowledge to growers, Project Genoeg Toegelaten ran from
2003 to 2005 and was concerned with the support of ve natural pesticides
for use in glasshouses. One product approved through the Genoeg scheme
was not approved in the UK by PSD. From 2004 to 2008, Project Genoeg
Breed focused on the support of ten natural pesticides for all uses. In 2008,
seven agreements for support were in place involving the co-nancing of 13
new products.
The project is managed by a consultancy called the Centre for Agriculture
and Environment (CLM), which has extensive experience in sustainable
agriculture. It was started to serve as an intermediary between farmers and
environmentalists and has good links with all stakeholders, cemented by reg-
ular meetings. The consensus and coalition building has been a key element
in the success of the project. In selecting products for support, an emphasis is
placed on products that have a low toxicity prole and where data on efcacy
and toxicity are available. Products are ones where successful authorization is
expected and where the company will defend the product.
Fifty per cent of the costs of research and registration are co-nanced to
a maximum of ?100,000. Help is provided in literature search for registration
by a body that has expertise in technical questions about ecotoxicology, the
National Institute for Public Health and the Environment (RIVM). The regu-
latory body, the Board for the Authorization of Pesticides (CTB), provided a
help desk facility to assist applicants and established a biopesticides team
made up of six staff members each with a dened expertise or speciality such
as characterization or residues.
There have been some problems with companies dropping out during the
process. For many applicants, the cost of registration remained a problem with
?400,000 being identied as a typical cost for the whole process. As in the UK,
a key lesson has been the importance of meetings with applicants early in the
application process to identify areas of difculty and possible solutions.
The USA: Promoting Biopesticides
The USA has an impressive record in promoting the registration of bio-
pesticides. Since current data requirements were published in 1984, nearly 80
microbial pesticides have been registered: 39 bacteria; 29 fungi; seven bacu-
loviruses; two yeasts; and one protozoon. The success of the US EPAs efforts
to give priority to the evaluation of reduced-risk pesticides is illustrated
by the fact that in 2004, of the 26 new active ingredients registered, over
half (14) were biologicals and ve were reduced-risk conventional pesticides
(Lindsay, 2005: 341). The EPA has always had a traditional pesticide regula-
tory process, which is data rich and resource intensive but is seeking to move
from data heavy to data smart (Lindsay, 2005: 343). In particular, [w]hat is
needed is a shift from a paradigm where extensive hazard testing is con-
ducted, and information that is not relevant is eliminated, to one where a
risk-based, hypothesis driven approach identies the information most
170 Chapter 5
relevant to the assessment (Lindsay, 2005: 345). The effort to promote bio-
pesticides in particular depended on a few committed individuals: Fifteen
years ago nobody paid us any attention. What changed this indifference was
that [t]here were staff who were really interested, senior leadership at a
political level within the Agency. Upper management tell us, spread the
technology, get it out there. Like the PSD, EPA provides pre-submission
meetings which discuss how to satisfy data requirements.
Direct comparisons between the USA and the EU are inhibited by the
fact that regulation in the USA is largely undertaken at the federal level,
whereas the EU has a complicated division of responsibilities between the
European institutions and the member states. Pesticide labelling is entirely a
federal matter in the USA, but as conrmed by a 1991 US Supreme Court
judgment, Wisconsin Public Intervenor v. Ralph Mortier, federal pesticide law
does not pre-empt local regulations dealing with the use of pesticides. A state
can refuse to register a product and hence the sale and use of any pesticide.
The two most active states in the area of pesticides regulation, both of which
have large fruit and vegetable sectors, have been California through its
Department of Pesticide Regulation and Florida through the Florida Pesticide
Law. California claims to have the nations toughest pesticide laws and the
largest and best-trained enforcement organization, with about 350 state
inspectors compared with about 45 in Florida. The state has been particularly
active in the encouragement of IPM. Unlike the federal regulator, California
does require efcacy data, although there are exemptions if it has previously
approved products containing the same active ingredient. At the federal
level, applicants for registration are required to have efcacy data available,
but they are not usually called in.
Nevertheless, the main impetus comes from the federal level. The EPA has
a dedicated Biopesticides and Pollution Prevention Division, which is the small-
est division in the Agency and in a different location, both factors that may
have contributed to the proactive philosophy and committed culture observed
when the Division was visited as part of the research. The Division head
commented in interview: We believe strongly that theres a role to create a
division just dedicated to [biopesticides]. Another staff member commented:
We do things differently from the rest of the ofce; we have a one-stop shop,
dont farm out anything on economic or ecological efcacy or health effects.
We have our own chemists, economists, toxicologists; cuts down on amount of
bureaucracy, helps us to implement things. Have all personnel in one division,
on [the] same oor, much easier if [the] person is sitting in [a] cubicle across
[the] oor.
This point was reinforced by the observation that legal experts from the ofce
of general counsel visited just once a week: Thats where the biggest friction
is, would be easier if full-time; does help familiarity.
EPA staff members attach considerable value to the Interregional Research
Project (IR-4) programme, which operates as a partnership between the United
States Department of Agriculture (USDA) and the land grant universities.
This was started in 1963 and remains focused on minor crops rather than
biopesticides, but started a Biopesticides Program in 1982. The programme
was expanded in 1994 to provide competitive grant funding to support stud-
ies on early development stage biopesticides for minor crop uses (Holm et al.,
2005a: 241). IR-4 helps biopesticide registrants with regulatory advice and the
preparation of applications for approval. It also developed organizational
capacity by supporting the growth of the Biopesticides Industry Alliance
(BPIA) as a trade association of biopesticide companies. Biopesticides divi-
sion staff work closely with IR-4 and it was noted in interview: As a govern-
ment agency were prevented from promoting a product or technology.
Comparing the European and US systems, a consultant commented:
The US system, in terms of data requirements is not less onerous but more
accessible to applicants because of the biopesticides sub-unit of EPA, provides
list of data requirements. Regulators in Europe were a little more sceptical
about the American arrangements. One biological product examined by PSD
turned out to have a human pathogen in the formulation, although the prod-
uct had been approved in the USA. A regulator commented: Reduced risk
means all things to all men in EPA. Difcult to identify from legislation what
is reduced risk.
In terms of the number of products registered, the US system has been
more successful than that in Europe. This may not be just due to differences
in the regulatory arrangements, but also to the existence of a large internal
market covering a variety of climatic zones that allows development costs to
be recouped relatively rapidly. The fact that the European market is frag-
mented by regulatory barriers is a reection of shortcomings in the realiza-
tion of the European project.
International Harmonization: the Role of OECD and WHO
It has been argued that the development of harmonized guidelines and
terminology by the OECD is critical to the advancement of work sharing on
the international level (Holm et al., 2005b: 31). The Biopesticides Steering
Group of OECD, which was established in 1999, provides an important
forum for regulators and industry to meet and work together. Working
together enables a speedier and more thorough evaluation of a biopesticides
risk, thus (it is hoped) speeding up the process of approving safer pesticides.
The OECD work has focused on writing guidance for the submission and
evaluation of test data. The agreed guidelines establish two formats, one for
industry to use when submitting dossiers and one for regulators to use when
writing their evaluation reports. The OECD guidance is intended to ensure
that dossiers and evaluation reports are clear and complete, and that
information is easy to nd. This makes it easier for governments to use each
others pesticide risk evaluations, overcoming potential non-tariff barriers.
The practical value of the guidance is shown by the fact that they were used
in relation to pheromones in the pilot scheme. One manufacturer noted that
the OECD guidelines were in some respects more arduous than what is
required by some national regulatory agencies.
172 Chapter 5
Not all countries are active participants, with Japan reportedly having
never attended. There was a feeling in Europe that the US try to keep much
of their own system rather than compromising. This was echoed by an EPA
respondent who commented: I think we can harmonise with Canada, but I
am not sure about all the other countries of the world. The North American
Free Trade Agreement (NAFTA) has a Technical Working Group on biopesti-
cides and agencies in Canada, Mexico and the USA undertake joint reviews
using OECD guidelines.
The WHO has had a Pesticide Evaluation Scheme (WHOPES) since 1960
that promotes and coordinates the testing and evaluation of pesticides for
public health. This covers the safety, efcacy and operational acceptability of
pesticides and develops specications for quality control and international
trade. In 2001 the FAO and the WHO agreed to develop joint specications
for pesticides.
Design Principles for a Better Regulatory System for Biopesticides
As part of our research, we sought to develop a set of design principles for a
better regulatory system for biopesticides. Our hope was that these principles
could inform future policy debates and assist the coherence of regulatory
proposals. We developed ve underlying principles.
1. Biopesticides have a key but specic role to play in crop protection.
Synthetic chemical pesticides are a precious resource for crop protection
and should be treated as such, but problems of resistance and the withdrawal
of some products mean that fewer chemical pesticides are available on the
market. Alternative crop protection tools are needed and biopesticides have
an important and increasing role to play in crop protection, although nor-
mally in combination with other tools including chemical pesticides as
part of IPM.
2. Biopesticides should be regulated. Just because something is natural
does not mean that it is safe. However, the regulatory system has tended
to follow a chemical pesticide model that does not facilitate the efcient
registration of biopesticides.
3. The regulatory system must support sustainability objectives. It should be
informed by a proper understanding of the precautionary principle. While there
should be a special emphasis on environmental sustainability, other aspects of
sustainability including economic sustainability should be taken into account.
4. Pest management should be ecologically based. It should make use of
natural enemies of pests and be undertaken within the context of Integrated
Crop Management (ICM) and IPM. Biopesticides offer benets to both con-
ventional and organic farming, providing an aspect of unity where there is
otherwise division.
5. It should be credible with all stakeholder groups including consumers. It
is particularly important that the regulatory system has the condence of
consumers in relation to human health issues.
Operational principles
There needs to be an improved knowledge basis and chain. There still needs
to be better understanding of the ecology of microbial control agents, the fate
and behaviour of microbial releases, and of the effects of secondary metabo-
lites/toxins produced by microorganisms, a minority of which could have
consequences for human health.
Stakeholders need to be fully involved in the debate on regulation and its
implementation and to have effective communication links with each other.
As is discussed further in Chapter 6, the biopesticides policy network is
weakly developed and sometimes politically unsophisticated. A key problem
is the lack of an inuential constituency of support for biopesticides, particu-
larly in environmental terms with the debate about a more sustainable
agriculture being framed around discourses about organic farming. The role
of retailers in imposing additional requirements on growers poses a number
of challenges that are discussed more fully in Chapter 7.
There needs to be a biopesticides champion organization, preferably
quasi-governmental in character, which can act as an advocate for biopesti-
cides. In the USA this role is to some extent performed by the biopesticides
division of the EPA, but the American model cannot simply be transferred to
Britain. Such a role would be compatible with the broad task and objectives
of Natural England in the UK, but it is not a role that it is ready to adopt.
Nevertheless, without an organizational champion with a clear advocacy
role, the case for biopesticides risks being sidelined.
Whether the organizational absorption of PSD within HSE will be
benecial remains to be seen, but it is important that the York location is
maintained to avoid the loss of experienced staff and consequent disruption
to the biopesticides programme. PSD has led the eld in Europe in biopesti-
cides regulation through the Biopesticides Scheme. The existing staff net-
work dealing with biopesticides within CRD should continue to be supported
and developed in terms of enhanced coordination and training, a clear group
identity and strong organizational support. ACP needs more knowledge
on biopesticides in general and the biology of microbial control agents in
particular. This could be achieved by creating a network of experts with
appropriate specialisms.
Although regulators in Europe support efcacy testing, views within
industry tend to be somewhat divided. It is in any case necessary for market-
ing claims and it protects users against deceptive claims from snake oil pro-
ducers who can damage the reputation of an emergent industry. There may
be scope for varying some of the requirements imposed in efcacy testing
and hence reducing the cost. These issues are being considered by the OECD
Biopesticides Steering Group. Consideration should be given to the ndings
of the EU-funded Efcacy Extrapolation Project carried out by PSD. A report
was made which presents proposals for harmonizing efcacy and crop safety
extrapolations with the aim of reducing the need for trial data while main-
taining high standards of performance and selectivity. A key area for review
is the number of tests required over what time period.
174 Chapter 5
A number of important developments are taking place at the EU level.
The role of the EFSA is still evolving, but concerns have been expressed that
its application of the rules may be too inexible and more data will be
requested for a risk assessment than are absolutely necessary. A key require-
ment is to ensure that mutual recognition works effectively between member
states. This would create a larger market for biopesticides and overcome
some of the economies of scale problems that manufacturers face. The eco-
zone proposal has attracted some criticism, but other than the further devel-
opment of cooperation between national registration agencies, it represents
the most feasible way forward.
Considerable sums of public money have been spent on the development
of biocontrol products which have not then been registered or marketed.
SMEs have encountered considerable difculties with the cost of the registra-
tion process, not just the registration fee, but the cost of development and
testing. Data collated by David Richardson about government direct or indi-
rect funding across 14 European states show that only three member states
provide no funding: Estonia, Slovenia and the UK (Denmark offsets fees
against the pesticides tax). Six countries, including France and Germany,
provide funding for trials. Such assistance may be seen as too near market
in the UK, which tends to follow a relatively rigorous denition of market
failure, whereas the USA is more inclined to support new technologies seen
as serving the national interest. There is a market failure to be addressed in
terms of the positive social and environmental externalities of biopesticides
not being realized.
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6
Policy Networks, Change
and Innovation
1
Scientic research can identify sustainable benets from biopesticides.
However, the regulatory system may not function in a way that allows the
potential benets for the rural economy, e.g. the consistent supply of quality
food more acceptable to customers, to be secured. As Chapter 5 has shown,
biopesticide development was (until recently) locked into an inexible and
unimaginative chemical pesticide model. The system of regulation was
preventing social benets from being captured. Given, however, that existing
actors in the policy network are primarily oriented to chemical solutions to
pest infestation problems, how has change been brought about? Policy net-
work theory points to policy networks being good at managing incremental
change, but tending only to innovate in conditions of crisis or exogenous
shock. A complicating factor is the role of the EU in pesticide legislation. Its
system of decision making and in-built checks and balances is not designed
for rapid policy change or paradigm shifts.
This chapter considers policy actors in biopesticides and pressures for
change in terms of a policy network perspective. It analyses the small size of
the policy network and its relative lack of political sophistication and focuses
on the notion of regulatory innovation. In other words, given that regulators
are risk averse, under what conditions can regulatory innovation occur? It
builds on Blacks framework (2005) to provide an assessment of the relative
importance of endogenous and exogenous pressures for change. Our particu-
lar focus is on regulatory innovation within CRD in the area of biopesticides.
By using the insights of policy network theory and interviews with key actors
we can identify the change agents and processes that have created a momen-
tum towards regulatory innovation. The question is whether environmentally
friendly scientic and technological innovations in pest control on food crops
can be matched by appropriate regulatory regimes that meet concerns about
public safety and environmental impact, but do not unduly constrain develop-
ments that help the achievement of sustainability goals for the rural economy.
178 Chapter 6
Policy Network Analysis
Richardson and Jordan (1979) explained the way in which policy making
in Britain was disaggregated into a number of subsystems giving pressure
groups ample opportunities to inuence policies of concern to them. They
argued that the policy-making map was made up of a series of distinct
vertical compartments and these tended to be organized around a govern-
ment department and its client groups, largely closed off from the general
public. They deliberately chose the term community to reect the intimate
relationship between groups and departments.
The term policy network has largely displaced that of policy community
in the literature. Indeed, policy network analysis has become the dominant
paradigm for the study of the policy-making process in British political
science (Dowding, 1995: 136). Relatively few networks have the internal sta-
bility and insulation from other networks typical of policy communities
(Grant, 2000: 49). Richardsons work, moreover, suggests a shift in emphasis
from a policy-making world of tightly knit policy communities to a policy
process more loosely organized and hence less predictable. One can distin-
guish between ve types of network ranging along a continuum from highly
integrated policy communities to loosely integrated issue networks (Rhodes
and Marsh, 1992: 13). At one end of the spectrum is the policy community,
which is based around stability of relationships, a highly restricted member-
ship, vertical interdependence based on shared service delivery responsibility
and insulation from other networks and, usually, the general public (including
Parliament) (Rhodes and Marsh, 1992: 13). At the other end of the continuum,
issue networks have a large number of members with a limited degree of
independence. Stability and continuity are at a premium, and the structure
tends to be atomistic (Rhodes and Marsh, 1992: 14). The Rhodes and Marsh
spectrum has been adapted by Daugbjerg (1998a) to present policy commu-
nities and issue networks as two extreme network types on a continuum. He
considers the dimensions of membership, integration and institutionalization,
and considers how these vary between an extreme policy community and an
extreme policy network (see Daugbjerg, 1998a: 4044).
The biopesticides policy network
The biopesticides policy network falls clearly within the loose end of the
spectrum. It is relatively weakly developed compared with other networks
analysed in the political science literature. Grant has commented that the
biological control industry has the weakest policy network I have encoun-
tered (cited in Chandler, 2007). It often lacks political sophistication in that
technical knowledge is not always matched by an understanding of political
processes. It is relatively immature in the sense of being at an early stage of
organizational development and some of its members have problems of
limited resources and capabilities. There is also a lack of trust between some
of the key actors. It is more than just a loose network; it is also incomplete in
Policy Networks, Change and Innovation 179
that the retailers are barely integrated into it at all. This results in network
underperformance, even if it is not completely dysfunctional (Greaves and
Grant, 2010). The following potential participants in the biological control
policy network can be identied at member state level:
1. The regulatory agency (which may often form the hub of the policy
network).
2. The growers (and their representative organizations).
3. The biocontrol manufacturers (and their representative organization).
4. Consultants (who can be important intermediaries).
5. Environmental non-governmental organizations (NGOs).
6. Retailers.
7. Consumer organizations.
8. Academic researchers.
DEFRA is excluded from this list as, under governance arrangements, its role
should be one of steering. It is expected to be softer, less intrusive and less
hierarchical than under traditional systems of government. In short, there
has been a shift from government by a unitary state to governance by and
through networks (Rhodes, 2006: 430). Governance is seen as signifying:
... a change in the meaning of government, referring to a new process of
governing; or a changed condition of ordered rule; or the new method by which
society is governed. I employ a stipulative denition; it refers to self-organizing,
interorganizational networks.
(Rhodes, 1997: 35)
The Rhodes formulation makes clear that policy networks facilitate negotia-
tion and the development of shared understandings among participants.
In order to function properly, policy networks must be constitutive of all
relevant stakeholders.
Network components
We need to consider each of the components in the self-steering policy
network. The national regulatory agency can play a key role in both creating
and sustaining a policy network. CRD can be seen as the hub of the network
and it has devoted considerable resources to stakeholder engagement. It has
set up regular joint liaison arrangements with the IBMA and its Availability
Action Plan Implementation Group comprises a range of stakeholders.
Nevertheless, it is constrained in the initiatives it can take, both in terms of
the existing pesticides legislation (both EU and UK) and its mandated
aims and objectives. The objectives of the organization appear consistent
with promoting the wider use of biopesticides, but perhaps only with further
ministerial approval and guidance. At a practical level, the approvals side of
CRD is set up with scientic staff to undertake the task of registration to
ensure the safe use of pesticides; it may not, therefore, be equipped to take
on an advocacy role. The role of the biopesticides champion is to assist
180 Chapter 6
biologicals through the registration process, not to be an advocate in any
stronger sense of the word. As a senior ofcial within the agency put it, My
challenge is to promote the scheme, not to promote biopesticides, there is a
difference. While there are differences of culture within CRD, the Director of
Approvals has been very actively involved in network formation and devel-
opment activities. The challenge had been that we particularly felt that we
were not meeting the right stakeholders and they were not hearing us. You
had to sit back and ask why they are not listening to us (interview, 8 December
2005). One reason for this was the incomplete policy network.
A particular challenge for farmers and growers is the withdrawal of plant
protection products as a result of the EU regulatory review process. The
National Farmers Union (NFU) is active within CRDs Minor Uses Network
which has considered the contribution of biological products to lling gaps in
availability. The NFU seems relatively well disposed towards CRD; indeed, in
discussions about the EUs REACH regulations they recommended that PSD
should form the core of a new chemicals agency. Through their organizations,
farmers and growers are relatively well integrated into the policy network.
Despite undergoing organizational development, the IBMA has been
hampered by a lack of resources and the fact its technical knowledge is not
always matched by a comparable level of political sophistication. IBMA has
often had difculty in acting in a proactive fashion and portraying itself as an
authoritative spokesperson for the industry that can make effective decisions
about its stance on issues sufciently quickly. It has also not organized all
potential registrants of biopesticides, which is a challenge for CRD in their
outreach efforts directed at the industry. In addition, previous experience
with the regulatory system has, to some extent, undermined the condence
of product developers. Even when they do make contact they may be reluc-
tant to provide relevant information, making it difcult for CRD to assist
them. For those rms that do make contact, our observations have shown
that pre-submission meetings are vital parts of the process.
PSD had to build up its relationship with IBMA in order to nd a route
into the industry. As a senior CRD ofcial put it, [We] had to build up con-
dence, [we are] now much closer to IBMA, [we] had to break into them, [we
went] out there telling them there is a plan, but they were reluctant to come
and meet us. Another ofcial summed up: Its a new relationship with
the IBMA. Theyve offered us visits round plants formulation technology,
unfamiliar techniques, opportunities to see it in a eld. One practical indica-
tion of this new relationship is the joint working group of IBMA and CRD on
efcacy issues. IBMA is also a member of the Availability Action Plan Group
and CRD and others have been invited to IBMA meetings. The REBECA
programme, funded by the European Commission, has also brought together
relevant actors who might not otherwise have had contact. It has also been
argued that the annual conference of the IBMA in Lucerne is emerging as a
one-stop shop for the policy network.
Given the relative fragmentation of the policy network, it might seem
that specialist consultants would be able to play an intermediary role in
bringing actors together and using their technical expertise to devise policy
solutions. To some extent, consultants do play such a role. For example, they
are prominent in the IBMA and often form the IBMA delegations that interact
with the CRD, e.g. in the joint efcacy working group. There is, however,
some ambivalence about them within the hub of the network. One perception
within CRD is that we do consultants job for them in the sense that consul-
tants ring up and ask questions that they incorporate into advice that they
sell to their clients. There is concern that in certain instances they could convey
the impression to some clients that access to the regulatory system is more
difcult than is the case and this can produce some suspicion of their role.
Environmental NGOs tend to have a wider remit than pesticides, with
the exception of the Pesticides Action Network (PAN). There is a lack of
engagement by such groups in the biopesticides debate, reecting indiffer-
ence rather than hostility. For its part, IBMA was slow to reach out to envi-
ronmental groups as potential allies (and still nds it difcult to establish a
dialogue), which is disappointing given that their members are producing
more sustainable products than conventional pesticides. Environmental
groups have often been relatively isolated, with the debate about a more
sustainable agriculture being framed more around discourses about organic
farming. Although they have generally been critical of pesticides and called
for greater restrictions on their use, environmental groups have not been
particularly supportive of biological alternatives. This may be in part because
of a suspicion that they are still pesticides.
Retailers often push for levels of pesticide reduction more rigorous than
those required by regulators, which in themselves are very stringent (see
Chapter 7). Our research suggests a lack of connection between large super-
markets and the rest of the policy network. They do not tend to actively
promote biopesticides to their growers as a sustainable alternative to syn-
thetic pesticides, arguing that they cannot promote particular commercial
products. Marks & Spencer and Sainsburys are two exceptions; indeed, the
latter held a conference in 2008 to discuss advances in the use of biopesticides
with their suppliers. CRD sources have stated that links with retailers were
relatively tenuous and this was conrmed by our interviews with large
supermarket chains. One supermarket chain commented: [We] only interact
with PSD if they want specic information from us. Supermarkets put more
emphasis on using category management and their own supply chains than
building relations with CRD. There is thus a lack of effective engagement
between the hub of the network, CRD, and a key set of commercial actors
that are pursuing their own pesticide policies (see Chapter 7).
Retailers see themselves as proxies for the consumer, and consumer
organizations are not particularly involved in the discussion of biopesticides.
Consumers tend to have a clear, if rather ill-informed, image of organic
produce, but relatively little understanding of the potential contribution of
biocontrol agents to a more environmentally sustainable agriculture. As one
retailer put it when referring to the relative ignorance of consumers, You do
get some daft responses. If you ask them about organics, they say no pesti-
cides are required, when you explain there are pesticides applied, they get
very upset.
182 Chapter 6
Academic researchers can help link various participants into a more
effective network. We feel that our research has facilitated information
exchange among relevant actors and heightened an awareness of the con-
tribution of biopesticides. Our workshops, moreover, have helped bring
network participants together. Academics must be careful not to cross the
dividing line between being analysts and advocates. Nevertheless, they
should be able to win the trust of participants whose interests or perspectives
do not always coincide and hence facilitate constructive dialogue and the
identication of policy solutions.
Policy networks at the EU level
Incomplete or fragmented policy networks are even more evident at EU
level. There is an absence of any functional equivalent at the EU level of the
national regulatory authorities which can serve as a hub around which a
policy network can cluster. Such regulatory bodies can provide a location
for meetings. They also have authority resources, meaning the chance of
inuencing the way in which those resources are used creates an incentive
for meeting them. Farmers organizations, the IBMA and environmental
organizations are all present in Brussels, but the greater complexity of the
decision-making process resulting from co-decision makes it even more
difcult to focus representative efforts efciently than at a national level.
However, REBECA (www.rebeca-net.de) lled a signicant vacuum by
creating a neutral yet informed policy space in which various actors could
interact. The attendances at their conferences showed the considerable level
of interest in the subject of biological control agents, but also the relative lack
of opportunities to interact on a systematic basis. Regulators can also meet in
the Biopesticides Steering Group of the OECD or in various EU-level com-
mittees. Informal, bilateral links between regulators are also continually
developing. The IBMA annual conference provides one meeting point. How-
ever, with the end of REBECA, there is no general umbrella framework that
can facilitate the discussion of issues at a European level among a wide range
of actors. One consequence has been that debates in the European Parliament
have not always been as well informed as one might hope.
Policy Networks and Change
Policy communities have high entry barriers around them and can become
rather exclusive networks of well-established insider groups. Policy networks
give structure to the decision-making process, providing outsiders and insid-
ers with different opportunities for either changing or maintaining the
existing order within a sector (Daugbjerg, 1998b: 79). Therefore, for defend-
ers of the status quo, a sectoral policy network with a great deal of cohesion
among its members is a powerful political resource (Daugbjerg, 1998b: 79).
What emerges is an approximation of an elite cartel where participants
collude so as to preserve the existing parameters of the policy-making
process (Grant, 2000: 51). The objective of the policy-making process within
such communities is often not solving real problems, but avoiding conict,
creating or maintaining stable relationships, and the avoidance of abrupt
policy changes (Stringer and Richardson, 1982: 22).
Indeed, the most common and recurrent criticism of the policy network
analysis is that it cannot explain change (Rhodes, 2006). Richardson (2000)
summarized such arguments in a seminal article. Essentially, policy network
analysis stresses how networks limit participation in the policy process,
decide which issues will be included and excluded from the policy agenda,
shape the behaviour of actors through the rules of the game, privilege certain
interests, and substitute private government for public accountability. It is
about stability, privilege and continuity. Richardson observes that the 1980s
and 1990s witnessed much policy change and instability in West European
states. In particular, governments adopted a more impositional policy style,
and interest groups learned to exploit opportunities presented by a policy
process that was increasingly characterized by multiple opportunity struc-
tures. Richardson focuses on the possible causes of policy change, including
the importance of state power (e.g. government has been more assertive in
attacking some of the old distributional coalitions or policy communities
which were resisting policy change), changes in the behaviour of groups as
they adjust to and exploit opportunities presented by multi-arena policy
making, and the impact of new policy fashions, reecting knowledge and
ideas which can act as a virus-like threat to existing policy communities.
There have been three main attempts to build the analysis of change into
policy networks: advocacy coalitions, the dialectical model and decentred
analysis (see Rhodes, 2006: 436438). The advocacy coalition framework (ACF)
has four basic premises, helpfully summarized by Sabatier and Jenkins-Smith
(1993: 16): (i) understanding the process of policy change requires a time
perspective of a decade or more; (ii) the most useful way to think about policy
change is through a focus on policy subsystems; (iii) those subsystems
must include an intergovernmental dimension; and (iv) public policies can
be conceptualized in the same manner as belief systems, that is, sets of values
priorities and causal assumptions about how to realize them. Sabatier and
Jenkins-Smith argue that coalitions attempt to translate their beliefs into public
policy and their belief systems determine the direction of policy. Their resources
determine their capacity to change government programmes. Resources
change over time, usually in response to changes external to the subsystem.
Furthermore, they distinguish between core and secondary beliefs and argue
that coalitions have a consensus on their policy core resistant to change. In
contrast, secondary aspects of the belief system can change rapidly (see
Sabatier and Jenkins-Smith, 1993: 2534).
Marsh and Smith (2000), meanwhile, suggest a dialectical model whereby
change is a function of the interaction between the structure of the network
and the agents operating in it, the network and the context in which it
operates, and the network and policy outcomes. Networks are structures
that can constrain or facilitate action but do not determine actions because
184 Chapter 6
actors interpret and negotiate contracts. Exogenous factors may prompt
network change, but actors mediate that change. We must examine not only
the context of change, but also structures, rules and interpersonal relation-
ships in the network. Finally, not only do networks affect policy outcomes,
but policy outcomes feed back and affect networks.
Third, there are those who propose an interpretative turn and argue that
policy network analysis should make greater use of ethnographic tools such
as: studying individual behaviour in everyday contexts; gathering data from
many different sources; adopting an unstructured approach; focusing on
one group or locale; and, in analyzing the data, stressing the interpretation
of the meanings and functions of human action (Rhodes, 2006; paraphras-
ing Hammersley, 1990). Bevir and Rhodes (2003: 6278) argue for a decentred
study of networks, for a shift of emphasis from institution to individual, and
a focus on the social construction of policy networks through the ability of
individuals to create meaning. Although we take a scientic realist as opposed
to a social constructivist approach (see Chapter 2), elite interviewing and
observations are ideal methods if one is interested in actors perceptions of
the world in which they live, the way in which they construct their world
and the shared assumptions that shape it (Burnham et al., 2008: 246).
Rhodes (2006) concludes that all three approaches to network change
are part of a broader trend in political science in exploring the impact of ideas
on policy making. Sabatiers work on advocacy coalitions, for example,
stands alongside that of Kingdons (1984) on policy ideas and policy agenda.
Richardson (2000) discusses this link between changing policy networks,
new ideas and setting policy agendas. Ideas and knowledge can, he says,
upset the cosy life of established policy communities and networks
(Richardson, 2000: 1021). They can provide a real challenge to stakeholders
who have relied on the security of cocoon-like policy communities. In prac-
tice new ideas and policy frames often capture all stakeholders, who often
nd themselves adjusting to a new set of rules and power distributions quite
different from the old policy regimes.
Of course, some of the network literature does engage with the issue of
change. Daugbjerg (1998a), for example, develops a theoretical model which
establishes a causal link between network types and policy change. He
argues that where policy change is put on to the agenda, the kind of network
that exists has an important inuence. With a cohesive network, policy
change is likely to be moderate because network members can form strong
coalitions against outsiders. In contrast, radical policy change is most likely
where a non-cohesive network exists. In such a network, coalition forming
will be difcult (Daugbjerg, 1998a: 188189). Greaves and Grant (2010), how-
ever, have challenged some of these theoretical propositions. Coalitions may
be less likely to occur in loose networks, thereby allowing outsiders in and
promoting network change. However, it is unclear whether the necessary
interactions for policy change can then take place. Even if a looser network
can promote change in the sense of putting a plan together, it may not be able
to be implemented effectively. This could be a particular problem with
incomplete networks. It is likely, therefore, that policy change requires a
certain degree of cohesion in the network, even if rigid policy communities
will often impede change (Greaves and Grant, 2010). Greaves and Grant
suggest, therefore, that changes in the biopesticides regulatory framework
have occurred despite the loose network. It was in large part due to pressure
from the Cabinet Ofce. The authority resources of the state were used to
produce an outcome (thereby supporting Richardsons notion of state power
being used to drive through change). A somewhat more cohesive network
may, however, have promoted greater change; indeed, regulatory reform has
coincided with some strengthening of the network in recent years (Greaves
and Grant, 2010).
Marshs dialectical model also provides some leverage, in particular in
terms of feedback effects from policy. Government attempts to encourage
biopesticides have resulted in regulatory reform and changing attitudes
within CRD, which has fed through into improvements in integration within
the network, which in turn has resulted in improved outcomes in terms of
rates of registration. Marsh and Rhodes, moreover, argue that factors exoge-
nous to policy networks lead to changes in both the network and the policy
outcome. To understand and explain policy change, we need to understand
and explain network change. As Marsh and Rhodes (1992: 257) put it:
Most (network) change is explained in terms of factors exogenous to the
network, although the extent and speed of the change is clearly inuenced by
the networks capacity to minimize the effect of such change.
Intervention from central government departments would count as exog-
enous pressure, given the way we have dened the biopesticides network. In
Marsh and Rhodes view, however, the driver for change in networks and
outcomes lies in broader economic and political change and changes in
knowledge. Certainly, there are contextual drivers suggesting that biopesti-
cides may be an idea whose time has come. First, the public is concerned
about the possible health effects of pesticide residues on food. Second, there
is consumer preference, even when there are no safety concerns, for a
reduction in pesticide residues in food, leading to action by retailers, con-
sumers and the Food Standards Agency (FSA). There is also a requirement to
integrate chemical pesticides with alternative methods in order to develop
systems of crop protection which are sustainable. This has an ecological
dimension; crops need to be protected using methods which do not damage
the environment, in particular in terms of water pollution and biodiversity.
Public concern over the impact of pesticides on the environment, therefore, is
a third driver of change. Pesticides are also required that prevent the devel-
opment of resistance by the pest to the control agent. Following the imple-
mentation of European Directive 91/414/EEC there has been a signicant
decline in the number of active ingredients permitted for use in crop protec-
tion products. Moreover, because of the expense of research and registration,
manufacturers are unlikely to develop new chemical products on a large
scale. As there has been a reduction in the number of pesticide products
available for use, this increases the problem of pesticide resistance. The broad
solution is to use IPM, as outlined in Chapter 1.
186 Chapter 6
These contextual drivers may, at the margins, have promoted network
change, or at least a greater integration of actors into the network. They
are similar, certainly, to the exogenous pressures referred to by Marsh and
Rhodes. However, we should not overstate their importance in pushing
through change. The public may be concerned about pesticide residues but
are likely to have no clear view on biological alternatives, of which they
are not well informed. They may also be put off by the term pesticides.
Retailers, as we have seen, have done little to engage in the debate. Although
growers are particularly affected by problems of resistance and the with-
drawal of plant protection products, they are policy takers rather than
policy makers. They operate within the constraints of a stringent regulatory
framework and have to cope with the market power of the supermarkets.
Linking back to the literature on the inuence of ideas on policy networks,
biopesticides are not taken adequate account of in debates on sustainability.
This debate tends to be polarized between conventional and organic alterna-
tives with insufcient attention paid to IPM. Biopesticides do not have a
particularly high prole among decision makers.
There are two nal issues relating to policy networks relevant to this
discussion. First, the policy network literature tends to refer to change as
opposed to innovation (see Chapter 1 for a distinction between these two
terms). Arguably, it should make more use of the latter. Second, policy net-
work analysis often fails to discuss what it means by policy. Indeed, the
notion of policy or policy outcomes does not provide the full picture in an
age of governance. The modern meaning of the English notion policy is that
of a course of action or plan, a set of political purposes as opposed to
administration (Wilson, 1887). Above all, as Parsons suggests, we can see
policy as a rationale, a manifestation of considered judgement. It is an attempt
to dene and structure a rational basis for action or inaction (Parsons, 1995: 14).
Policy can be seen as culminating in a government decision. Birch (1979; cited
in Jones, 2001) distinguished between two broad kinds of government deci-
sions: (i) rules, regulations and public pronouncements; and (ii) public expen-
diture and its distribution. Does such an approach need updating, however,
to reect a new world of governance and the regulatory state
(see Moran, 2005)? As outlined in Chapter 1, in the regulatory state many
decisions are taken by government agencies.
However, can decisions taken by such agencies be dened as policy?
Osborne and Gaebler (1992) make the distinction between policy decisions
(steering) and service delivery (rowing). They argue that bureaucracy is a
bankrupt tool for rowing, and in its place they propose entrepreneurial
government, with its stress on working with the private sector and respon-
siveness to customers. This transformation of the public sector involves less
government or less rowing but more governance or more steering. In
essence, this is a denitional issue; it does not alter the fact that policy net-
works could impact on government agencies in the same way they may
impact on traditional policy outcomes. Furthermore, CRD has a policy
advisory role and some of its activities (such as the Biopesticides Scheme) go
beyond routine matters and can be dened as policy.
Having said this, the risk averseness of regulators means it may be
difcult to drive through the necessary change. Moreover, we are left with
the problem of whether network change can feed into signicant policy
change if the overall network remains very loose and incomplete. It is our
view that the incomplete network helps to explain why change has not been
as signicant as it could have been. However, as we have seen, policy
network analysis on its own cannot fully account for the change that has
taken place. We propose, therefore, to move towards policy network analysis
and focus on exogenous pressure (from government departments) and
endogenous pressures (from within CRD).
Regulatory Innovation
Innovation remains a central challenge for systems of regulation. As
Greaves (2009: 245) notes, Bureaucrats and regulators are typically risk
averse. The desire to avoid things going wrong means they are not natural
innovators. Risk averseness does not create an encouraging environment
for regulatory innovation (indeed, the term is almost a contradiction). As
we will see, regulatory innovation has occurred within CRD through an
interaction of endogenous and exogenous factors. These have come together
to create a window of opportunity through which regulatory innovation
has been able to occur.
Regulatory change, innovation or adaptation?
Does, however, the change count as innovation? To return to Halls typology
(as outlined in Chapter 1), some aspects of the Biopesticides Scheme are
essentially rst-order policy changes (e.g. lower fees for biologicals). Most,
however, fall within the category of second-order policy changes (e.g. a
biopesticides champion, pre-submission meetings, etc.). In some ways, lower
fees are the biggest change but, as Black suggests, rst-order changes may be
signicant in terms of scale or impact whilst not strictly counting as innova-
tion (Black, 2005a). Taking everything together, we can describe what has
occurred as regulatory innovation; to return to Black, it has involved new
solutions (Black, 2005a). Regulatory adaptation, on the other hand, would
imply more of a modication or alteration of existing practice, or incremental
change as opposed to the more radical reform which has taken place. It is an
unusual step for a regulatory agency that usually has to stick closely to what
is laid down in statute to negotiate new policy spaces in which to operate
(which is essentially what has happened here). In other words, PSD sought
clearance from DEFRA, particularly in relation to the funding of the scheme,
thereby creating a new space in which to take action. This has extended their
formal remit, albeit cleared by ministers. As their Director of Approvals puts
it, this has been quite remarkable for a regulatory agency (Sainsburys
Conference, 18 March 2008).
188 Chapter 6
Blacks ve worlds
We introduced Blacks ve worlds of regulatory innovation in Chapter 1. It
will be helpful now to elaborate on them a little. An emphasis on champions
is found in much of the work in public sector innovation. The characteristics
of such champions are risk preferring, being open to new ideas, persuasive,
empathetic and occupying key strategic positions within organizations.
Generally speaking, such individuals will have sufcient nancial resources
to absorb losses from unprotable innovations, be able to cope with a high
degree of uncertainty, and have a favourable attitude towards change and
risk taking. In the world of the individual, innovation is explained by one, or
sometimes two, key individuals who are able to push their performed inno-
vation through critical decision junctures or policy windows. This relates to
the work of Kingdon (1984) who argued that policy entrepreneurs take
advantage of policy windows offered by the concatenation of policy prob-
lems, policies and politics to catapult new items on to the political agenda
and change policy.
The organizational world suggests that innovation is fostered by organi-
zations in which: the leader or leaders have a positive attitude towards change;
there is low centralization; its members have a high degree of knowledge
and expertise; procedures are not highly formalized; there is a high degree of
interpersonal connections between the organizations members; and there is
a high degree of organizational slack, for example, the extent to which
uncommitted resources are available to the organization, with the biggest
factor being size ceteris paribus, large organizations are more innovative
than smaller ones. Also important are the existence of cultures that are
supportive of risk taking and can tolerate mistakes and failures.
The work on innovation within government (the state world) comes
mainly from political science. As Black writes, if the question how and why
does innovation in public policy occur is rephrased as how and why does
policy change occur or how and why does policy learning occur, then
immediately almost any theory of public policy formation would have an
answer (Black, 2005b: 25). Public choice theory would state that innovations
are political goods which are sold to the highest bidder or coalition of bid-
ders, and will depend on the distribution of costs and benets of particular
groups. Pluralism would argue that they come about through an interplay of
interest group pressures. Public opinion response theory would state that
they are the result of public pressure, mediated by the media. Rational the-
ories of bureaucracy would argue that they are the result of self-interested
bureaucratic decisions (Downs, 1967).
It is helpful to focus on such rational choice theories. Bureaucracies
have to cope with considerable forces of inertia, as outlined in the classic
text Inside Bureaucracy by Downs (1967: 195197). First, like most organiza-
tions, bureaucracies have a powerful tendency to continue doing today
what they did yesterday. This is because established processes represent
an enormous previous investment in terms of money, time and effort. If
new behaviour patterns are adopted, these costs must be faced again.
Downs believes that the more ofcials that are affected, the greater resistance
will be to signicant change. Therefore, the larger an organization is, the
more reluctant it will be to change, and small bureaus tend to be more ex-
ible and innovation minded than larger ones. Second, self-interest motivates
ofcials to oppose changes which would result in net reductions in things
they personally value, such as personal power, prestige and income. There-
fore, ofcials will tend to oppose changes that would lead to a net reduc-
tion in the amount of resources under their own control; and changes that
would decrease the number, scope or relative importance of the social
functions entrusted to them. Downs explains that this is why transfers of
functions from one section to another are often resisted by the sections
losing functions.
Downs, however, suggests some drivers for change (Downs, 1967: 198
200). First, there is the desire to do a good job. This could be due to loyalty
to specic parts of the bureaucracy, to specic ideas or to society as a whole.
This motive will be particularly prevalent in the creation of new bureaus or
new sections within an existing bureau. Second, there is the desire for
aggrandisement. Downs writes that self-interest is a powerful cause of iner-
tia, but it can motivate change if ofcials receive greater rewards for altering
the status quo than preserving it. The greatest of such rewards are gains in
power, income and prestige associated with increases in the resources con-
trolled by a given ofcial or a given bureau (Downs, 1967: 198). Politicians,
however, are more reluctant than ofcials to increase the total size of the
government budget. Ofcials, therefore, have a better chance of getting their
resource-expanding innovations improved if they can reduce expenditures
elsewhere. Therefore, proposed innovations must carry out social functions
performed elsewhere, leading ofcials with a powerful motive to capture
functions performed by other bureaucracies. A third motive for change in
bureaus is self-defence against pressure from external agents, such as aboli-
tion or threats to reduce its resources. Bureaucracy threatened with aboli-
tion, for example, must nd new functions or reinstate the importance of its
present ones. To some extent Downs analysis was undermined by manifest
evidence that bureaucrats satised rather than maximised (Deakin and
Parry, 2000: 63). Dunleavys (1991) bureau shaping model came to be inu-
ential, suggesting that size and aggrandisement were not ends in them-
selves but that bureaucrats would calculatedly shape their task to obtain
the optimal mixture of rewarding and achievable work (Deakin and Parry,
2000: 63).
There is not always such a clear distinction between change and innovation
in the literature as Black (2005a) suggests: Downs (1967), for example, seems
to use the terms interchangeably. That being said, the literature in the state
world directly associated with innovation is rather narrow. The institu-
tional literature, however, has focused to some extent on innovations, and
provides a broad set of arguments. Central to new institutionalism is that
institutions matter as they provide the structure to which the action and
interaction occurs (March and Olsen, 1984). The approach suggests that
innovation is explained by the impact of institutional structures on decision
190 Chapter 6
making by political actors, including bureaucrats and those in regulatory
agencies.
The global world focuses on policy making by international bodies and
networks. States have been relatively passive or bypassed in many areas of
policy development which are nevertheless regulatory in character. Either
they are willing to be instructed by international organizations or epistemic
communities as to what action to take,
2
or they are bypassed by transnational
organizations that set technical or professional standards (Boli and Thomas,
1997). Finally, we have the world of the individual. An idea is likely to be
adopted and enacted primarily on the shape and form of the innovation itself
and, for some, on the extent to which it ts with the prevailing cognitive/
normative frameworks. The more the innovation is simply expressed, trial-
able and observable, the more it is expressed as a general theory, and the
more it ts, or can be represented as tting, with dominant cognitive and
normative schemas, the more likely it is the idea or innovation will be
adopted (Black, 2005b: 40).
Through our research, we have developed an understanding of how
regulatory innovation within CRD is likely to have occurred. In terms of
Blacks ve worlds, key individuals have been vital in driving the process
forward, within both the Cabinet Ofce and CRD. Similarly, organizational
characteristics have played a role (for example, the relatively small size of the
organization, a desire for knowledge among the scientic regulators, etc.).
Moreover, there has been the intervention of the Cabinet Ofce and the
impact of institutions (the state world). Although the global world is of
less signicance, CRD operates within OECD guidelines, has engaged with
REBECA, and the review of Directive 91/414 is clearly important. In terms of
the world of the innovation, biopesticides t into their surrounding envi-
ronment, not least in terms of issues surrounding sustainability, pesticide
resistance and the limited number of products. They are not, however, an
idea easy to get to grips with or widely understood.
Black can be criticized for trying to cover every possible theory or expla-
nation: there is not much differentiation or selection, and therefore potentially
little leverage. To some extent she acknowledges this, stating one is inevitably
prey to the criticism that what is offered is simply a bewildering variety of per-
spectives or explanations with no clear direction as to which course one
should take (Black, 2005b: 41). Black states that her aim is to provide an analytical
framework for much richer explorations (Black, 2005b: 41). It is concluded that nei-
ther the occurrence nor the outcomes of innovation can be controlled and
predicted. Innovation simply cannot be engineered (Black and Lodge, 2005:
194). We propose a framework that focuses on the contextual and exogenous
and endogenous drivers for regulatory innovation (see Greaves, 2009 for a more
detailed justication for this). While overlapping with Blacks analysis, it
provides a clearer framework for our purposes. Blacks analysis may not
always provide the necessary clarity. For example, individuals may be part of
the world of the individual or the world of the state. There is also considerable
overlap between aspects of the individual and organizational world: it is
not always clear what should be placed in which category. Similarly, there is
overlap between the organizational world and much of the institutional
literature. We believe that our framework will help to provide greater clarity.
Exogenous and Endogenous Pressures
The intervention of the executive is an example of exogenous pressure. The
then Business Regulation Team (BRT) of the Regulatory Impact Unit of the
Cabinet Ofce noted in 2003 that, although DEFRA had been funding
the research and development of alternatives to synthetic pesticides, none
had been able to obtain the authorisation required for such products to be
placed for sale in the UK as plant protection products. They argued that PSDs
testing requirements were evidently designed to cope with standard, mass-
produced synthetic chemical pesticides which, by their nature, tend to deliver
very high efcacy rates, and not with this group of safer alternatives this
appeared to be an interesting example of regulation-inspired market failure
(BRT, 2003: 19).
DEFRA hoped to encourage the wider use of biopesticides in order to
achieve its sustainability objectives. However, given such limited progress
the institutions of the core executive were required to intervene. In the coded
language of the civil service, the BRT approached PSD seeking to help to
establish a workable solution to this problem. In Grants words, they used
their authority to lean on PSD (Grant, 2005: 15). The fact that the Govern-
ment leaned on PSD was conrmed both by a senior gure within PSD and
by an industrial executive seconded to BRT to work on biopesticides. The
Director of Approvals commented that there was a political driver but it
wasnt DEFRA or growers, it was the Cabinet Ofce. Furthermore, it was
someone on secondment to the Cabinet Ofce, not a career civil servant
(Biopesticides Workshop, 31 October 2007). He added, We did need some
pressure to introduce the scheme. He gave us a kick in the teeth (REBECA
Conference, 2021 September 2007). PSDs aims and objectives, agreed
with ministers in spring 2003, included reducing the negative impact of
pesticides by encouraging reductions in their use, taking account of good
practice, and developing and introducing alternative control measures
(PSD, 2004: 9).
One retailer put it to us: PSD is under pressure to try and help their policies
to adapt. The Regulatory Affairs Ofcer for a manufacturer and supplier of
pesticides (including biopesticides) provided an interesting insight into how
PSD is beginning to change. They want to be seen to be doing something [it
is] now in their best interests to look at solutions. If theyre the rst regulatory
authority to get something in place and have a way to get products to the mar-
ket, other European countries will follow what they have done. The decision
to make the pilot scheme formal, for example, was almost done from a PR
point of view. They were told they had to do something about it. Similarly,
someone on high said, you will have a biopesticides scheme. Such exogenous
pressure, however, needed to combine with endogenous forces; or in other
words a positive response from within the regulatory body. It was reported
192 Chapter 6
that PSD was keen to discuss ways in which the pursuit of this new aim could
be promoted (BRT, 2003: 19). In other words, they realized they had to do
something. In the words of Pendlington and Dickinson (2003: 23):
The message from the Business Regulation Teams work on biopesticides is
quite simple: the Principles of Good Regulation can be used as a framework for
dialogue between regulator and regulated. The successful conclusion of this
project reects well on all concerned. On the side of the regulator, there was an
obvious recognition of the existence of a problem and a willingness to think
creatively about possible solutions.
The Director of Policy and the Director of Approvals made the joint decision
to have a pilot scheme. The latter decided to make the Biopesticides Scheme
permanent, conrming that key individuals were vital in moving the process
forward (Biopesticides Workshop, 31 October 2007). The Director of Approv-
als has stressed the importance of an effective and strong team in driving
through change (Biopesticides Workshop, 31 October 2007). One consequence
of the Biopesticides Scheme has been the development of an informal inter-
nal network of staff with interest and expertise in issues related to biological
control (W. Grant, unpublished). These include the appointment of specialist
bio-contacts. CRD staff members are used to team working as they work in
groups on approval processes and the agency has a relatively informal
working style and horizontal structure in which relationships are based on
collegiality and mutual respect (W. Grant, unpublished). They have received
training to help them to develop their skills and have been very receptive to
this career development opportunity (W. Grant, unpublished). We have
noticed how those working on biopesticides show great enthusiasm for their
work, perhaps because of a desire to do a better job, or to gain new skills or
expertise, or that doing the job well is a successful career-building strategy.
This links back to some of the arguments of Downs (1967) and Dunleavy
(1991). A senior ofcial adds that they were lucky in the people they had
picked to work on biopesticides, if others had been chosen it may not have
worked so well (unstructured discussion, 31 October 2007).
In one of our observations the approvals process was started by three
resource managers with an initiation meeting. This, along with the approval
process integrating a number of different specialisms (a large number of
individuals were brought into pre-submission meetings), shows that it is a
relatively horizontal process. This may be more favourable to innovation as
individuals have an opportunity to learn from different specialists. Moreover,
those within approvals see themselves as scientists rst and as regulators
second: in other words, scientic regulators. They are keen to extend their
scientic expertise and have shown an interest in learning about biological
alternatives. This knowledge is driving regulatory innovation forward (link-
ing back to Black, 2005b: 20), with pre-submission meeting in particular
allowing CRD to build up its expertise and develop a more appropriate
registration process. As the Director of Approvals puts it, they have built a
team of specialists who understand the issues and are continuing to learn
(Sainsburys Conference, 18 March 2008).
Institutional Reform
As a new institutionalist would claim, the structure of institutions inuences
the behaviour of those within them. Stakeholders have held differing views
on how the regulatory structure regarding pesticides could be reformed. One
suggestion in our interviews was to enlarge the role of PSD so that it became
a more general chemical regulatory and inspection authority with functions
from other government agencies combined into it. Another idea was that
PSD should be subsumed into the Environment Agency. This, however, could
change the focus of PSD work to environmental impact, which, when it
comes to biopesticides, could be even more costly than demonstrating
efcacy. A further suggestion was for a separate agency for biological
controls. As Grant puts it, however, there might be insufcient work for
such an agency on a country basis, but there might be a role in this area for
the European Food Safety Agency at EU level (Grant, 2005: 18).
The UK RCEP, meanwhile, published a report in September 2005 entitled
Crop Spraying and the Health of Residents and Bystanders. This received consid-
erable media attention and recommended that stricter controls be placed on
the spraying of pesticides on crops, given that they may be causing ill health
to bystanders and those living near sprayed elds. The report recommended
that responsibility for pesticides policy be separate from that of the approval
of pesticides. One suggestion was to move the policy function from the PSD
to a unit within the Environment Directorate of DEFRA. The report added
that the remaining functions concerned with the approval of pesticides could
be transferred to the Environment Agency in order to ensure better coordina-
tion with wider environmental objectives. The ACP published their response
to the report in December 2005. While there were parts of it with which they
agreed (ACP, 2005: 3), they were generally very critical. With regard to the
governance issues, they believed it to be a complex issue, and did not believe
that the limited discussion in the report provided an adequate basis on which
to form a judgement. They went on:
We can see that there are advantages in close liaison between the policy and
regulatory functions ... and we would like to see the case for separation
in more detail. We would, however, emphasise the need, when making
decisions in this area, to take into account the current excellence of the
scientic and technical staff at PSD. In our view, their performance is as strong
as that of the best government departments and agencies, and ahead of the
majority. It also compares favourably with that of pesticide regulatory agencies
in other European countries. We believe it would be most unfortunate if a
reorganisation caused this valuable concentration or expertise to be lost.
(ACP, 2005: 33)
Of course, there is a tendency for governments to bring about institutional
changes in response to criticism as a substitute for making changes in policy.
For example, if PSD was incorporated into the Environment Agency, would
its functioning change that much, particularly if the same people continued to
work in the same distinct ofce in York? That being said, one particular way
194 Chapter 6
of encouraging innovation may be through systematic reviews of provision.
The Hampton Review on UK regulation, set up by the Chancellor of the
Exchequer, reported in April 2005 and proposed streamlining the regulatory
structure on the grounds that there were too many small regulators (Hampton,
2005). A Better Regulation Executive was set up in the Cabinet Ofce to
deliver the reforms. As Grant puts it, what is evident is that the core executive,
in terms of both the Cabinet Ofce and the Treasury, are actively engaged in
issues of regulatory structure (Grant, 2005: 18). Indeed, the Hampton Review
was prompted in part by the Treasury who are concerned about the cost and
powers of regulators. Part of the broader political context, moreover, is the
growing criticism of the government for excessive regulation.
The Hampton Report proposed streamlining the regulatory structure on
the grounds that there were too many small regulators. It did not make a
specic recommendation regarding PSD, which was on the cusp as far as size
was concerned. However, the implication could be drawn that it should be
merged into a larger more thematic regulator. DEFRA launched a formal con-
sultation on merging PSD with the HSE, linking to the latters existing
responsibilities for biocides and REACH. Ministers decided the organiza-
tions should be merged from 1 April 2008. As part of this decision it was
also agreed that strategic policy for pesticides should remain with DEFRA
and operational policy should transfer with PSD to HSE (PSD, 2008: 4). There
is a risk that a greater focus on chemicals strategy within the merged
organization might lead to less attention being placed on biological
alternatives.
Despite the thinking behind Hampton, a relatively small organization
may be more exible and responsive and better able to develop an organiza-
tional culture favouring innovative responses to new challenges. Further-
more, a body with a clear and specic purpose may be more conducive to
regulatory innovation than a larger and potentially more unwieldy one.
Downs (1967), as we have seen, argued that change is easier to drive through
in smaller organizations: in other words, the more individuals affected the
more difcult it will be to push it through. Of course, the literature on orga-
nizations suggests it is easier in larger organizations due to uncommitted
resources and organizational slack. In our view, staff will be more account-
able for their actions in smaller organizations; in other words it is easier to
note who is performing their jobs effectively. Furthermore, good working
relationships and a high degree of interpersonal connections exist within the
approvals side of CRD (linking back to Black, 2005b: 20); its close-knit nature
fostered by its size. On balance, therefore, the relatively small size of the
organization and its clear purpose are likely to have been conducive to
regulatory innovation.
Conclusions
Modern regulatory philosophy emphasizes a move away from command
and control regulation. To put it another way, there has been a move away
from top-down, hierarchical forms of government towards more horizontal
forms of governance involving negotiation between various actors. Stakeholder
engagement is a key component of this new mode of governing. Policy
network analysis is of relevance here and it is important to pay attention to
problems arising from incomplete or fragmented policy networks. Regulatory
innovation is needed to facilitate the wider availability of biological control
agents, but is not easy to achieve. Reconguring the regulatory process
involves a learning process for the regulators and a willingness to engage
effectively with a range of stakeholders. Again, this links back to notions of
governance and policy network analysis. The Biopesticides Scheme has not
overcome all problems as the level of applications is still relatively low. This
reects in part the fragmented character of the policy network and the fact
that not all developers are IBMA members.
What is generally agreed is that there needs to be more stakeholder
involvement in policy design and implementation. The weak policy network
in the UK is in contrast to the USA where the biopesticides industry as a
whole pushed for action on biopesticides, rather than the government (inter-
view with EPA, 18 November 2005). It also contrasts with the Netherlands
where there is a much more effective relationship between different stake-
holders, in part through the medium of the Genoeg project. There are specic
features that have made this possible, but this does not mean that there could
not be more effective dialogue in the UK. Put simply, the biopesticides net-
work in the UK provides a good and understudied example of network
underperformance (Greaves and Grant, 2010). In the following chapter we
consider the notion of retail governance. As we have seen, the sphere of
consumption is insufciently articulated in the network. This leads to a cre-
ation of a supplementary private system of regulation in an attempt to meet
consumer concerns about pesticides. However, this supplementary system
of regulation does little to promote biopesticides as a safer alternative.
Note
1
This chapter draws on Greaves (2009) and Greaves and Grant (2010).
2
Epistemic communities are knowledge-based communities with an authoritative claim
to policy-relevant knowledge within their domain of expertise.
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7
Retail Governance
Retailers are capable of playing an important role in the dissemination of
biocontrol products. They enjoy high levels of trust from their customers,
who are concerned about residues from synthetic pesticides on fresh produce.
By advocating the wider use of biocontrol products by growers, retailers can
do much to stimulate their adoption. However, this needs to be done in a
way that does not make the work of growers more difcult. It also has to be
remembered that retailers are in business to make a prot and there are some
tensions between their private systems of regulation and the state-backed
system. This chapter draws on interviews with retail managers and others;
the grammar and sense of the quotations have been improved.
Retailers have been permitted to assume functions that might otherwise
be regarded as public in character, extending the scope of private retail
governance. This can set up tensions with the public world of regulation,
often referred to as the regulatory state (see Chapter 1), as it can mean two
systems of regulation operating alongside each other. In a strict sense, pri-
vate regulatory governance is not regulation in that it involves the issue of
authoritative decisions by a state body to private actors. Instead, it relies on
the use of contractual mechanisms to achieve desired goals. The market
power of large retailers means that standards that they impose are in prac-
tice mandatory. One regulatory agency respondent argued in interview:
Growers are concerned that more restrictions are being put on how they
grow produce and this is giving an advantage to imported produce. They
see this as regulation, which it isnt, it is guidance. However, the effect on
the private actor is broadly the same, it is just that the potential penalties are
different: in one case, a ne or similar penalty; in the other, the withdrawal
of an important contract.
The chapter draws in particular on interviews with major supermarkets.
Senior technical managers (all in the fresh produce area) at head ofce were
generally the respondents in supermarket chains, although two different
Retail Governance 199
managers were interviewed in the largest retailer and one other retailer
sent three managers and two consultants to be interviewed at a university
location. Because of considerations of commercial condentiality, retailers
are identied by letters A to H.
The Economic Power of Retailers
Retailers play a key role in British political economy, but one that is relatively
understudied. Britain has a highly concentrated food retail sector in particu-
lar with one rm, Tesco, accounting for some 30% of total grocery sales.
Along with three other companies (Asda, Sainsburys and Morrisons) it
accounts for 76.5% of the UK grocery market (Food Ethics Council, 2005: 5).
Retailers of food and household goods play a key role in determining rates of
ination which are an issue of crucial concern to government, even if interest
rate setting has been depoliticized. In August 2007, for example, the Con-
sumer Price Index fell sharply, in part because of price cutting by retailers.
However, retailers have a wider role in relation to other issues of public
concern such as food safety and food quality.
The post-war period has seen a shift of power down the food chain, not
just in the UK, from the farmer and the food processor to the retailer. In the
rst three decades after World War II, producers were encouraged and
subsidized to maximize production against the background of the experience
of food scarcity at the end of the armed conict in Europe. There were also
fears about food security in the context of the Cold War. Over time concerns
developed about the budgetary costs of the subsidies paid to farmers, their
distorting impact on world trade and the consequences that intensive farm-
ing had for animal welfare and the environment. Nevertheless, farmers still
receive substantial subsidies in almost all OECD countries, the principal
exceptions being Australia and New Zealand.
The retail sector was still very fragmented in the UK and elsewhere in
the decades after World War II, even though there were a number of multiple
chains. Over time the UK grocery market came to be dominated by a small
number of retailers. Although it has happened more slowly there, this pat-
tern is being replicated in continental Europe. The factors that have favoured
concentration at a national level have included improvements in road trans-
port and air freight which have facilitated the development of centralized
depots that then service individual stores. Products can be sourced from
across the world in a exible way that requires the producer to adjust to
variations in demand resulting from factors such as changes in the weather.
The development of information technology has allowed much more precise
control of stock ordering systems. This in turn permits more efcient supply
chain management as well as the recording and analysis of precise data,
related to demographics, about consumer purchasing patterns.
As the buying power of the big retailer groups has become more concen-
trated, one has seen a second phase of food regulation dominated by supply
chain management and food standards strategies, designed and increasingly
200 Chapter 7
applied by the large multiple food retailers (Marsden et al., 2009: 124). Rather
than the state having a key role, food regulation was driven primarily by the
way food safety issues are perceived by large food retailers; leaving the State
mainly to act as auditors rather than enforcers of the mainstream process
(Marsden et al., 2009: 125). Using their market power the large multiple retail-
ers have been able to impose increasingly demanding conditions on manu-
facturers and primary producers. Manufacturers may be required to pay for
the privilege of their goods being prominently displayed in the store, asked
to discount products in two-for-one or similar offers or to contribute to the
cost of new store openings. Primary producers face increasingly demanding
contracts in terms of price, quality and food safety standards, backed up by
regular inspection visits in accordance with the slogan if you dont comply,
you cant supply. It can be argued that the oligopsony power of European
retailers has been strengthened by producer-led food safety and quality
assurance schemes (Food Ethics Council, 2005: 5).
Marsden et al. (2009) identify the development of a third hybrid public
private phase of food regulation involving greater institutionalization at
both the domestic and EU levels. This represents a complex model of good
governance in which public and private interests are bound together in ever
more sophisticated ways to deliver safe food (Marsden et al., 2009: 204). They
see a blurring of the public and private in relation to food safety as particu-
larly apparent in relation to risk because private and public actors have
complementary interests in managing food risk to maintain public condence
in the foods they consume. However, they do not see these developments as
diminishing the role of retailer-led private regulation. Retailer power is not
diminished even though there may be some reconguration of its relationship
with the state.
The Political Power of Retailers
The growing economic power of retailers has been matched by a growth in
their political power, reected in the formation of pressure groups that target
retailers. This growth in political power has not been through the conventional
route of trade associations or even through direct contacts between major com-
panies and politicians, although these are not without importance. However,
the main emphasis is on the development of a private system of governance
by retailers that meets consumer concerns and goes beyond what is required
by government-designed systems of regulation and also assists in the delivery
of government policy objectives. As Marsden et al. (2000: 28) explain:
By the early 1990s in Britain there was a discernible switch in public
policy to shift responsibility for food matters to the retailers; the major
retailers have clearly become signicant actors in the promotion and
implementation of, for example, health policy Reciprocally, the
regulatory state has become critically dependent upon the continued
economic dominance of the retailers in their role as the major provider
of quality food goods.
Marsden et al. (2000) argue that, As a result, in a very real sense, [the retail-
ers] act on behalf of the state in delivering consumers rights and choices.
Retailers are involved in a number of policy areas such as preventive
health policies that promote the consumption of fruit and vegetables where
there is a clear convergence in the interests of retailers and government.
However, food safety has been an area in which the shift of responsibility has
been particularly extensive. The 1990 Food Safety Act was a signicant point
that made retailers give more consideration to their responsibility for food
safety. The ability of the major retailers privately to regulate their supply
chains and thus guarantee food standards has been formally recognised with
the Food Safety Act (1990) (Marsden et al., 2000: 53). An important frame-
work of food law still exists and may lead to enforcement action on retailers
that sell food that is contaminated or unhealthy. Nevertheless, the general
trend is for public food safety regulation to become less detailed and less
prescriptive. At the same time, important forms of private regulation are
more detailed, with a high degree of intervention curtailing freedom of regu-
lated rms (Havinga, 2006: 529). Thus, it is increasingly the quality and
safety standards set by retailers and other companies, rather than those
set by governments, which matter most to producers and consumers (Food
Ethics Council, 2005: 3). As a manager at Asda Wal-Mart has put it, The
retailer has moved to being the guardian of food standards (Brown, 2005: 20).
This form of relationship is entirely consistent with a depoliticized mode
of governance where responsibility is shifted from government to other actors.
In essence, depoliticisation as a governing strategy is the process of placing at one
remove the political character of decision-making (Burnham, 2001: 128). It has
typically been discussed in relation to macroeconomic policy making, but has
also been deployed in other spheres of policy. Thus, the operational slogan
all power to the central bankers has its echo in all power to the multiple
retailers. However, the blurring of public and private authority is not without
its problems. In relation to pesticides in particular what has developed is a
supplementary system of regulation by retailers that goes beyond the require-
ments of the state system. Pesticides are the most intensively regulated area of
the food chain, but nevertheless remain an area of consumer concern that
could frustrate policy objectives such as high levels of fruit and vegetable
consumption as a preventive health measure. Research by the Institute of
Grocery Distribution (IGD) found that The respondents saw the use of pesti-
cides as an area of interest and concern and wanted to know what had been
used on their food products (IGD, 2002). The coexistence of public and private
systems of regulation produces tensions between the system of private retail
governance and more traditional components of the regulatory state.
The Drivers of Private Regulation
The involvement of supermarkets in creating private systems of regulation
of pesticides is primarily driven by commercial considerations, although part
of that is protection of reputation and the brand image. As Retailer D put it,
202 Chapter 7
We are working to protect our logo, the reputation we have in terms of
food safety. Supermarkets are relied on by their consumers as their most
important provider of information on healthy eating, ranking higher than
the government regulatory body, the FSA (FSA, 2007: 62). Pesticides residues
on food remain a subject of concern for retailers. Hence, by demonstrating
that their fruit and vegetables have fewer pesticide residues than those of
their competitors, supermarkets may be able to develop a competitive edge.
As one supermarket manager commented, If the customer wants no resi-
dues we should look on that as an opportunity This ts in with the brand
image, the message in our shops. Another retailer commented: It is not just
about consumers, it is about protecting the whole brand.
Two notes of caution are necessary. Supermarkets are not a homogeneous
group; they have their own perceptions of where they t into the market and
this in turn drives their strategies, particularly in terms of the extent to which
they place an emphasis on price or quality considerations. It is important to
note that research by the IGD shows that price, sell-by date and taste are the
main factors inuencing purchase by over 70% of consumers. In contrast less
than a quarter of consumers consider factors covering production issues such
as GM, animal welfare, and grown in the UK as inuencing purchases (IGD,
2002). Retailer A, one of the innovators in terms of private regulation, is
rather unusual in stating that [o]ur business is not about large volumes, its
about premium quality, doing things differently, a niche food retailer. In con-
trast, Retailer G, one of the smaller rms in the sector, commented: One is
always driven back to costs. The market place weve got is very competitive
so you cant afford to be out of line commercially.
The technical and managerial resources that supermarkets have to deal
with these issues vary in their extent. Retailer C remarked of Retailer D, they
havent got the technical resources in house, they are looking for a stable
risk management route. Retailer D conrmed in interview that it was more
reliant on the use of external consultants, commenting We need to compete
in terms of how the rest of the industry is moving. Were a retailer, dont
apply pesticides to anything, its not our area of expertise. Retailer F frankly
admitted that it was replicating all the things that Retailers A and H had
done. Retailer C noted that Retailer D are adopting the system we have,
calling it a different name and slightly different, but I am more than happy
with that. Retailer G had experienced substantial staff cuts over the last year
and commented: We let the regulators and our growers get on with it. He
elaborated: We are all different. My line manager wanted me to do a [Retailer A]
list. I said I would have to sit behind my desk all day doing the list, updating
it, thats why we have PSD. Not all retailers can deploy the resources required
for effective private regulation.
Second, retailers are not internally homogeneous. The lead on pesticide
issues is usually taken by technical managers who have the relevant expertise.
However, it was suggested in interviews that policy communication or mar-
keting teams might have a different perspective. When Retailer F was asked if
its new programme was intended to give it a commercial edge, the reply was:
It doesnt give an edge at the moment. The head of commercial trading will
dislike it I am not just interested in the price this year. I want a long-term
sustainable relationship with packers and then with growers My bosses
would say this is about giving us a commercial edge. Im passionate about it.
At Retailer C the role of technical managers for produce categories was
to make sure we have products on the shelves that the customer wants in
terms of quality and price all year round and feeding back into best farming
practice. In contrast, the trading law and technical manager acted as an
overall coordinator and referee, making sure that the balance is right across
board. [Im] coming from a customer perspective and risk to human health
and legal compliance.
There may be limits to the extent to which it is possible to create a greener
image for a supermarket. As one retailer commented, The ability to put one-
self on high moral ground is shrinking, there is not much headroom left to
say how squeaky clean we are, the likely public relations return is reducing,
particularly on the produce side. However, there are also more negative
drivers about potential damage to brand and reputation. Concern about
adverse media publicity was a recurrent theme in the interviews. As Retailer
C put it, No one wants to be the person in the paper next time round.
Another retailer commented: Any retailer does not want a front page in tab-
loids protecting the brand a key part of that. A senior technical manager
commented: Directors wont say to you, I have a concern on X, its only if it
becomes an issue and it is up in lights in the local paper and [our] name is on
television. His counterpart in another retailer commented: All our residue
testing is geared around public perception. If the Daily Mail rings up and
says Youve got a problem with your spinach, press ofce can say, We
know about that and xed it months ago Pesticides management works
ne if it doesnt get in the papers.
NGOs and the negative publicity they can generate were also seen as
drivers of company policy. One retailer had at one time refused to meet with
them, but [w]e had a lot of bad problems from campaign groups who started
picking on [Retailer A]. The retailer started a strategy of engagement with
such groups, holding conferences to which they were invited along with gov-
ernment regulatory agencies. Retailer C noted that Retailer B, which sought to
cultivate a green image, have lots of conversations with Friends of the Earth
and Greenpeace. Retailer H, which also seeks to portray a green image, noted
that it had very good links into NGOs that sat on its group of experts on pes-
ticides, specically naming Friends of the Earth and the Royal Society for the
Protection of Birds. One retailer considered that the pressure was lower
than it had been. This was partly because some of the battles had been won
in terms of retailers responding to concerns. It also reected the increased
importance of other issues including nutrition, waste and energy issues.
How Private Regulation Works
The exercise of private regulation in retailing largely takes place on a
rm-by-rm basis with considerable variations in the schemes devised by
204 Chapter 7
each rm. This reects the drive to gain a commercial edge over competitors
and the company state model of governmentbusiness relations in Britain,
with trade associations often being relatively weak intermediaries and many
initiatives taken by rms. The least well resourced retailer did, however, work
closely with the Fresh Produce Consortium noting that it would have insuf-
cient clout to work independently. Some use was made of informal networks
to exchange information. One of the managers at Retailer D commented:
Weve all got contacts. Its an incestuous business. Individuals move around
rms and develop contacts in that way. Youve got your own contacts. Retailer
H commented: Weve done bits and pieces with other retailers over the years.
I think you know which ones we would work with.
The role of standards organizations
Insofar as retailers do work together, it is through standards organizations
that can set requirements about the way in which products are produced.
In this way they can offer a collective response to consumer concerns and
reassure consumers. In the UK the origins of these schemes go back to the
NFUretailer partnership of the early 1990s. EurepGAP (now GlobalGAP)
was set up in 1997 by a German-based company EHI to enable retailers to
cope with seasonality of fresh produce and the need for imports to provide
the continuity of supply demanded by consumers. It has 500 members who
are European food retailers, agricultural producers and associate members
from the input and service side of agriculture:
EurepGAP was driven by the desire to reassure consumers Food safety is a
global issue and transcends international boundaries. Many EurepGAP players
are global players in the retail industry and obtain food products from around
the world. For these reasons a need has arisen for a commonly recognized and
applied reference standard of Good Agricultural Practice which has at its centre
a consumer focus.
(EurepGAP, 2006)
Its role is to create international standards for agriculture. Technically speak-
ing EurepGAP is a set of normative documents suitable to be accredited to
internationally recognized standards such as ISO Guide 65 (EurepGAP,
2006). Its focus is on practices on the farm, with other Codes of Conduct and
certication schemes relevant to food packing and processing coming into
play once the product leaves the farm. It has met objections from African
countries arguing that it was an additional trade barrier and the issue has
been reviewed by the World Trade Organization.
EurepGAP covers imported produce, and as GlobalGAP increasingly
trades around the world, while the UK Assured Produce Scheme was set up
as a means of responding to requests from retailers on food safety (interview
with former Chair, 27 June 2005). Its importance is also recognized in the
National Pesticides Strategy: The Farm Assurance Schemes have been and
are likely to remain important vehicles for changing practice in the farming
industry (PSD, 2006: 12). If growers of produce want to market to the major
multiple retailers, they have to be members. Fifty-two fruit, vegetable and
salad crops are covered. The board and council of the scheme are made up
of representatives of the UK supermarkets, growers, processors and the
NFU. The scheme involves registering the crops grown, the completion of
a Self-Assessment Questionnaire and an annual audit on the farm by an
independent certier to verify that the questionnaire has been properly com-
pleted. One of the objectives is to minimize pesticide inputs. It is claimed that
the scheme saves growers substantial time and costs from having to meet
many potentially different requirements from each of the market outlets
(Assured Food Standards, 2005). While this is the case in many respects, it
does not entirely apply to pesticides, given the different requirements of
different retailers.
Testing for residues
The primary safety/health concern in residues is exceeding the MRLs. All
the retailers interviewed acknowledged that such occurrences are rare and
are more frequent on imported produce. This contrasts with the presence of
residues below the MRLs which through the PSD approval process are con-
sidered safe, but the consumer, perhaps stimulated by media commentary,
considers as being unhealthy and/or unsafe. The broader context is a soci-
ety characterised by a higher level of risk consciousness producing what
has been called a risk society, in which there is an increased recognition
of the potentially negative effects of scientic and technical developments, the
positive effects being increasingly taken for granted (Lowe et al., 2008: 228).
These perceptions then feed back to the retailer in terms of what one retailer
described as This is what our customers have told us they want. This
particular retailer then placed this information into its corporate responsi-
bility framework, leading to the conclusion that what was required was
food without the baggage of pesticide residues. What was less clear was
how the retailer would supply sufcient quantities of food at a competi-
tive price.
Retailer schemes of pesticide classication
Retailers may prohibit the use of particular pesticides that have been
approved under the state regulatory system or for others permit their use
only with the specic consent of the retailer. There are a number of pesticides
that are approved by CRD and prohibited on produce sold by a particular
retailer. The basis of this list differs between retailers. Retailer H, which par-
ticularly emphasizes a green image, had prohibited approximately 130 and
was monitoring another 300. As far as the monitored list was concerned, you
can use them but you must have sound and solid reasons and information
must be readily available. [Its] a way of tightening the screw, putting more
206 Chapter 7
pressure on people. Retailer A started with a list of 79 pesticides it wanted to
prohibit, but found that this would create difculties with suppliers. How-
ever, it is putting continuous pressure on its suppliers: When we sit down
with suppliers to review business as well as a commercial review we will
have a technical overview, look at pesticides issues, what progress theyve
made. Retailer F, who was following the lead of A and H, was compiling a
restricted list to give suppliers a steer, step out of old fashioned chemistry. A
third-party organization was being hired to establish a matrix that could be
used as a basis for decision making and was evaluating 260 pesticides in
terms of that matrix.
However, Retailer C took a somewhat different stance, although it did
have its own classication system:
We wont go further than legislation in terms of we dont like X because Friends
of the Earth dont. We dont like to work that way If you go too far, wed
have problems with availability, then people just switch and youve lost that
trade, availability has to be good in [the] produce market.
Most retailers use a red (prohibited), yellow (requiring permission) and
green (permitted) classication system for pesticides, but Retailer D thought
that this was too coarse a classication and that a more elaborate risk man-
agement system would provide a good management tool for growers. Their
categorization shows how elaborate a private regulatory scheme can be:
1. Red: very high risks, should not be used unless a full case can be made.
Over a 5-year period, about 5% of pesticide actives used outside the UK
would be classied as red.
2. Amber 1: would state risks associated with use, would agree action plan
as to what suppliers should be doing to demonstrate management of risks,
ask for residue data. About 10% of actives.
3. Amber 2: some risks, would keep situation under review. A smaller
proportion of actives than in Amber 1.
4. Amber 3: some issues but nothing that one needs to be concerned about.
5. Green: no issues. Most actives would be either Amber 3 or Green.
How does all this look from the perspective of the grower? A large-scale
Fenland grower is one of the biggest leaf salad suppliers in the country,
specializing in producing lettuce, onions and chicories. They had 17 different
customers and six or seven major different specications; Retailer C had dif-
ferent specications for two contracts. Although they sold their produce to
intermediaries, they stated that [a]t the end of the day we are really dealing
with supermarkets. Given that price differentials were converging, retailers
were keen to get some other point of difference. We were shown two plots of
lettuce being grown for different supermarkets; one had a deeper shade of
red, which was thought to provide a competitive advantage. Retailer A was
seen as driving a lot of innovation in food and as having a very sophisticated
technical department. Retailer H was seen as trying to upgrade its produce
in one fell swoop and lacked a technical department. Retailer A was seen as
a little more understanding. It depends on which representative you are
talking to, different approaches in interpreting what is possible. Nevertheless,
their slogan was if you dont comply, you cant supply. Supermarket
customers make regular visits to the farm and Retailer A had deemed that the
onion washing facility was no longer of a sufciently high standard, illustrating
how retailers can exert inuence on investment decisions by growers.
All supermarket chains test a sample of the produce coming into their
stores for pesticide residues. Even the least well resourced retailer tested
for 328 active ingredients. Retailer C tested about 700 individual products
a year. Testing was focused on products where it was thought there might
be problems, e.g. lettuce grown under protection in December and January.
In general, the greatest pesticide residue problems occurred with imports,
particularly in soft fruits and exotics such as papaya or lychee. Retailer C
commented: The real struggle for [the] retailer is exotics. More familiar
products that are imported can also give problems. Retailer C had a prob-
lem with potatoes from Egypt with several years of MRLs being exceeded.
Because the soil in Egypt is sandy and thinner, a fungicide could get on to
the tuber. An action plan was agreed with the grower, allowing reclassi-
cation of the pesticide from red to amber in the retailers scheme. If the
problem did not reappear after a few years, a green classication would
be granted.
Given that there is a state system for monitoring and reporting on levels
of pesticide residues, why do retailers undertake their extensive testing? One
reason is simply to safeguard against liability claims. As one retailer com-
mented, If we were taken to court because someone died or was seriously ill,
we have to prove due diligence, that we have done everything in our power.
There is also concern, as regulatory systems becoming tighter, about grow-
ers, particularly outside the UK, using pesticides that are illegal. It is less easy
to tackle these problems when they arise outside the UK, although retailers
do make considerable efforts. For example, Retailer A visited suppliers in
Latin America for business reviews that covered progress made on pesticide
issues. In one case, as a result, three amber list pesticides were replaced by
biopesticides.
Retailer C emphasized the importance of managing customer perceptions
of the industry: If you dont tell the customer about pesticides theyre quite
happy. What the customer typically says is: Youre in charge of that, let me
get on with, I dont want to know. The human health risk from pesticides
was negligible but the public dont see it that way, its all about managing the
customers trust. Retailer F agreed that consumer expectations have to be
better managed by us, trust has grown. This is very hard ground.
Category management
In order to understand how retailers control the use of pesticides by suppliers,
it is necessary to understand the basic principles of the system of category
management. Retailer F commented, Interaction is with the packer rather
than the grower. Category management is done for supermarkets by suppliers.
208 Chapter 7
Category management is how supermarkets do things and I cant imagine we
would go back on that. Retailers have rationalized their supply base:
The major supermarkets now deal with just a handful of suppliers in key
product areas (potatoes, root vegetables, brassicas, salads, top fruit, stone fruit
and soft fruit) and take every opportunity to pass responsibility (and associated
costs) for quality control and procurement, storage and distribution upstream
to their key suppliers, in return for which the chosen few are rewarded with
volume growth.
(Fearne and Hughes, 2000: 763)
In essence, responsibility is shifted down the food chain to the grower,
while power, particularly buying power, remains with the supermarket.
Asked if there were any benets in being a lead supplier, a manager at Retailer
C commented: Not really. There is workload on behalf of other suppliers
[and us], they dont get any extra business. We are treating them as industry
experts. The need for the supermarket to retain control, particularly in terms
of traceability, requires reducing the number of suppliers. As Retailer G
explained, The only way to control is by restricting number of suppliers,
gone from 200 to 60 in last three years. We have one supplier for all our
potatoes, I know that I have full traceability.
Retailers make considerable use of the technical expertise of suppliers,
particularly in relation to pesticides as Retailer C explained:
We have lead suppliers, [XYZ] for brassicas, because their technical team
is very good, they understand pesticides far better than I do. I am a facilitator
and coordinator On brassicas, we know strengths and weaknesses of our
supply base on pesticides We know how strong they are on knowledge
and application of pesticides.
The State and the Retailer Governance Systems of Regulation
As discussed in Chapter 6, the links between retailers and PSD were relatively
weakly developed. Often they were conned to attendance at open meetings of
the ACP or perhaps membership of the Pesticides Forum. Retailer D com-
mented: We only interact with PSD if they want specic information from us.
Retailer C was quite critical of PSD, although his statement reects the different
perceptions and priorities of a commercial and regulatory organization:
You could use the retailer muscle to help to move [things] forward. Thats
where PSD and DEFRA should be looking. No sign of movement by PSD, say
we always do it that way, youve got to do it that way In all my dealings
with PSD what really frightens me is that they have no real life experience on
the farm or what the market is saying We give PSD a hard time about being
more robust. We have a lovehate relationship with them at times.
Retailer A had adopted a more proactive approach to PSD and had had
several meetings with them. This supermarkets senior technologist thought
that PSD did their job well, although he thought that the FSA was a lot more
customer focused. However, in relation to the retailers prohibitions list, PSD
had argued Theyre not dangerous, why are you trying to do something
different? and Retailer A had replied Were addressing customer concerns.
Once again this shows the different focus and priorities of the regulatory
agency and the supermarket.
Discussions with PSD conrmed that they had a dialogue with super-
markets but it was limited. Although regulators had to be guarded about
what they said, it was evident that there was some unease about supermar-
kets banning pesticides that had been judged to be safe by the approvals
process. Expressing a personal view, one regulator commented that it makes
it difcult for us, giving the response that lots of pesticides are not safe.
Regulators considered that they had no inuence over what supermarkets
did: This is not something we can do anything about. All pesticides have
gone through [the] approval process and shouldnt cause a problem. We cant
say to Retailer A and Retailer H, you cant do this. Another regulator com-
mented: Retailers have their cake and eat it, they expect impossibly high
standards from farmers who are forced into [the] situation of using them.
There is an evident tension between the role of a state regulatory agency
whose task is to rule whether particular pesticides are safe for people and the
environment and supermarkets driven by the concerns of their consumers
which leads them to ban the use of products deemed safe by the regulator
after a thorough process of scrutiny. As Retailer F commented when asked
how much company policy was driven by the consumer, With pesticides it
is less about what is safe, it is about fear factors.
The Costs and Benets of Private Regulation
These need to be considered from the perspective of the grower, the retailer,
the consumer, the regulator and the environment. The shift of power within
the food chain from growers to retailers has been reected in keener prices
combined with demands for higher quality, and controls on the use of pesti-
cides by retailers are one aspect of that. This increases the complexity of the
task faced by the grower and the demands placed on management time. This
is made more difcult by a shortage of technically qualied individuals able
to manage pesticide use, although this partly reects the level of pay that
the sector can afford. A Fenland grower that was visited had a technical
staff of two, one of whom had been trained up from the yard when it was
evident that she had potential. Many of the costs of the system of private
regulation are thus borne by the grower. Therefore, when a retailer develops
a strategy for sourcing more sustainable products, they as governors of the
supply chain can push all compliance risks and costs down to the supplier
(Thankappan and Marsden, 2005: 56). This can have distributive conse-
quences that marginalize smaller farmers as better capitalized farmers are
more able to adapt to such requirements.
From the perspective of the retailer, imposing additional requirements
on growers is a way of defending their reputation and brand, particularly
against adverse publicity, which is a widely shared concern. For some
210 Chapter 7
retailers it is also a means of demonstrating that they are greener than
their competitors. As Retailer D put it, Its an excellent way of defending
our image if pressure groups come to us and say, What are you going to
do about it? Nothing comes to the shelves at the expense of the consumer,
operator or the environment. Retailer D claimed that it was more able to
take decisions about pesticides than the UK Government because it had a
better database.
The new role of the consumer
At a general level society has become more organized around consumption
as an activity than production. There has been a set of broader changes in
society towards reexive consumption, whereby people think of themselves
as active, discerning consumers whose choices contribute to their sense of
identity. Consumption choices, although structured by retailers, assume a
new signicance:
The growth of afuence has led to a stress on personal development,
and society too is re-oriented towards the values of individuality and
self-expression. With the decline in the dening power of old economic and
political forms associated with workplace, class and nation self-identity
forming has shifted to spheres where individuals have direction and control.
This leads to a growing personal focus on consumption and leisure activities
and the cultural resources and goods that surround them.
(Lowe et al., 2008: 228)
Retailers see themselves as proxies for consumers, and FSA data show
that consumers are concerned about pesticides and have a high level of trust
in information provided by supermarkets. From a supermarket perspective,
mainstream consumers have a limited understanding of pesticides and
display a lack of awareness of regulatory process. More discerning consum-
ers, mainly in the ABC1 categories, are seen as not trusting of regulatory
authorities (Brown, 2005: 18). It is clear that consumers have become slightly
unnerved by the number and regularity of food scares which is in the main
due to the increasing industrialization of food (Brown, 2005: 20).
It might be argued that supermarkets have contributed to this process of
industrialization. Nevertheless, as Retailer F put it, Im very focused on the
consumer; Im not going to take any risks. I am paid by [F] to be focused on
the consumer. The retailer is, of course, focused on the consumer to ensure
that it does not lose the consumer. The retailer is trying to limit damage to its
customer base and not its individual customers. Any loss of reputation may
drive customers to its competitors. It is this that is at the root of the retailers
concern. By developing a greener image, a particular retailer hopes to gain
a competitive edge over its rivals.
This portrayal of the retailer as the proxy defender of the consumer is,
however, more contested than the claims of supermarkets might suggest.
From one perspective, the role of consumer is an increasingly empowering
one that gives the shopper more inuence than he or she enjoys as a voter.
Choice editing, whereby businesses make environmentally and socially
sound sourcing decisions on behalf of their consumers, is therefore a par-
ticularly important trend (Food Ethics Council, 2007: 4). From another per-
spective, the consumer, possessing limited information, is vulnerable to the
marketing ploys of the retailer. There is a clear link here to the depoliticization
narrative. One can extend Hays point (2007: 128) that the marketization of
electoral competition is in danger of reducing the electorate to a series of
atomistic rational consumers who, as atomistic rational consumers will
rationally disengage.
Encouraging or at least permitting supermarkets to take on additional
tasks in the regulation of food safety is consistent with Hays account of
what amounts to an abdication of responsibility by politicians and a transfer
of difcult challenges to experts, informed by a public choice perspective
that markets know best. It might be argued that allowing supermarkets to
construct their own supplementary system of regulation is consistent with
Lord Falconers belief that depoliticization of key decision-making is a vital
element in bringing power close to the people (quoted in Hay, 2007: 93). It
is also consistent with a view that sees citizens primarily as consumers of
public services.
By voting with their purchases, consumers are able to express preferences
for products to be produced in a particular way or even boycott products
from countries of whose policies they disapprove. Micheletti (2003) constructs
an account of political consumerism in terms of a theory of individualized
collective action that combines self-interest and the general good. Political
consumerism represents actions by people who make choices among pro-
ducers and products with the goal of changing objectionable institutional or
market practices (Micheletti, 2003: 2). It may even provide a basis for polit-
ical mobilization: For example, in their search for good soap for their child
they may meet other families in stores who have the same or other similar
problems. The families may decide to pool their private worries and engage
in very concrete, problem oriented, local networks (Micheletti, 2003: 1819).
Given that the majority of food and grocery shopping is still undertaken by
women, Micheletti sees political shopping as a means of empowerment for
women and relates this specically to the case of pesticides. She sees women
as generally more sensitive to risk and inclined to react more negatively to
the use of pesticides on goods needed for their family. Micheletti is aware of
the tensions between political consumerism and more conventional concep-
tions of regulation. She admits that it can be seen as part of a ight from
politics and an ersatz for proper democratic politics and engagements,
whose focus is the political system and government regulatory policy
(Micheletti, 2003: 160).
There is quite a big leap from convenient consumption to political
engagement and empowerment, not least for women. As Bircheld com-
ments (2005: 598), in Polanyis vision [m]arkets are embedded into society
rather than society being submerged into markets. Yet this is the fate that
awaits the political shopper for whom the moment of liberation experienced
212 Chapter 7
when a packet of free-trade coffee is bought may be a transient illusion that
changes neither consciousness nor power structures. As far as the specic
case of pesticides is concerned, but also more generally, one of the difculties
with the notion of the political consumer is that of information asymmetries
between the shopper and the rest of the food chain. As Thankappan and
Marsden note (2005: 45), The danger of proliferating schemes by individual
supermarkets, on top of the existing national assurance programmes and
umbrella initiatives is that the consumer will be left more confused than
ever. Research undertaken by the National Consumer Council, shows that
consumers are completely bafed by the range of schemes, logos and claims
that surround the food industry.
When consumers make their purchase decisions, they are choosing from
a menu of goods provided by the supermarket. The decisions are often made
under time pressure and are largely driven by price. Hence, short cuts to
information on quality are of considerable value. For example, consumers
inuenced by policy considerations place considerable trust in produce certi-
ed as organic. What they often do not realize is that a limited range of
traditional pesticides can be applied to organic produce grown in the UK:
sulfur, soft soap and rotenone. These are either of natural origin (rotenone
and soft soap) or simple chemical elements (sulfur) compared with the more
complex substances typically used as pesticides in non-organic farming.
Retailer F referred to the relative ignorance of consumers about organic pro-
duce: You get some daft responses. If you ask them about organics, they say
no pesticides are required, when you explain there are pesticides applied,
they get very upset. Retailer H commented:
In area of organics there is a perception that it is pesticides free Do you
realize that copper is used heavily and is more harmful than pesticides in
current production? When this comes out sales of organics will collapse, [the]
public will say weve been misled.
The informed consumer using his or her purchasing power to affect policy,
and perhaps even mobilizing with other consumers, is the exception rather
than the rule. The typical consumer is an information taker rather than a
policy maker. The choice of supermarket made by a consumer is inuenced,
apart from the fact that there are often a limited number of supermarkets to
choose from within a given locality, by a mix of price and quality consider-
ations encapsulated in the image cultivated by the supermarket. However,
this is a marketing tool to entice the consumer within the store, not a source
of empowerment.
From the regulators perspective it is operating a rigorous system for
the approval (and withdrawal) of pesticides. By prohibiting the use of
approved pesticides, retailers are implying that the state system is less
than entirely satisfactory, although retailers would claim that they are not
trying to undermine it. As Retailer H put it, We are supportive of the reg-
ulatory system, what we have looked at is a slightly different approach
We are slightly ahead of the legislation, but its a kind of positive approach
as well.
One way of assessing how the private regulatory efforts of retailers
meet environmental needs is to look at how far they encourage the wider
use of biopesticides by growers. In interviews retailers acknowledged the
environmental benets of biopesticides, but were reluctant to take a pro-
active role. A principal exception was Retailer A, which had discussed
alternatives with growers and provided examples of three pesticides on its
amber list replaced with bioproducts. It had also sought to develop links
with companies producing biocontrol agents. However, in general, retail-
ers did not seem to be very well informed about biological alternatives to
synthetic pesticides, welcoming the visit from the project team as an
opportunity to learn more. Indeed, in 2008 one retailer held a conference
on the subject in which the project team gave a presentation as a means of
disseminating the message about their potential contribution to growers.
Retailers were understandably reluctant to recommend particular prod-
ucts to growers. As the environmentally oriented Retailer H commented,
We have to be careful on chemicals and biologicals, make sure we dont
start saying to the grower you should use product x rather than product y.
Retailer D commented: We always have to ask ourselves what effect does
it have on us commercially in terms of costs and yields? We are always
driven back to costs.
Conclusions
Using their contracts with growers for leverage, large supermarket chains
have constructed often elaborate systems designed to prohibit or restrict the
use of pesticides permitted by the state regulatory system. The regulatory
state model has been widely criticized for its centrist conception of state
power (Thankappan and Marsden, 2005: 56). The advantage of such a
system is that its objectives are transparently stated and it seeks to apply
regulations consistently to different actors in accordance with the stipulated
goals. This is in contrast to the variability of standards between retailers that
imposes additional costs on growers. There is also scope in the regulatory
state for regulatory innovation in terms of facilitating the registration of more
environmentally sustainable pest control agents such as biopesticides.
The private regulatory system developed by supermarkets can be
portrayed as empowering the consumer. Supermarkets are attempting to
respond to consumer concerns, but it is evident from our interviews that
they are also trying to shape and manage those concerns. Above all, as prot-
making organizations they are driven by a search for commercial advan-
tage. A technical manager in a supermarket chain faces the challenge of
doing all the work to ensure that the product is produced safely, protects
the environment and biodiversity, maintains quality standards and avail-
ability at a price we need to sell it on to keep our prots. If resources are
devoted to promoting environmentally safer actives such as biopesticides,
this is the result of a commercial positioning of a particular retailer like A.
Initiatives are always going to be inuenced by commercial considerations,
214 Chapter 7
not least because sustainability as a set of quality standards may provide
leverage for large enterprises to control markets and raise barriers to com-
petition (Thankappan and Marsden, 2005: 56).
In some respects, the objectives of retailers are contradictory. They would
like to see residue-free fresh produce, but this is inconsistent with the need
for a continuous supply of competitively priced goods that meet a particular
specication. Above all, there is a tension between this objective and avail-
ability of produce which is a major commercial driver as lack of availability
can lead to loss of market share. Some of the most challenging residue prob-
lems arise with imported produce, but as Retailer C put it, Were still going
to need strawberries at Christmas; it would be a brave retailer who said were
not going to do things out of season.
A polemical literature has emerged criticizing the displacement of retailers
in the contemporary British political economy (Blythman, 2005; Simms,
2007). However, although some specic retailer practices may be curbed by
the Competition Commission and the proposed supermarket ombudsman,
retail concentration and the leverage it gives them on the food chain are not
going to go into reverse. The indication is that the market will concentrate
further, with the large multiple stores increasing their shares through new
openings, and possibly through mergers (Clarke et al., 2002: 154155). What
is needed is a more sophisticated debate about the roles of supermarkets that
neither demonizes them nor portrays them as liberators of the consumer. In
the specic case of pesticides regulation, there needs to be a more structured
dialogue between the supermarkets and CRD.
Retailers are able to exert their substantial inuence in the food chain to
inuence grower decision making in order to protect their brand reputation.
It should be noted that there is considerable variation in the practices of
retailers, inuenced by the resources available to them, their analysis of their
market position and their assessment of the social composition of their cus-
tomers and their purchasing preferences. Some retailers are more proactive
in relation to pesticides than others.
What in practice amounts to a supplementary approval system contributes
to misconceptions over pesticide safety by in effect the retailers running their
own approval system. This gives the perception that not all approved pes-
ticides are safe. Their standards can be very difcult for growers to meet
and can be contradictory. For example, they would encourage the use of
natural predators but would reject any pre-packed foods that have insects
in them.
The supplementary system of private governance for pesticides does
pose some challenges. First, different retailers have different requirements,
enhancing the complexity of decision making for growers and producing in
effect what is a non-standardized system of pesticide use. Second, retailers
prohibit rather than promote alternatives such as pesticides, although they
would reasonably argue that they cannot endorse particular products. Third,
retailers lack public accountability and their actions are often driven, quite
legitimately, by a desire to gain an edge over their competitors rather than by
considerations of public policy.
References
Assured Food Standards (2005) Frequently Asked Questions. Available at: http://www.
assuredproduce.co.uk/AProduce/faq.asp (accessed June 2005).
Bircheld, V. (2005) Jos Bov and the globalisation countermovement in France and
beyond: a Polanyian interpretation. Review of International Studies 31, 581598.
Blythman, J. (2005) Shopped: the Shocking Power of British Supermarkets. Harper
Perennial, London.
Brown, C.M. (2005) Retail perspectives on crop production. In: The BCPC International
Congress Proceedings: 2005, Vol. 1. British Crop Protection Council, Alton, UK,
pp. 1722.
Burnham, P. (2001) New Labour and the politics of depoliticisation. British Journal of
Politics and International Relations 3, 127149.
Clarke, R., Davies, S., Dobson, P. and Waterson, M. (2002) Buyer Power and Competition
in European Food Retailing. Edward Elgar, Cheltenham, UK.
EurepGAP (2006) Eurepgap Protocol for Fresh Fruit and Vegetables. Available at: http://
www.eurepgap.org/Languages/English/about.html (accessed June 2006).
Fearne, A. and Hughes, D. (2000) Success factors in the fresh produce supply chain:
insights from the UK. British Food Journal 102, 760772.
Food Ethics Council (2005) Power in the Food System: Understanding Trends and
Improving Accountability. Food Ethics Council, Brighton, UK.
Food Ethics Council (2007) Food Miles or Food Minutes: Is Sustainability All in the
Timing? Food Ethics Council, Brighton, UK.
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food chains: roles for social science. Food Science and Technology 19, 226233.
Marsden, T., Flynn, A. and Harrison, M. (2000) Consuming Interests: the Social Provision
of Foods. UCL Press, London.
Marsden, T., Lee, R., Flynn, A. and Thankappan, S. (2009) The New Regulation and
Governance of Food: Beyond the Food Crisis? Routledge, Abingdon, UK.
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Collective Action. Palgrave-Macmillan, Basingstoke, UK.
PSD (2006) Pesticides and the Environment: a Strategy for the Sustainable Use of Plant
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Relationships, Accountability, Sustainability and Society, Cardiff University, Cardiff,
UK.
8
Conclusions
This book originated from a UK Research Council-funded RELU programme
on the Rural Economy and Land Use (RELU) which attempted to address
the frustrations of natural scientists who struggle with the apparent dif-
culty of bringing biopesticides to market when their biological intuition
suggests they are such obvious solutions to pest problems. In an attempt to
unravel the problem and come forward with solutions, natural and social
scientists joined forces. The social scientists fell into two groups. Economists
focused on a series of economic barriers to adoption of biopesticides, while
political scientists considered the system for their regulation is principally at
fault. As we have seen in the preceding chapters it is clearly more complex
than that. In this concluding chapter we try to draw together some of the
emerging thoughts.
There is a very large number of plant species cultivated throughout the
world that are used to feed the human population and their livestock, for
bres and building materials or for fuel. We have focused primarily on food
crops but the emerging principles apply to all crops. A relatively small num-
ber of plant species such as rice, wheat and maize are cultivated to produce
the staple foods for the world population, while a huge number of plant
species provide the greater nutritional variety and interest in diets. The yield
or quality of each of these plant species, whether or not it is a staple, is
limited at some stage during its cultivation by a community of invertebrate
pests, diseases and weeds, collectively referred to as pests. The increasing
world population and its increasing afuence and urbanization are placing
ever greater strain on the world food production system to produce and dis-
tribute more and more food in a sustainable way to nourish that population
adequately. Increased food production is achieved rst through improve-
ments in agronomy to achieve greater yields per unit area and second by
minimizing waste and spoilage. The control of pests in the eld contributes
to the maximization of yield and reduces spoilage postharvest. The current
Conclusions 217
debate over the risk to food security is pushing all these issues higher up the
political agenda. Regulation needs to take account of the benets as well as
the costs of growing crops using plant protection products.
The solution to an impending food security crisis is potentially at odds
with the policies on sustainability that propose that mankind treads lightly
on the environment, does not aggravate and ideally mitigates climate change
and its impacts, and does not deplete biodiversity further. Modern large-scale
agriculture does have the potential with large machinery, modern plant
varieties and agrochemicals to feed the world, but at what cost? It has been
set out earlier how crops are complex ecological communities and that the
manipulation of different components of these communities to the benet of
the crop and of mankind should be approached as an exercise in applied
ecology, rather than the application of technology despite the ecology.
Each crop pest also has its own community of predators, parasites and
diseases that limit their numbers and vigour. Historically mankind has
relied largely on these interactions to achieve some control, yet devastating
crop losses occurred from time to time. Over the last 100 years there have
been major advances in our understanding of the complex interactions
between the crops we cultivate and their biotic environment and of the
potential to manipulate this environment to the benet of the crop. At the
same time a sophisticated chemical industry has developed that discovers,
manufactures, distributes and sells pesticides that control many crop pests.
Coincident with this some regions of the world, particularly the developed
North, have experienced dramatic globalization of food markets, initially of
the staple crops and recently of nearly all crops. This has politicized trade
and regulated aspects of food production. At this point further challenges
emerge due to the different spatial and temporal scales of the political and
economic landscape.
The rapid growth of the global agrochemical industry after World War II
focused effort on products for crops grown on large acreages (mainly staple
and bre crops) where sales would be large and prots maximized. This
remains the case to this day, but with the hope or expectation these products
will also nd use on at least some of the very many minor crops, many of
which are signicant contributors to a balanced diet. In the developed world
the sale and use of pesticides are more closely regulated than for any other
chemicals including pharmaceuticals. The stringent conditions to which
pesticides have to comply have evolved as our understanding of the environ-
mental and human health impacts of these chemicals in particular have
developed. Initially large numbers of products emerged which found their
way into every corner of agricultural production. As regulations have
matured and become tighter, the pipeline of new chemistry has declined
at the same time as products are being withdrawn from the market as they
no longer meet the more stringent regulations or are now uneconomic to
produce and market. The consequence is there remain chemical solutions,
though a more limited choice, to many pests on the broad-acre staple crops,
but many minor crops now have very few chemicals available to control their
pests, especially given that a product may not work well on some soil types.
218 Chapter 8
Though these differences have always been apparent since pesticides were
rst invented, they are now more evident than ever.
Intuitively, the manipulation of all the biotic interactions within the
cropping environment, along with the judicious use of pesticides where they
are available, in IPM must be a solution. This is what the revised European
regulatory regime enacted in 2009 is based upon. Yet this is where the
challenges really are, and there are many of them manifesting themselves on
different scales. Many biological solutions require detailed research to
develop the biological x, but also considerable on-farm management skill
to implement. Second, biological interactions are specic to two or at most a
very small number of species, so novel solutions need to be developed for
almost every croppest combination. This contrasts greatly with the chemi-
cal approach where modes of action dictate that a chemical will be effective
against a far wider range of pests. The biological solutions are very resource
intensive while only delivering niche solutions, which the economics of the
global agro-chemical industry nds it difcult to reconcile. Additionally the
regulatory process has evolved to accommodate the chemical model and is
less easily applied to a multitude of niche biological solutions.
The IPM approach will include a number of pest management methods
in a portfolio that in many cases may be complements, or substitutes. Here,
complementarity between techniques may take the form of relationships
that are simple additive (site and time specic), spatial additive (eld mar-
gin to centre, ground level to crop canopy activity, etc.) or temporal additive
(early to late season active), and any of these relationships may serve to
increase mean levels of pest control efcacy. Furthermore, the combination
of technology sets that include functional substitute techniques,
1
by build-
ing resilience into systems, could prove highly effective at controlling the
variance of overall pest control function.
The acceptance of the portfolio concept in which a number of control
options can be integrated together in different combinations to deliver an
equivalent outcome has to be complemented by a high level of knowledge
and management skill to implement in an economically acceptable way.
Some technologies group together due to their similarity of approach and
methods of application. A farmer may therefore adopt a number of approaches
that are similar, but be constrained by the economics of application and a
risk-averse nature from stepping into the next technology portfolio. This
alone may constrain the step away from a chemistry-based approach to pest
control into an IPM strategy with many components.
Individual farmers may struggle to acquire and interpret the knowledge
required to implement complex portfolio approaches. In much of the devel-
oped world there is declining investment in agricultural education and
research, and frequently the complexities of the technologies involved are
becoming greater than the individual small business can absorb. In devel-
oped countries there is increasing polarization of farm business size with
small family farms struggling to accommodate technological advances and
deliver a prot. This contrasts with those farm businesses that are expanding
through amalgamation and takeover and relish new technology, particularly
Conclusions 219
in the IPM arena. Their large size enables them to employ the specialist
technical personnel who understand and implement the developing and
increasingly complex technology.
We have therefore arrived at a failure in both the regulatory process
and traditional economic models that cannot accommodate satisfactorily
biological products, including biopesticides, for application to minor crops.
So perhaps biopesticides are niche solutions to niche problems. This is
compounded further by the nature of the market for minor crops, many of
which are the fruit and vegetables of our diet that are sold fresh with exact-
ing quality standards. Individual units of harvest of predened size, such
as an individual apple or a head of lettuce, are marketed. The production of
staple crops from broad-acre agriculture is frequently processed prior to
human consumption or is used as animal feed or non-food crops, so total
yield is of greater importance with the quality of individual units of crop
being subordinate to it. The market price is determined by the global com-
modity markets.
To address the minor crops market, a collection of new biological technol-
ogy companies has emerged since the early 1990s in an attempt to deliver to
these niche markets, frequently in clearly dened and modest geographical
regions. These companies are characterized as SMEs, although in practice
they are often micro enterprises with just a few employees and are frequently
driven by biological entrepreneurs with a passion for what they believe bio-
logical solutions can deliver. These companies invariably have very limited
budgets and individually very little inuence by comparison with the more
global chemical industry. Some of these small companies have formed the
IBMA to give themselves more political inuence and a role as stakeholders
in policy debates. However, the market size for individual products will
invariably remain small, with a few exceptions, due to the minor crops at
which many products are targeted.
The targets in Europe for many of the biological products are pests of
minor fruit and vegetable crops which have largely been grown in an
unsubsidized agricultural economy, subsidies having been directed primar-
ily towards broad-acre staple crops and livestock. Consequently producers
of minor crops have developed a much greater awareness of and a close
working relationship with their markets, particularly the multiple retailers.
This reveals yet another David and Goliath relationship. The sale of fresh
produce by multiple retailers is very protable. We have seen through our
interviews with retailers their sensitivity (driven in part by the nancial
sector) to maintenance of market share, defence of brands and reputation as
well as shareholder condence, all of which could be adversely affected
through marketing of inferior-quality fresh produce. Of particular impor-
tance to them is the detection of pesticide residues on produce or the pres-
ence of any pest or foreign bodies with the produce. Retailers apply
considerable pressure on their suppliers to ensure pesticide residues are not
detected. Some individual producers and marketing groups may make con-
siderable investments in technology and skilled management resources to
manage pesticide applications with great care and to incorporate biological
220 Chapter 8
solutions to pest control into their production process, but the risk remains
theirs and not the retailers. The retailers, with a few exceptions, do not
concern themselves with the regulation and promotion of pesticides and
biological alternatives, leaving it to the manufacturers and the farmers to
drive the need for products for use on minor crops. However, the pesticide
usage constraints placed on suppliers by some retailers, particularly the need
to select chemical control options from a restricted list of pesticides, does
create a private system of regulation which supplements and perhaps
undermines the public system.
The regulators in Europe and the USA do seem to be rising to the challenge
to facilitate the registration of biopesticides by establishing specialist teams
to share their knowledge with manufacturers to ease the collation of all rele-
vant data. But could biopesticides be a perfect substitute for chemical pesti-
cides? Arguably, no! Their efcacy, as measured by percentage kill, their
speed of action, as measured by time to achieve 50% kill, and their reliability,
as measured by the variance of their kill rate, are generally far less attractive
than the chemical alternative. Sole use of biopesticides in a mono-technology
approach would probably be economically suboptimal at least in private cost
terms. More generally, the UK ACP (2003) report states that:
Many of the alternative control tactics are only partially effective or have a very
selective action against certain pests. They may therefore give inadequate
control when used alone.
While used in isolation, the efcacy of many IPM components does appear
less attractive than that of chemical control. One may therefore caution
against the search for biopesticides as silver bullets and suggest that com-
bined, or integrated, systems approaches are more suitable. There is evidence
that efcacy of IPM improves with an increased number of biocontrol options
used together.
Biopesticides could prove to full a number of key roles in IPM portfolio
approaches. However, consideration of portfolio technology adoption,
particularly in the case of mixes of knowledge or system technologies
( sometimes referred to as disembodied technology) and capital or material
product technologies (referred to as embodied technologies), is complex.
This distinction is important for two phases of the technology development
process. First, only embodied technologies are likely to be brought forward
to market by private companies. While private companies can register
patents and capture rents from the sale of products which embody a techno-
logical advance, individual users are not excludable from disembodied
knowledge technologies. Second, private companies have much to gain from
the extension and market development of embodied technologies while only
government and NGOs are likely to promote system or disembodied techno-
logical advances but both probably lack the resources for the task. Bio-
pesticides, alongside pheromones, plant extracts and antifeedants, can be
considered as embodied technologies and might nd their commercial cham-
pions. However, other disembodied IPM portfolio technologies are unlikely
to be championed by the private sector unless those companies recognize the
Conclusions 221
true portfolio nature of IPM upon which their own sales rely. The adoption
problem becomes more severe when there are both scale economies and
network externalities in the technology adoption complex.
There has been a considerable decline in the number of active ingredients
available to the broad-acre farmer although there are generally still many
chemical solutions available. Many minor crops are in a very different posi-
tion with no chemical solutions for many pests. Through economic necessity,
growers have been driven to use biological alternatives. A good example is
the tomato and cucumber growers of north-west Europe, who grow their
crops in glasshouses. Initially resistance to acaricides drove the introduction
of predatory mites to control the two-spotted spider mite. There was then a
need for further biological solutions for other pests, but the real economic
push for complete biologically based integrated control came with the
introduction of bumblebees to pollinate the crop, which gave even fruit set.
Biological solutions were then driven by the need to preserve the valuable
pollinators. This illustrates the need for the appropriate economic drivers at
the scale of the farm if biological solutions are to be deployed.
A further scale consideration is the availability of technologies to produce
adequate quantities of biopesticdes, or other biological control products, for
the application to millions of hectares of broad-acre crops. This is well
illustrated by the control of the soybean caterpillar with Anticarsia gemmatalis
NPV in Brazil, which proved to be highly effective, but the inability to pro-
duce sufcient quantities of virus in vivo has put the whole technology and its
wider reputation at risk. Therefore, until there are major technological
advances that can shift the production of more biological products from in
vivo-based systems to those of industrial chemical production, their use may
be trapped within minor crops.
The prime focus of the discussion so far has been to make suitable products,
including biological agents, available for use, particularly on minor crops.
The role this has in the wider delivery of a secure food supply is less clear.
Government and regulator objectives have centred on ensuring products are
safe to human health and cause no damage to the environment while to date
taking less account of delivering food security or safe water supplies,
although the agenda is rapidly shifting. It opens up the question of what
agricultural land is for. Does it have functions beyond the supply of food?
The answer to this is certainly yes. Land cultivation impacts on the release
and sequestration of greenhouse gases, modies the ow of water through
the water cycle, alters biodiversity to name just a few. To deliver all these
requires a greater joining up of the regulatory processes so land managers
can deliver all we expect from land.
Compared with the macro agendas of climate change and food security,
the micro agenda of biocontrol products may seem to be relatively insigni-
cant. Nevertheless, they offer a key element of the IPM approach that is now
at the centre of the EU regulatory agenda and is likely to play an important
role in climate change adaptation, a topic that has been relatively neglected
at EU level compared with climate change mitigation. The future develop-
ment of the Common Agricultural Policy is also likely to prove an important
222 Chapter 8
context for the development of sustainable agriculture, for example in rela-
tion to the signals provided by agri-environmental schemes that provide an
economic stimulus for the introduction of new technologies.
This book has also provided a lens to examine some wider issues in
contemporary society. Can regulators overcome their inherent risk averseness
to facilitate the development of new products which offer more sustainable
solutions? Our research suggests that they can, given a suitable set of condi-
tions and stimuli. In a world in which power has owed down the food chain
to retailers as proxy representatives of the consumer, how can they be encour-
aged to use their market power to support sustainable solutions? Part of the
response to this challenge would involve their more effective integration in
the relevant policy networks. Above all, our research has shown that collab-
oration between economists, political scientists and biological scientists can
generate insights and understandings that would not be provided by work
based on just one discipline.
Note
1
Functional substitutes are often, rather derogatorily, referred to as functional redundance
in the applied ecological literature.
Reference
ACP (2003) Final Report of the Sub-group of the Advisory Committee on Pesticides on
Alternatives to Conventional Pest Control Techniques in the UK: a Scoping Study of
the Potential for Their Wider Use. Advisory Committee on Pesticides, York, UK.
223
Index
Acarina 2325
Adelges tsugae 47
Advisory Committee on Pesticides
(ACP) 4
Africa
integrated pest management 6062
pushpull strategy 108
African palm weevil 108
agri-environmental policy (AEP)
135144
alien species 4548, 7980
Diabrotica virgifera 4647
allelochemicals 101102
Anticarsia gemmatalis 87, 221
aphids 2122
cotton aphid 89
arable crops 5960
Arthrobotrys species 95
Ascomycota 8890
Aspergillus avus 28
augmentation biological control 7779
inoculation approach 78, 79
inundation approach 7778
Bacillus 94
subtilis 94, 95
thuringiensis (Bt) 58, 78, 8283,
104106
genetically modied crops
8386
safety 117
bacteria 29, 8283
Beauveria bassiana 89, 104, 105106,
117118, 120
Bemisia tabaci 22
bioherbicides 9798
biological control agents 52, 6264,
7375
microbial agents 7576
invertebrate control 8191
nematode control 95
plant pathogen control 9297
regulation 108116
safety 116120
strategies 7681
weed control 9798
natural compounds 51, 99
microbial 100101
plant derived 99100
safety 120121
semiochemicals 103
natural enemies 37, 72, 7375,
104
escape hypothesis 4748
harlequin ladybird 119
strategies 7681
strategies 7677
augmentation biological control
7779
classical biological control
7980
224 Index
biological control agents continued
strategies continued
conservation biological control
8081
introduction 7980
biopesticides 2, 35, 52, 7173
adoption 4, 198199
integrated pest management
103108, 219221
nematode control 95
regulation 108116
safety 116120
strategies 7681
weed control 9798
microbial 100101
plant derived 99100
safety 120121
semiochemicals 103
policy networks 177178, 194195
biopesticides 178179
change 182187
components 179182
institutional reform 193194
regulatory innovation 187192
regulation 58, 7273, 108116,
148149
CRD 6, 8, 9, 135, 149153,
154158, 161, 173174,
179194, 208209
EU 5, 80, 158169, 182
innovation 810, 187192
OECD 171172
policy networks 177195
retail governance 198199
UK 6, 8, 149158
USA 8, 169171
WHO 171172
retail governance 201204, 210214
cost 209210
pesticide classication 205207
residues 205
standards organizations
204205
supply chain 207208
safety 114118
botanicals 120121
semiochemicals 120121
biostimulants 155156
Blacks ve worlds 187191
botanicals 99100
safety 120121
Brazil 87
broad-acre crops 5960
broad-spectrum activity 3637
Bt crops 8386
Canada 8788
carbamates 34
cassava 9091
Chemicals Regulation Directorate (CRD)
6, 8, 9, 135, 149151, 161, 173174
biopesticides scheme 157158
cost 158
efcacy testing 156157
enforcement 154156
maximum residue limits (MRLs)
152153
minor use crops 151152
off-label approvals 152
pressures 191192
retailers 208209
China 86
Claviceps 2728
climatic zones 161162, 164166
Coleoptera 21
Collego 9798
Colletotrichum gloeosporioides 9798
Colorado potato beetle 23, 105106
competition 4344
Coniothyrium minitans 105
control 13
adoption 4, 198199
103108, 219221
natural compounds 51, 99101,
103
integrated pest management (IPM)
3, 16, 3941, 6264, 144145,
218221
adoption 5355, 131135
Index 225
agri-environmental policy
135144
biological control agents 52,
6264, 7375
biopesticides 7576, 103108,
219221
crop protection 4950, 53
developing countries 6062
economic thresholds 4849
eld vegetable crops 5758
5960
greenhouse crops 5557
103
72, 7381, 104, 119
orchard crops 58
population dynamics 4149
pesticides 3233, 216218
carbamates 34
development 3335, 39
dichlorodiphenyltrichloroethane
23, 34
fungicides 35
herbicides 35
organochlorine 34
organophosphate 3435
problems with 3538
pyrethroids 34, 100
withdrawal of 39, 160
cotton
aphids 89
genetically modied (GM) crops
5960, 84, 86
61
cottony cushion scale 79
adoption 4, 198199
103108, 219221
103
cultural practices 5051
genetic methods 5253
3, 16, 3941, 6264, 144145,
218221
adoption 5355, 131135
135144
biological control agents 52,
6264, 7375
219221
5960
103
72, 7381, 104, 119
orchard crops 58
carbamates 34
23, 34
fungicides 35
herbicides 35
organochlorine 34
problems with 3538
pyrethroids 34, 100
physical methods 51
plant breeding 5152
selective pesticides 50
Crop Protection Management Plans
(CPMPs) 138139
Cuba 106107, 114
cultural practices 5051
customers 210213
Cydia pomonella granulovirus (CpGV)
87, 105
Denmark 167168
226 Index
DeVine 9798
Diabrotica virgifera 4647
dichlorodiphenyltrichloroethane (DDT)
23, 34
Diptera 21
disease 2526
bacteria 29
fungi 2628
microbial control 9293
antagonism 9395
induced host resistance 9597
nematodes 30
oomycetes 2829
Phytophthora infestans 3031, 48
vectors 2123, 24
viruses 29, 8688
vectors 24
downy mildews 2829
economic
adoption 131135
thresholds 4849
entomopathogenic nematodes 7475,
9192
Entomophaga maimaiga 90
Entomophthorales 8889
Entry Level Stewardship scheme (ELS)
137144
environmental conditions
pest population dynamics 43, 45
environmental persistence 36
Environmental Stewardship scheme
137144
ergot 2728
essential oils 99100
EU
8385
regulation 5, 80, 158159
biopesticides 166
climatic zones 161162,
164166
Denmark 167168
directive 91/414 159160,
162163
EFSA 159160
EPPO 161
loss of active ingredients 160
Netherlands 168169
policy networks 182
reform 162169
shortcomings 160162
Sustainable Uses Directive
163164
Water Framework Directive
167
European Crop Protection Association
(ECPA) 154, 163
European Food Safety Authority (EFSA)
159160
European and Mediterranean Plant
Protection Organization (EPPO)
161
European spruce sawy 8788
experimentation 1115
model systems 1315
Food Safety Act (1990) 201
forecasting
environmental conditions 43
Frankliniella occidentalis 22, 38
fungi 88
control 35
entomopathogenic 8891, 117
pathogens 2628
fungicides 35
genetically modied (GM) crops 5960
Bt 8386
Gilpinia hercyniae 8788
GlobalGAP 204205
glyphosate 5960
government policy
135144
innovation 810
change 182187
components 179182
regulatory innovation
187192
regulation 58, 7273, 108116,
148149
Index 227
CRD 6, 8, 9, 135, 149153,
154158, 161, 173174,
179194, 208209
EU 5, 80, 158169, 182
OECD 171172
UK 6, 8, 149158
USA 8, 169171
WHO 171172
retailer power 200201
gypsy moth 90
Hampton review 194
Hemiptera 21, 22
hemlock woolly adelgid 47
herbicides 35
5960
Heterorhabditis 74, 105
Higher Level Stewardship scheme
(HLS) 137
human safety 32, 38, 115116
Hymenoptera 21
Icerya purchasi 79
India 61
industrial farming 3335, 216218
insects 2023
aphids 2122
Colorado potato beetle 23
cotton aphids 89
insecticide resistance 3738
locusts 21, 22, 8990
bacteria 8283
Bt genetically modied crops
8386
fungi 8891
viruses 8688
microbial 100101
plant derived 99100
semiochemicals 103
natural enemies 37, 72, 7375, 104
strategies 7681
carbamates 34
23, 34
organochlorine 34
problems with 3538
pyrethroids 34, 100
sawies 21
spittlebugs 89
thrips 21, 22
whitey 22
integrated pest management (IPM) 3,
16, 3941, 6264, 144145,
218221
adoption 5355, 131135
135144
biological control agents 52, 6264,
7375
219221
5960
nematode control 95
strategies 7681
weed control 9798
microbial 100101
plant derived 99100
semiochemicals 103
natural enemies 37, 38, 72, 7375, 104
strategies 7681
228 Index
integrated pest management continued
orchard crops 58
competition 4344
environmental conditions 43,
45
life history strategies 4243
predation 44
size increase 4448
intensive farming 3335, 216218
interdisciplinary working 1011
complex systems 1213
individualistic fallacy 1315
Oedipus effect 11
International Biocontrol Manufacturers
Association (IBMA) 155156,
162163, 164, 179181
invertebrates
insects 2023
aphids 2122
Colorado potato beetle 23
cotton aphids 89
insecticide resistance 3738
locusts 21, 22, 8990
pesticides 3235, 39, 100,
216218
sawies 21
spittlebugs 89
thrips 21, 22
whitey 22
8386
bacteria 8283
fungi 8891
viruses 8688
mites 2325
molluscs 25
microbial 100101
plant derived 99100
semiochemicals 103
strategies 7681
Irish famine 3031
Lepidoptera 21
Leptinotarsa decemlineata 23, 46
locusts 21, 22, 8990
Lymantria dispar 47, 90
Magnaporthe grisea 9697
Mahanarva species 89
maize
59, 8386
western corn rootworm (WCR)
4647, 84
maximum residue limits (MRLs) 152153
Metarhizium anisopliae 8990, 117118
8386
bacteria 8283
fungi 8891
viruses 8688
nematode control 95
antagonism 9395
regulation 108116
safety 116120
strategies 7677
7779
7980
8081
introduction 7980
weed control 9798
mites 2325
model
adoption 133135
systems 1315
molluscs 25
microbial 100101
plant derived 99100
safety 120121
semiochemicals 101
allelochemicals 101102
Index 229
pheromones 102103
strategies 7677
7779
7980
8081
introduction 7980
neem oil 99100
nematodes 30
entomopathogenic 7475, 9192
Neozygites species 81, 89, 9091
Netherlands 168169
nicotine 99
northern jointvetch 9798
Oedipus effect 11
oomycetes 2829
orchard crops 58
Organic Entry Level Stewardship
scheme (OELS) 137, 140
Organisation for Economic Co-operation
and Development (OECD)
171172
organochlorine (OC) 34
organophosphate (OP) 3435
Orthoptera 21, 22
carbamates 34
(DDT) 23, 34
fungicides 35
herbicides 35
3, 16, 3941, 6264, 144145,
218221
adoption 5355, 131135
135144
219221
103
orchard crops 58
organochlorine (OC) 34
organophosphate (OP) 3435
problems with 35
broad-spectrum activity 3637
environmental persistence 36
pest resurgence 37
resistance 3738
secondary pests 37
toxicity 38
pyrethroids 34, 100
regulation 58, 7273, 108116,
148149
CRD 6, 8, 9, 135, 149153,
154158, 161, 173174,
179194, 208209
EU 5, 80, 158169, 182
OECD 171172
UK 6, 8, 149158
USA 8, 169171
WHO 171172
safety 32, 38
tax 167168
Pesticides Safety Directorate (PSD) see
Chemicals Regulation
Directorate (CRD)
Phasmarhabditis hermaphrodita 92
pheromones 102103, 107108, 120121
Phytophthora 28
infestans 3031, 48
palmivora 9798
plant breeding 5152
plant pathogens 2526
bacteria 29
fungi 2628
microbial control 9293
antagonism 9395
230 Index
plant pathogens continued
nematodes 30
oomycetes 2829
vectors 2123, 24
viruses 29, 8688
vectors 24
Pochonia chlamydosporia 95
change 182187
components 179182
pressures 191192
political science 1011
complex systems 1213
individualistic fallacy 1315
Oedipus effect 11
competition 4344
environmental conditions 43, 45
life history strategies 4243
predation 44
size increase
alien species 4548
agricultural disturbance 4445
emerging pests 48
environmental conditions 45
resource concentration 44
portfolio economies 132133
potato
Colorado potato beetle 23, 105106
predation 44
probenazole 9697
production 76, 107
Pseudomonas 94
Puccinia
chondrillina 98
graminis f.sp. tritici 48
pushpull strategy 108
pyrethroids 34, 100
pyrrolizidine alkaloids (PAs) 107
regulation 58, 7273, 108116,
148149
CRD 6, 8, 9, 135, 149151, 161,
173174
cost 158
enforcement 154156
maximum residue limits
152153
retailers 208209
EU 5, 80, 158159
biopesticides 166
climatic zones 161162,
164166
Denmark 167168
directive 91/414 159160,
162163
EPPO 161
EFSA 159160
loss of active ingredients 160
Netherlands 168169
policy networks 182
reform 162169
shortcomings 160162
Sustainable Uses Directive
163164
Water Framework
Directive 167
pressures 191192
OECD 171172
change 182187
components 179182
UK 6, 8, 149158
see also Chemicals Regulation
Directorate (CRD)
USA 8, 169171
WHO 171172
residues 205
resistance 3738
retailers 181, 198199
CRD 208209
Index 231
customers 210213
power 199201
regulation 201204, 210214
cost 209210
pesticide classication 205207
residues 205
standards organizations
204205
supply chain 207208
rice 9697
risk 132
Rodolia cardinalis 79
Rural Economy and Land Use (RELU)
programme 23
safety
botanicals 120121
human 32, 38, 115118
sawies 21
safety 120121
Septoria tritici 39
single farm payment 136137
skeleton weed 98
slugs 25
snails 25
soybean 87, 221
spider mites 104
Spinosad 100
spittlebugs 89
spruce sawy 8788
standards organizations 204205
Steinernema 105
carpocapsae 105
feltiae 9192
riobrave 105
straight-chain lepidopteran pheromones
(SCLPs) 103, 120121
stranglervine 98
sugarcane 89
sustainable farming 13
Sustainable Uses Directive 163164
systemic acquired resistance 9597
thrips 21, 22
Thysanoptera 21
tomato 56, 58
Trichoderma 93
harzianum 93
UK
Advisory Committee on Pesticides
(ACP) 4
135144
Chemicals Regulation Directorate
(CRD) 6, 8, 9, 135, 149151,
161, 173174
cost 158
enforcement 154156
maximum residue limits
152153
regulatory innovation
187192
retailers 208209
entomopathogenic nematodes 75
Environmental Stewardship scheme
137144
adoption 140144
retailers 199201
USA
cotton aphid 89
gypsy moth 90
hemlock woolly adelgid 47
135136
Neozygites species 81
regulation 8, 169171
western corn rootworm (WCR)
4647
Varroa destructor 2425, 38
vectors 2123, 24
virus 29, 8688
vectors 24
232 Index
Water Framework Directive 167
weeds 3132
microbial control agents 9798
western corn rootworm (WCR) 4647
western ower thrips 22, 38, 104
wheat 39
whitey 22
World Health Organization (WHO)
171172
yield 12
integrated pest management 5355
loss 1920
Zygomycota 8889

Biopesticides - Pest Management and Regulation

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Pest Management and Regulation

Multiple management tactics integrated for a single group of pests (arthropods,

produce an antibiotic-like substance, active in

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