On the ethics of biological control of insect pests

Agriculture and Human Values 14: 283–289, 1997. c 1997 Kluwer Academic Publishers. Printed in the Netherlands. On the ethics of biological control of insect pests Jeffery W. Bentley1 and Robert J. O’Neil2 1 Cochabamba, Bolivia; 2 Purdue University, West Lafayette, Indiana, USA Accepted in revised form June 12, 1997 Abstract. Of the four types of biological control, (1) natural, (2) conservation, (3) augmentation, and (4) importation), ethical concerns have been raised almost exclusively about only one type: importation. These concerns rest largely on fears of extinction of animal species. Importation biological control is a cost-effective alternative to chemical control for basic food crops of resource-poor farmers. Regarding the other types of biological control, natural biological control is not consciously manipulated by humans. Augmentation has some technical concerns, but is generally an environmentally-sound, viable alternative to chemicals and offers local employment. Conservation can help empower farmers to preserve native species, while saving labor and money and reducing chemical insecticides. Key words: Biological control, Ethical issues, Evironmental policy Jeff Bentley is a North American anthropologist who worked in Honduras (Zamorano, 1987–1994) designing a “Natural Pest Control” program, based largely on understanding campesino folk entomology and training smallholder farmers about the conservation of native natural enemies. Since 1994, Bentley has worked as an independent consultant in South America. Bob O’Neil is a specialist in biological control, who studies the basic biology and use of predatory insects. He has been involved since 1984 with the Crop Protection Department, Zamorano, Honduras and is active in biological control research and community outreach with farmers in the midwestern USA. He is an entomologist in the Department of Entomology, Purdue University, West Lafayette, Indiana, USA. Introduction Humans have permanently altered ecosystems since the Upper Paleolithic, when the global expansion of humans coincided with the extinction of hundreds of species of large mammals and birds (Diamond, 1992). Human change of the environment quickened with the agricultural revolution. Crops like maize spread from Mexico to much of the area between Canada and Argentina (Kroeber, 1969 [1939]). Crops and domesticated animals spread from the Near East through Europe (6 to 3,000 years ago) with the spread of the Indo-European-speaking peoples (Mallory, 1989). On a global scale, farming peoples (and their crops and animals) expanded at the expense of local hunter-gatherers (Bellwood, 1991). The world’s ecosystems were altered even faster during the age of discovery, when plants, animals, human populations, and diseases spread between all inhabited continents (Viola and Margolis, 1991). The intercontinental movement of crops and their pests created new conditions for pest growth, as pest population dynamics were no longer constrained by regulatory factors in their areas of origin. For insects, whose populations can be significantly influenced by natural enemies (parasitoids, predators, and pathogens), the lack of key natural enemies allowed for unchecked growth leading to pest outbreaks and crop losses. Early specialists reasoned that re-uniting pests with their natural enemies could reduce pest outbreaks, a concept later termed the “importation method” or “classical biological control.” Since its first success in the USA over 100 years ago, “classical biological control” has resulted in the complete or substantial control of over 200 insect pests (Van Driesche and Bellows, 1996) – making this method one of the most successful approaches to pest control (DeBach and Rosen, 1991). Biological control is more than the importation method and is applied to more situations than insect pests of crops. The scientific, agronomic, ecological, and ethical questions vary by situation, and depends on whether one is addressing, for example, cultural methods that increase the impact of plant pathogenic antagonists (a form of biological control in plant pathology; see Abawi and Thurston, 1994; Page and Bridge, 1993) or applying sugar to crops to attract insect predators (a form of “conservation” biological control). Ethical considerations are made more complex as programmatic or policy decisions made for one type of biological control have ramifications for other types. For example, the number of natural 284 JEFFERY W. BENTLEY AND ROBERT J. O’NEIL enemy species available for “augmentative” biological control (the periodic release of natural enemies) is directly affected by the discovery of new natural enemies from classical biological control efforts. This is because many natural enemies used in augmentative programs were discovered and used in previous importation programs, e.g., the use of Encarsia formosa to control greenhouse whitefly. Reduction of effort in classical programs not only reduces the success rates of these programs, but it also reduces the options available to farmers, homeowners, gardeners, and others using augmentative programs. In this paper, we focus on the biological control of herbivorous insect pests. We contrast ethical considerations of the various types of biological control to each other and to the primary method of insect pest control: insecticides. We draw on our experience teaching biological control to smallholder farmers and our observations of the effects of reliance on pesticides for pest control. These observations and experiences have taught us that whatever ethical considerations are made about the practices of biological control, they must be viewed with respect to the need to provide alternatives to the pesticide paradigm that dominates agricultural systems. Failure to do so is a disservice to farmers needing environmentally sound solutions to their pest problems. 1. Tactics of biological control The major tactics of biological control are (1) natural, (2) conservation, (3) augmentation, and (4) importation of natural enemies. Each tactic suggests unique ethical concerns. 1.1 Natural biological control Biological control as a technology implies conscious manipulation by people to keep populations of herbivorous insects too low to become pests. In the absence of manipulation by humans, i.e., classical biological control, the mortality caused by natural enemies on insects is a fact of life and has no ethical problems. Only as people modify the relationship between natural enemies and pests do ethical considerations enter. 1.2 Conservation Conservation of natural enemies is the conscious efforts of people, especially farmers, to protect or increase the populations of natural enemies of pests through the manipulation of the environment. Examples include reducing insecticide applications, not destroying ant nests, planting flowers to provide nectar for adult parasitoid wasps, and building roofs or arbors to provide habitat for social (predaceous) wasps (Van Driesche and Bellows, 1996; Debach and Rosen, 1991). Chinese peasant farmers have traditional techniques for using ants to control citrus pests (Huang and Yang, 1987; see also Way and Khoo, 1992). Conservation usually costs little labor or cash and simply increases the populations of existing, usually native, natural enemies. This strategy involves people working with nature instead of against it. The manipulation of natural enemies to reduce pests has few if any long-term environmental risks. Unless we are prepared to argue that farmers do nothing to favor, disturb, or benefit one population of insects over another, the local manipulation of indigenous natural enemies to control pests has no ethical considerations independent of those relating to manipulating the environment to produce food versus maintaining “natural” ecosystems without human food production. 1.3 Augmentation Augmentation is the periodic release of natural enemies and is typically a more invasive form of manipulation than natural enemy conservation (Cate, 1990; Waage and Greathead, 1988). Augmentative biological control is being practiced worldwide with an estimated 10 percent of greenhouses in the USA using this method (OTA, 1995), and ca. 50,000 ha of fruit and vegetable crops grown in Europe with the aid of natural enemies (Bigler, 1991). Ethical considerations in augmentative biological control can be related to the frequency of releases, the location of releases, the geographic scale of releases, and the host specificity and other aspects of the biology of the natural enemy. Also relevant, but not discussed here, are ethical considerations of the business of selling natural enemies (e.g., quality control issues, effectiveness of commercially-available natural enemies, contaminants in shipments, etc.: see Hoy et al., 1991). We point out that the commercial sale of natural enemies has generated a new industry: in 1990, Colombia had 24 firms rearing natural enemies (Kaimowitz, 1995), and in the USA about 90 firms sell natural enemies (Hunter, 1994). These firms provide local employment, and alternative control options for farmers, homeowners, and pest managers. It is our belief that private enterprise, not governments, should be the principle suppliers of natural enemies to the public in general and farmers specifically. The release of natural enemies within contained environments (e.g., greenhouses and interiorscapes) has fewer ethical considerations than similar releases outside. For example, the use of Encarsia formosa to control greenhouse whitefly (Trialeurodes vaporariorum) requires multiple releases of the parasitoid, because the greenhouse environment does not provide for sustained population growth of the parasitoid, since the host (whitefly) is not continually present. There are no data that show that natural enemies released into greenhouses, interiorscapes, or other contained areas have caused environmental ON THE ETHICS OF BIOLOGICAL CONTROL OF INSECT PESTS damage (Van Driesche and Bellows, 1996). When releases are made outside of contained environments, additional concerns come into play. Principally, those natural enemies that are generalists, that can establish populations in the release environment, and that are used simultaneously over a broad geographical area invoke more concern than highly specific natural enemies that do not establish populations or are used sporadically in localized areas. Typically, natural enemies used in augmentation programs, for any number of reasons, are incapable of sustaining population growth in the release environment (Van Driesche and Bellows, 1996), but there are few examples of natural enemies that have established populations following augmentative releases [e.g., Phytoseiulus persimilis in California (McMurtry et al., 1978)]. The establishment of natural enemies used in augmentative biological control raises similar ethical issues to the establishment of an “exotic” natural enemy used in a “classical” biological control program (see below). For natural enemies used in augmentative programs that do not maintain populations without continual releases, their negative environmental effects, if any, are likely to be of short duration, localized, and would dissipate with time, as releases are discontinued. The specificity of the natural enemy use in biological control programs is often cited as a concern (Howarth, 1991; OTA, 1995; Van Driesche and Bellows, 1996). Regardless of how we define specificity (e.g., at the species, genus, or family level), the genetic plasticity of species and the inadequacies of our ability to meaningfully measure specificity under controlled conditions means that we risk using natural enemies that attack more than the target pest species. This is true for natural enemies used in augmentative and “classical” biological control programs. Ethically, a balance should be struck between the need for, and value of, augmentation versus the level and degree of collateral environmental damage. With over 100 species of natural enemies for sale in the USA alone (Hunter, 1994), “environmental impact” studies can not be done for every situation, nor do we think they should be. We suggest that the need for such studies should be demonstrated from field data or strongly suggested by the situation (e.g., the presence of an endangered species in the release area). An example of the type of study is given by Andow et al. (1995), who examined non-target effects of augmentative releases of Trichogramma nubilale to control the European corn borer, Ostrinia nubilalis, in maize. Although the authors found that eggs of an endangered butterfly (the “Karner blue,” Lycaeides melissa samuelis) could serve as hosts for the parasitoid, their analyses and field data suggest that impact of T. nubilale releases on the butterfly’s population dynamics would be negligible. Orr and Landis (1994) in their study of nontarget effects of releases of Trichogramma brassicae (to control European corn borer), documented that although 285 the parasitoid does attack eggs of non-target lepidoptera in the laboratory and in maize fields, no lepidopteran eggs located at a distance as short as 10 m from the releases sites were attacked. We specifically mention this finding because it has been suggested that widespread use of this parasitoid may endanger the long-term survival of several species of Lepidoptera, although, actual field measures of its impact suggests that such fears may be unfounded (Andow et al., 1995). Similar protocols could be adopted for natural enemies used in augmentative programs when their use suggest significant environmental impact. Ethical considerations in augmentative biological control may be related to the scope of the program rather than the concept of periodically releasing natural enemies, per se. For example the widespread use of a microbial insecticide in a large tract of forest or mass release of a predators in thousands of hectares of agronomic fields, invokes more questions than use of the same organisms in a homeowner’s backyard. Since such programs are typically in the domain of governments, that, presumably, can afford “environmental impact” studies, the collateral environmental damage done by the simultaneous mass releases of natural enemies over wide areas could be incorporated into an assessment of the overall program. However, the need and extent for such studies should be a function of the host specificity of the natural enemy, its ability to sustain population growth in the release area, the availability and cost of alternative controls, and the current insecticide use patterns. Some pathogens of insects (excepting nematodes) used in augmentative programs in the USA are considered “microbial pesticides” and are registered for use with the Environmental Protection Agency. Ethical issues for augmentation of insect pathogens are similar to those for augmentation of parasitoids and predators. There are fewer possible ethical considerations for host-specific pathogens that do not establish populations, or are used in enclosed spaces, or over limited areas, than for pathogens with broad host ranges that establish after application over wide areas. Direct vertebrate toxicity for pathogens used to control insects is rare (Saik et al., 1989) and although non-target invertebrate impacts have been shown, they are generally less severe than those that occur with pesticide use (see, for example, Zgomba, 1986; Couch and Foss, 1989; Croft, 1990; Miller, 1990; USDA, 1995). There are few documented cases of sustained reductions in non-target populations, or disruptions of community, or ecosystem stability, or dynamics from the use of microbial pesticides (Van Driesche and Bellows, 1996; OTA, 1995). 1.4 Importation (classical biological control) Classical biological control is the introduction of (usually) an exotic natural enemy to control (usually) an intro- 286 JEFFERY W. BENTLEY AND ROBERT J. O’NEIL duced pest. The first documented case was in 1888, when Albert Koebele introduced the vedalia beetle (Rodolia cardinalis) from Australia to control the cottony-cushion scale (Icerya purchasi), a serious citrus pest in California. The beetle was successful, preying on the scale insect and keeping it under control until the late 1940s, when the widespread use of DDT upset the ecological balance (Cate, 1990; Waage and Greathead, 1988; Janick et al., 1981). Since then, there have been hundreds of successful cases (Cate, 1990), e.g., black fly (Aleurocanthus woglumi) in Florida citrus (Tefertiller et al., 1991), ash whitefly (Siphoninus phillyreae) in California (Bellows et al., 1992), and alfalfa weevil (Hypera positca) in the eastern USA (Day, 1981). One of the most impressive recent successes has been the introduction of the parasitoid wasp Epidinocaris lopezi from South America to Africa to control cassava mealybug (Phenacoccus manihoti), which had been inadvertently introduced from South America, to Africa. By the 1970s, the mealybug threatened to destroy the African cassava crop, a major food that withstands drought and poor soil fertility and can be harvested yearround (Goldman, 1995). The introduction of the parasitoid reduced the significant damage done to this subsistence crop of millions of Africans, and it has precluded the use of insecticides targeted at the mealybug on millions of hectares (Herren and Neuenschwander, 1991). The classical biological control method has been attempted in about 1200 projects worldwide in the past 100 years, contributing to the control of 200 pest insects (Van Driesche and Bellows, 1996; DeBach and Rosen, 1991). The vast majority of attempts have been made with insect predators and parasitoids. The notion that classical biological control with arthropod natural enemies may cause continent-wide or global alterations to ecosystems (sensu Lockwood, 1996) has not been documented in any study. There is a single documented case of local extinction of an insect – that of the introduced coconut moth (Leavuana iridescens) in Fiji, although several other cases have been proposed (Howarth, 1991). Permanent, nontarget effects remain largely undocumented and the magnitude of ecological “disruption” via the successful establishment of arthropod natural enemies for insect control must be lower than the collective observational abilities of hundreds of scientists throughout the world who have been involved in classical biological control projects. In contrast, negative effects of insecticides are abundantly documented, e.g., secondary pest outbreaks (Jirström, 1996; Murray, 1994; Ramalho et al., 1990; Vélez, 1994; Whitten and Oakeshott, 1991), insecticide resistance (Bolaños, 1990; Gould, 1991; McKenzie and Byford, 1993; Murray, 1994; Pimentel and Goodman, 1978; Sechser, 1989), and worker poisonings (Loevinsohn, 1987; Murray, 1994; Rola and Pingali, 1993). The suggestion that other pest control technologies, specifically insecticides, are spatio-temporally limited in their environmental effects (Lockwood, 1996) is questionable. For example, DDT is present in penguin eggs in Antarctica (Bolaños, 1990), and pesticides from tropical Asia and Latin America are volatilized and fall in the Canadian Arctic, where they accumulate in toxic levels in fish eaten by Native Americans (Pearce, 1995). Since the mid 1980s, fresh produce has become much more widely traded internationally. Frozen peas bought in New York may have been grown in Guatemala, and chemical pesticides were probably applied to them (Murray, 1994). Ethical questions about classical biological control must be asked in the context of its long-term record of success and safety and against a backdrop of available options and real-world conditions. 2. Ethics by type of pest control Sahlins (1996) recently proposed that even anthropological theory is rooted in Judeo-Christian folk cosmology. The author’s ethics may be equally naive, but they include concerns for rural people (Berry, 1990) and for the natural environment, e.g., preventing human destruction of biodiversity (Wilson, 1988, 1992). We accept the ethics of minimizing change to big, native, unique and integrated ecosystems (Lockwood, 1996) – but few agro-ecosystems are big, native, unique, or integrated. They are “big” depending on one’s definition of the “ecosystem,” but they are less native, unique, and integrated than natural ecosystems. Much of Lockwood’s (1996) argument is that pest control does not justify extinction or other environmental damage outside the agro-ecosystem. Accepting this ethical guideline, we work in biological control because it allows for sustainable food production while minimizing danger to non-target species – especially when compared to chemical pest control (see OTA, 1995). Our ethics are expressed through the goals of praxis: to improve the well-being of rural people, to protect consumers from poisoning, and to increase or maintain crop yields, while sustaining the natural environment. Chemical pest control is difficult to defend ethically. US vice-president, Al Gore, has reviewed the growing environmental threat from chemical pesticides, and we will not repeat his argument here (Gore, 1992). Chemical companies argue that negative side-effects from pesticides are justified to increase food production and prevent hunger. This dubious claim is refuted by the fact that the percentage of crops lost to pests has remained stable since pesticides were first massively used (US figure is ca. 35 percent loss before and after adopting pesticides, see Pimentel, 1991). To this statistic, we add that others equally shocking such as: over 500 species of arthropods have evolved resistance to pesticides by 1983 (Quiroz, 1993) and nearly 20,000 cases of pesticide poisoning were reported in Central America in the mid-1970s (Mendes, ON THE ETHICS OF BIOLOGICAL CONTROL OF INSECT PESTS 1977). No comparable statistics exist for biological control. While a single chemical insecticide will (eventually) dissipate from an ecosystem (although this may take decades), the reduction of the use of insecticides as a class of control agents will only be done if alternatives are available. Until insecticides are replaced by alternative control tactics, agriculture will continually be faced with the regulation, storage, safety, and environmental costs of using insecticides. Replacing environmental contamination by one type of insecticide with another only perpetuates the problem. However, our main argument against chemical pesticides is not because of their environmental or human health problems, although we are concerned about those issues, but because chemical control is usually a shortterm “solution” to a pest problem. Chemical control on the whole cannot be justified agronomically; the technology is not sustainable in the sense that the pests evolve resistance to the chemical while their natural enemies are decimated (Bentley et al., 1995). The more farmers use pesticides, the more “essential” pesticides become, as the complex invertebrate ecology of their farm ecology is replaced by a simplified relationship of between pesticide and pest. Our own experience working with farmers has reenforced the frequency of this unfortunate outcome. From 1987 to 1994, one of us (JWB) asked farmers throughout Honduras whether pests were more common “now” or before farmers adopted pesticides. During hundreds of interviews and in group discussions with thousands farmers during training courses (Bentley et al., 1994), farmers never reported that pests chronically diminished as a result of chemical pesticides. Farmers consistently told us that there were more kinds of pests than before the adoption of chemical pesticides in the 1970s and that pest populations were greater. In response to farmers’ insights on their pest problems, workshops were designed to teach farmers the basics of insect ecology and biological control (Bentley, 1994). Once farmers appreciated the existence and importance of natural enemies, they combined these ideas with their traditional knowledge to synthesize new techniques for conserving native, beneficial organisms (Bentley, 1989; Rodrı́guez and Bentley, 1995a, b). A similar training program for Honduran and Nicaraguan farmers, for the control of crop diseases, also had positive results (Sherwood and Bentley, 1995). However, no matter how creative farmers are, they can not control all their insect pest problems by conserving native natural enemies. To add to their abilities to control pests without resorting to chemicals, farmers must have the options to augment natural enemies and to participate in, and benefit from, classical biological control programs. We do not know the number of living species on the planet, not even to the nearest order of magni- 287 tude (Wilson, 1992), and with the vast majority of insect species unidentified (let alone understood), we cannot empirically predict all the effects of a new species. But the difference between what is possible and what has been shown to have happened is important as a basis for ethical decisions. Real people have been poisoned by pesticides and the contamination of water, soil, and air from pesticide use is easily measured and abundantly documented. Ecosystem-level, global effects of biological control have not been substantiated – the concerns of Howarth (1991) and Lockwood (1996) notwithstanding. To address these and other issues, more basic biological and ecological field research is needed. This should be (but is not) a major international concern. However, the collective history of biological control of insect pests has shown it to be an effective, economical, environmentally-sound and socially equitable pest control tactic. The cassava program that saved a major food crop for Africa was almost denied permission to start, because local politicians were unduly concerned with the potential damage by the natural enemy (Waage and Greathead, 1988). If African leaders had had a bit more negative information about biological control, the program might never have been started and several million poor people would have had a major food crop threatened by the introduction of a new pest. 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