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SCIENCE ADVANCES | RESEARCH ARTICLE

ENVIRONMENTAL STUDIES Copyright © 2022


The Authors, some
The direct drivers of recent global anthropogenic rights reserved;
exclusive licensee
biodiversity loss American Association
for the Advancement
of Science. No claim to
Pedro Jaureguiberry1†, Nicolas Titeux2,3,4†, Martin Wiemers2,5, Diana E. Bowler3,6,7, original U.S. Government
Luca Coscieme8, Abigail S. Golden9,10, Carlos A. Guerra3,11, Ute Jacob12,13, Yasuo Takahashi14, Works. Distributed
Josef Settele2,3,15, Sandra Díaz1, Zsolt Molnár16, Andy Purvis17,18* under a Creative
Commons Attribution
Effective policies to halt biodiversity loss require knowing which anthropogenic drivers are the most important License 4.0 (CC BY).
direct causes. Whereas previous knowledge has been limited in scope and rigor, here we statistically synthesize
empirical comparisons of recent driver impacts found through a wide-ranging review. We show that land/sea use
change has been the dominant direct driver of recent biodiversity loss worldwide. Direct exploitation of natural
resources ranks second and pollution third; climate change and invasive alien species have been significantly less
important than the top two drivers. The oceans, where direct exploitation and climate change dominate, have a
different driver hierarchy from land and fresh water. It also varies among types of biodiversity indicators. For
example, climate change is a more important driver of community composition change than of changes in species
populations. Stopping global biodiversity loss requires policies and actions to tackle all the major drivers and
their interactions, not some of them in isolation.

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INTRODUCTION drivers (9). Thus, policies that do not mitigate the direct drivers are
Human well-being is underpinned by ecological systems and the bound to fail, whatever effect they may have on indirect drivers ear-
benefits they provide to people (1–4), so anthropogenic impacts on lier in the causal chain (2).
nature are of growing scientific, political, and societal concern (2, 5). Climate change has rightly attracted attention as a recent and
Knowing which of the human pressures that proximally influence accelerating direct driver (5, 10, 11), but other drivers—direct ex-
biodiversity—henceforth, direct drivers—are doing the most damage ploitation of natural resources, land/sea use change, pollution, and
worldwide is a prerequisite for designing new systemic policies and invasive alien species—also still cause widespread biodiversity loss
action targets that can achieve major sustainability objectives such (12–14). Which of these direct drivers has the most impact on the
as the post-2020 global biodiversity framework of the Convention various dimensions of biodiversity—from genes and species to eco-
on Biological Diversity (CBD) or the Sustainable Development Goals systems—surprisingly remains an open question. Previous attempts
(SDGs) of the United Nations (6–8). This is so because all the ways to answer it have either used expert judgment (12, 15), focused on
that human values and behaviors (the ultimate indirect drivers) the analysis of one or a few indicators of particular aspects of biodi-
cause biodiversity loss must, by definition, act through the direct versity or specific taxonomic groups (14, 16, 17), or considered only
a subset of the main drivers (17, 18). None of these approaches can
1
Instituto Multidisciplinario de Biología Vegetal (IMBIV), CONICET and FCEFyN,
provide policy makers with the robust conclusions they need about
Universidad Nacional de Córdoba, Casilla de Correo 495, 5000 Córdoba, Argentina. which direct drivers most need mitigation.
2
UFZ – Helmholtz Centre for Environmental Research, Department of Community As part of the global assessment report from the Intergovernmental
Ecology and Department of Conservation Biology and Social-Ecological Systems, Science-Policy Platform on Biodiversity and Ecosystem Services
Theodor-Lieser-Str. 4, 06114 Halle, Germany. 3German Centre for Integrative Biodiversity
Research (iDiv) Halle-Jena-Leipzig, 04103 Leipzig, Germany. 4Luxembourg Institute (IPBES) (2), we systematically reviewed natural science studies pub-
of Science and Technology, Environmental Research and Innovation Department, lished since 2005 that compared the impacts that multiple direct drivers
Observatory for Climate, Environment and Biodiversity, Rue du Brill 41, 4422 Belvaux, have had on any of a large set of indicators of the state of biodiversity
Luxembourg. 5Senckenberg Deutsches Entomologisches Institut, Eberswalder Str.
90, 15374 Müncheberg, Germany. 6Friedrich Schiller University Jena, Institute of (tables S1 to S4). We excluded studies that compared projected future
Biodiversity, Dornburger Str. 159, 07743 Jena, Germany. 7UFZ – Helmholtz Centre effects of drivers. We screened the 45,162 studies (including gray litera-
for Environmental Research, Department Ecosystem Services, Permoserstraße 15, ture) found by systematic database searches or suggested by a global
04318 Leipzig, Germany. 8Hot or Cool Institute, Quartiersweg 4, 10829 Berlin, Germany.
9
Graduate Program in Ecology and Evolution, and Department of Marine and
set of experts and stakeholders involved in the external reviewing
Coastal Sciences, Rutgers University, New Brunswick, NJ 08901, USA. 10School of process of the IPBES report, read the most relevant 575 in full, and
Aquatic and Fishery Sciences, University of Washington, Seattle, WA 98195, USA. 11Institute extracted information from the 163 studies that included nonredun-
of Biology, Martin Luther University Halle Wittenberg, Am Kirchtor 1, 06108 Halle, dant comparisons of the impacts on biodiversity of at least two of the
Germany. 12Helmholtz Institute for Functional Marine Biodiversity at the University
of Oldenburg, Ammerländer Heerstraße 231, 26129 Oldenburg, Germany. 13Alfred five predefined classes of direct drivers: climate change, land/sea use
Wegener Institute, Helmholtz Centre for Polar and Marine Research, Am Handelshafen 12, change, direct exploitation of natural resources, pollution, and inva-
27570 Bremerhaven, Germany. 14Institute for Global Environmental Strategies, 2108-11 sive alien species (see Materials and Methods). Focusing on these
Kamiyamaguchi, Hayama, Kanagawa 240-0115, Japan. 15Institute of Biological Sci-
ences, University of the Philippines, Los Baños, College, 4031 Laguna, Philippines.
multidriver assessments is necessary to avoid simply mirroring any
16
Centre for Ecological Research, Institute of Ecology and Botany, 2163 Vácrátót, research biases toward investigating particular drivers (15, 18). Most
Hungary. 17Natural History Museum, Department of Life Sciences, London SW7 of these studies did not consider impacts before 1970 (1983 was the
5BD, UK. 18Imperial College London, Department of Life Sciences, Silwood Park, median start year of time series analyzed in the studies). For the analyses
Ascot SL5 7PY, UK.
*Corresponding author. Email: [email protected] in this paper, to estimate each driver’s position in the overall domi-
†These authors contributed equally to this work. nance hierarchy even though some have been studied more than

Jaureguiberry et al., Sci. Adv. 8, eabm9982 (2022) 9 November 2022 1 of 11


SCIENCE ADVANCES | RESEARCH ARTICLE

others (19), we converted each multidriver assessment into one or the second-ranked driver, direct exploitation [bootstrap P = 0.92; all
more nonredundant pairwise comparisons between drivers (see P values reported in the text have been adjusted for multiple testing
Materials and Methods). Analyzing these head-to-head comparisons (23) when appropriate]. Both land/sea use change and direct exploita-
(table S5) allowed us to quantify each driver’s dominance (20), using tion were significantly dominant over climate change (bootstrap
bootstrapping to test whether pairs of drivers differed significantly in P = 0.034 and P = 0.040, respectively) and invasive alien species
their impact. Wherever possible, we also assigned each comparison (P < 0.0001 for both).
to one of the four IPBES geographic regions (Africa, Americas, Asia The dominance hierarchy of drivers differed significantly between
and the Pacific, or Europe and Central Asia) (21); to the terrestrial, terrestrial, freshwater, and marine realms (randomization P < 0.0001),
freshwater, or marine realm; and to one of the six broad dimensions with the hierarchy in the sea differing significantly from both that
of biodiversity represented by the classes of Essential Biodiversity on land (randomization P < 0.0001) and that in fresh water (random-
Variables [EBVs; (22)]—genetic composition, species populations, species ization P = 0.018; Fig. 1B). Land/sea use change was ranked first in
traits, community composition, ecosystem structure, and ecosystem terrestrial systems, significantly ahead of direct exploitation (boot-
function (table S4). This allowed us to use randomizations to test the strap P = 0.026), and in freshwater ecosystems, ahead of pollution,
statistical significance of differences in the driver dominance hierar- but direct exploitation was the dominant driver in marine ecosystems
chies among major regions, types of ecosystems, and dimensions of with climate change second.
biodiversity; these groupings are still broad and heterogeneous, but The dominance hierarchy was broadly consistent among the four
biological and socioeconomic differences among them may be reflected IPBES regions, although land/sea use change was ranked first and
in their driver dominance hierarchies (see Materials and Methods). direct exploitation second in Asia and the Pacific and in Europe and
Our evidence reflected large-scale geographic and taxonomic biases Central Asia (the regions with most studies), whereas these ranks were
in knowledge, with fewer studies from Africa than from the other regions reversed in Africa and the Americas (Fig. 2). Drivers showed strong
and, for those indicators relating to taxonomic groups, far more infor- differences in dominance within Africa (steepness = 0.573, P = 0.004)

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mation from vertebrates than from plants or invertebrates (table S6). and Asia and the Pacific (steepness = 0.501, P = 0.001) but not in the
Americas (steepness = 0.292, P = 0.14) or Europe and Central Asia
(steepness = 0.265, P = 0.41). However, these among-region differences in
RESULTS the dominance hierarchy of drivers were not themselves statistically
Overall, land/sea use change was the dominant direct driver of bio- significant (all four regions: randomization P = 0.326; planned con-
diversity loss (Fig. 1A), although it was not significantly ahead of trast of the two most study-rich regions: randomization P = 0.082).

A B Terrestrial
(N = 87)
Land/sea use Land/sea use
change change

3.16
2.77-3.40 Direct
Invasive alien
exploitation
species

2.83
1.78 2.34
2.32-3.09 Direct 1.47-1.99
00
1.76-2.72

Invasive alien exploitation


species

1.40 1.32
1.27 2.46 0.97-2.06 1.08-1.83

0.98-1.43 2.18-2.82 Marine Freshwater


(N = 58) Pollution Climate (N = 38)
change
Land/sea use Land/sea use
change change

ns
1.73
1.19-2.15
Direct 2.69
exploitation 2.42-3.51 Direct
Invasive alien Invasive alien
species exploitation
species

0.83 2.82
0.65-1.27 2.61-3.41
1.61 1.99
0.87-1.82 1.42-2.34

1.91 1.53
1.67-2.40 1.11-2.01

2.11 2.51
1.76-2.47 1.82-2.75 2.18 1.53
Pollution Climate 1.89-2.97 0.77-2.03

change Pollution Climate Pollution


Climate
change change

Fig. 1. Dominance hierarchies of the five studied direct drivers of biodiversity loss. (A) Overall hierarchy (N = 154 studies) and (B) hierarchies for terrestrial, marine,
and freshwater realms. Area of the circle for each driver is proportional to its dominance score (20) (indicated inside with 95% confidence interval; possible range = 0 to
4). Arrows linking pairs of drivers show the significance of the dominance difference between them based on bootstrapping: Arrow thickness reflects unadjusted P values
(thin: P < 0.1, intermediate: P < 0.05, thick: P < 0.01, no arrow: P ≥ 0.1), and arrow shading reflects P values adjusted for multiple testing (black: P < 0.05, gray: P ≥ 0.05). The
central triangle in (B) reports the significance of differences in the among-driver dominance hierarchy between pairs of realms (***: randomization P < 0.001; *: P < 0.05;
ns: P > 0.5). N gives numbers of studies available for the analysis within each realm. The steepness of the driver hierarchy also rejects the null hypothesis that all drivers
have the same impact overall (steepness = 0.405, P = 0.0001), in the terrestrial realm (steepness = 0.465, P < 0.0001), and in the marine realm (steepness = 0.479, P < 0.001),
but not in fresh water (steepness = 0.292, P = 0.13).

Jaureguiberry et al., Sci. Adv. 8, eabm9982 (2022) 9 November 2022 2 of 11


SCIENCE ADVANCES | RESEARCH ARTICLE

Americas Land/sea use Land/sea use Europe and


(N = 41) change change Central Asia
(N = 48)

2.45 2.43
2.01-2.94 Direct 1.74-3.05
Direct
Invasive alien exploitation Invasive alien exploitation
species species

1.76 2.59 1.28 2.23


2.11-3.07 0.78-1.56 1.60-2.97
1.08-2.30

1.52 1.68 1.93 2.13


1.17-2.00 1.17-2.12 1.42-2.45 1.69-2.71

Pollution Climate Pollution Climate


change change

Africa Land/sea use Land/sea use


Asia and
(N = 22) change change the
t Pacific
(N = 48)

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2.78 Direct 3.06
2.09-3.44 2.72-3.42 Direct
exploitation Invasive alien
Invasive alien exploitation
species species

1.09 3.20 1.46 2.70


0.88-1.52 2.80-3.56 1.10-2.00 2.15-3.04

1.60 1.33 1.59 1.20


0.74-2.38 0.96-1.62 1.22-2.00 0.72-1.66

Pollution Climate Pollution Climate


change change

Fig. 2. Land/sea use change and direct exploitation are the main drivers in all regions. Area of the circle for each driver is proportional to its dominance score (20)
(indicated inside with 95% confidence interval; possible range = 0 to 4) within each IPBES region. Arrows linking pairs of drivers show the significance of the dominance
difference between them based on bootstrapping: Arrow thickness reflects unadjusted P values (thin: P < 0.1, intermediate: P < 0.05, thick: P < 0.01, no arrow: P ≥ 0.1), and
arrow shading reflects P values adjusted for multiple testing (black: P < 0.05, gray: P ≥ 0.05). N gives numbers of studies available for the analysis within each region.

The dominance hierarchy of drivers varied significantly among classes in both the terrestrial (randomization P = 0.0187) and fresh-
the six EBV classes (randomization test: P = 0.0004; Fig. 3). It also water (P = 0.0181) realms, with climate change again being ranked
differed between the two classes with most data (species populations higher as a driver for changes in community composition than for
and community composition: planned contrast randomization other changes. None of the four IPBES regions showed significant
P < 0.0001). While land/sea use change was ranked first and direct variation in the dominance hierarchy of drivers among the EBV
exploitation second as a driver of change in species populations, they classes (smallest randomization P = 0.077).
were, respectively, ranked second and fourth in community compo-
sition. Climate change ranked first among the drivers of community
composition changes, but last among the drivers of species popula- DISCUSSION
tion changes. Land/sea use change was also ranked as the top driver We have shown clearly that land/sea use change—mainly in the form
of changes in ecosystem structure and ecosystem function. Invasive of rapid expansion and intensifying management of land used for
alien species were the dominant driver of changes in species traits, cropping or animal husbandry (9)—and direct exploitation—mostly
and, though with an extremely small dataset, climate change was through fishing, logging, hunting, and wildlife trade (9)—have been
the top-ranked driver of changes in genetic composition (Fig. 3). the two dominant drivers of global biodiversity loss overall over re-
While biodiversity-focused search terms may have contributed to cent decades (Fig. 1A). Whereas previous comparisons of driver
the shortage of comparisons of direct driver impacts for ecosystem importance have been based on either very few indicators or expert
function, the dearth of comparisons for species traits and genetic judgment, our analyses have robustly synthesized scientific knowl-
composition is a knowledge gap that highlights the lack of back- edge on the relative impacts of multiple direct drivers on an un-
ground information on temporal changes in these dimensions of bio- precedentedly wide array of indicators of the state of biodiversity
diversity (24). Driver dominance varied significantly among EBV (table S1). They also include tests of consistency among the main

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SCIENCE ADVANCES | RESEARCH ARTICLE

2.88 2.88
Community Ecosystem
composition function
0.83 1.60 1.24 1.53

(N = 34) 1.79 2.91 2.79 1.56 (N = 19)

1.25 2.55
Species Ecosystem
traits 2.65 2.33 0.49 2.33 structure

(N = 15) 2.28 1.49 2.37 2.27 (N = 33)

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1.77
3.14
Species Genetic
populations 1.06 0.81 composition
1.56 3.08

(N = 78) 2.95 3.41 (N = 2)


1.44 0.78

Land/sea use change Direct exploitation Climate change Pollution Invasive alien species

Fig. 3. The main drivers of biodiversity loss differ among the six EBV classes. Area of the circle for each driver is proportional to its dominance score (20) indicated
inside the circle (possible range = 0 to 4). One-way arrows linking pairs of drivers show the significance of the dominance difference between them based on bootstrap-
ping. Two-way arrows between EBV classes indicate significant pairwise differences in their driver dominance hierarchies based on randomization tests. For all arrows,
thickness reflects unadjusted P values (thick: P < 0.01, intermediate: P < 0.05, thin: P < 0.1, no arrow: P ≥ 0.1) and shading reflects P values adjusted for multiple testing
(black: P < 0.05, gray: P ≥ 0.05). N gives numbers of studies available for the analysis within each EBV class. The question mark indicates the very uncertain rankings for
genetic composition because of small sample size. EBV class icons created by C. Gutiérrez of the Humboldt Institute (Bogotá, Colombia) for GEO BON.

geographic regions, types of ecosystems, and dimensions of biodiversity. this capability is itself a worthwhile goal, given the inevitability of
By focusing on comparisons of two or more drivers, we have side- ongoing climate change for at least decades, the limited state of
stepped biases caused by unequal research attention among them (18) knowledge of the complex ways it will interact with the other direct
and by underreporting of small effects (25). Climate change is probably drivers, and the potential contribution of biodiversity to climate
the most rapidly intensifying threat to biodiversity, and its impacts adaptation and mitigation (5, 32).
are increasingly well quantified (26), but other threats are still doing Given the need to tackle direct drivers in a holistic way, it is con-
more damage. cerning that targets in current global environmental agreements—
This finding highlights the scale of the challenge facing those who such as the CBD and the UN Framework Convention on Climate
are negotiating and implementing the post-2020 global biodiversity Change (UNFCCC)—are defined in isolation. The risk of this framing
framework of the CBD. Combating climate change alone will not be is that a narrow focus on one driver can lead to actions that overlook—
enough to prevent—or possibly even slow—the further loss of bio- and in the worst case undermine—targets on others (5). For in-
diversity, unless damaging land/sea use change and direct exploitation stance, some “nature-blind” strategies for mitigating climate change
are also tackled with similar ambition and determination (14, 27). include large-­scale expansion of cropland bioenergy, but the resulting
Rapidly upscaling holistic management practices that benefit both loss of natural habitat will directly harm biodiversity (33) and is
climate and biodiversity will be key (5, 28) and must be done in a already among the pressures with fastest-growing impacts (34).
manner that safeguards livelihoods and ways of life (29, 30). Actions Even considering the benefit of reduced climate change, the net
that succeed in reversing or slowing biodiversity declines can not impact on biodiversity is likely to be negative (5, 33, 35). By contrast,
only considerably slow human-caused climate change (31): They nature-based solutions such as large-scale restoration of natural
can also make ecosystems more able to maintain functionality— forest (36) and effective protection of coastal wetlands (37) not only
and hence the flows of nature’s contributions to people—in the face help to mitigate climate change but also can directly provide addi-
of ongoing climatic and other environmental changes (29). Enhancing tional benefits to biodiversity and people (5, 38).

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SCIENCE ADVANCES | RESEARCH ARTICLE

The significantly different hierarchy in the ocean (Fig. 1B) sug- for many drivers of change (48). Biodiversity models have largely
gests that, at the broadest scale, policies, strategies, and action targets focused on the drivers with good data, notably climate and land use,
for marine conservation need to emphasize direct exploitation and with limited, if any, exploration of interactions [e.g., (46, 49)]. Most
climate change more—and land/sea use change less—than their equiva- projections of future biodiversity use scenarios that were originally
lents for the terrestrial and freshwater realms. The scale at which developed for climate science, and which treat some of the other
oceans are currently managed to reduce marine defaunation because drivers in a much less integrated way, if at all (50, 51). The need for
of overfishing does not adequately match the great mobility of a clearer and more integrated picture of recent and future driver
organisms at sea (39). Many of these disperse across multiple manage- impacts is pressing. Interactions between climatic and other drivers
ment jurisdictions, and the mean size of marine protected areas is will become more widespread as more areas experience high inten-
much smaller than the home range size of most species. This mis- sities of both. Improved data on drivers (41, 52), new approaches to
match may make it easier for these organisms to be affected by fishing modeling their interactions (53), and new scenario frameworks that
operations, either directly when they are overfished or indirectly through better reflect the complex interplay between people and nature (54)
bycatch. Although climate change is reshuffling marine ecological should all help to produce a clearer picture. Understanding the ef-
communities, high colonization potential helps many species to shift fects of dynamically changing and interacting drivers is also import-
their geographical distribution across wider spatial scales than spe- ant beyond biodiversity loss. Land-use change and direct exploitation are
cies on land (40). Climate change also has a particularly important also both drivers of emergence of zoonotic and vector-borne diseases
impact on indicators of community composition on land and in fresh (55, 56); whereas current policies aim to control diseases after they
water (Fig. 3), but our analysis shows that changes in data-rich EBV have emerged, robust understanding of the driver links and feed-
classes are all strongly driven by land/sea use change, pointing to its backs may help to develop policies that can make emergence less
major role across the various dimensions of biodiversity. The impact likely in the first place (57).
of direct exploitation on species populations is unsurprising but Tackling accelerating climate change and bending the curve of

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may, in part, reflect an understandable data bias toward populations biodiversity loss while still producing affordable food and safe water
and species that are being actively exploited. for people will require ambitious targets, policies, and actions that
Although the overall driver hierarchy is clear, exceptions are not are more holistic than at present (2, 5, 28, 32, 49, 58). While UNFCCC
rare: Nearly 30% of pairwise comparisons went against the overall COP26 showed promising signs of the needed integration, with its
ranking; each driver was the most important in some studies; and recognition of the links between biodiversity and climate, its outcomes
we provide the first robust evidence that the hierarchies differ sig- lacked the ambition required to meet the challenge. As well as miti-
nificantly among realms (Fig. 1B) and EBV classes (Fig. 3). One ob- gating the direct drivers, tackling the root causes of biodiversity
vious source of this context dependency is that all drivers show loss—demographic, socioeconomic, and technological changes togeth-
strong geographic variation in intensity, many even at quite small er with the societal values and governance structures that underpin
spatial scales (41). On land, nonclimatic drivers tend to covary pos- them—requires urgent transformative change (2, 4, 5, 28, 49, 59). If
itively with each other spatially but negatively with climate change we are to maximize our options for managing inevitable changes
such that only the temperate broadleaf and mixed forest biome fac- (31, 32) and widen the currently narrow (49, 60) path to a sustain-
es above-average intensity of all drivers (41). This may explain why able future, the results presented here show clearly that this nature-­
the two IPBES regions where this biome is extensive (the Americas positive transformation must tackle these indirect drivers of land/
and Europe and Central Asia) show a less strongly marked hierarchy sea use change and direct exploitation with as much determination
among the drivers than elsewhere (Fig. 2). The context dependency as the causes of climate change.
of driver rankings has been used to argue that these rankings are at
best irrelevant for conservation (42). However, far from diminishing
the importance of rankings for the development of effective policies MATERIALS AND METHODS
and action targets, context dependency instead emphasizes that the Overview of the literature review and synthesis
rankings must be based on evidence from a wide range of contexts— Systematic reviews of the scientific literature are key to synthesizing
different realms, regions, taxa, and indicators—as we have done here, a large and rapidly growing body of evidence but can be time-consuming
to ensure their robustness. depending on the amount of studies available on the topic of interest.
Our analysis provides an overview of driver hierarchies in the Rapid evidence assessments are similar to systematic reviews but
past few decades. Valuable next steps include adding a temporal with some components of the process simplified or omitted to pro-
dimension and identifying the most important interactions among duce information within a short period of time (61). A rapid evidence
drivers, for both recent changes and future projections (43). Neither assessment was carried out as part of the IPBES Global Assessment
is straightforward, however. Few multidriver comparisons can be Report on Biodiversity and Ecosystem Services to rank broad classes
partitioned into different time periods. While quantitative estimates of anthropogenic direct drivers as causes of changes in the state of
of the impacts of climate change—the driver that is studied most biodiversity. These broad classes—climate change, direct exploita-
often (18)—show increases over time (44, 45) that are projected to tion of natural resources, invasive alien species, land/sea use change,
continue (5, 46, 47), similarly robust information is not yet readily and pollution—are not equally represented in the literature (18, 50).
available for the less studied drivers. Likewise, interactions among To ensure that our inferences were not biased by uneven research
drivers, both in terms of nonadditive impacts on biodiversity where effort, we therefore focused on the results from studies that com-
both are present and in terms of social-ecological feedbacks (e.g., pared the impact of two or more drivers on some facet of biodiversity.
how actions to mitigate one driver might influence the others), are Because these comparisons were predominantly qualitative rather than
not yet well understood (5). These difficulties reflect linked limitations quantitative, we synthesized the rankings they implied into domi-
in data and tools. Detailed spatiotemporal data have been lacking nance hierarchies of the direct drivers—in terms of their impacts on

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SCIENCE ADVANCES | RESEARCH ARTICLE

major dimensions of biodiversity. Unlike the nonstatistical summary combined using the Boolean operator “AND” to represent each of
of the evidence in the IPBES Global Assessment (2, 62, 63), the ana- the 10 pairwise combinations of drivers.
lytical approach used here avoids making any assumption about the Full search strings for impacts of drivers on biodiversity
drivers not considered in each such comparison. By synthesizing Each partial search string reflecting an individual indicator (table S1)
driver ranks in multidriver studies, our approach also side-steps was combined with each of the 10 partial search strings reflecting a
problems that could arise with estimating each driver’s quantitative pair of drivers (table S2) using the Boolean operator AND to identify
impact if small effect sizes are underreported in the literature (64). studies assessing the impacts of two drivers on each indicator.
We have analyzed our compilation of comparisons at the global Synthetic studies that assessed and compared the impact of major
scale, within each of the four IPBES regions and within the terrestrial, drivers without mentioning them explicitly in the title, keywords, or
freshwater, and marine realms. We also performed appropriate sta- abstract could be missed by the above approach. The following search
tistical significance tests of differences in importance within a hierarchy, string was therefore used to find such studies: (driver* OR factor*
and of differences between hierarchies for different subsets—realms, OR determinant* OR “driving force*” OR threat* OR “proximate
regions, or dimensions of biodiversity (i.e., the six classes of EBV). cause*” OR pressure* OR stressor* OR risk* OR “global change”)
The assessment was organized in seven successive steps aiming at AND (multi* OR quantif* OR compar* OR partition* OR rank* OR
identifying, synthesizing, and analyzing adequate information from order* OR relative OR interact* OR interplay* OR synerg* OR mag-
the most relevant natural science studies. nitude* OR rate* OR effect* OR impact* OR influe* OR pace* OR
extent OR importan*). In the same way as for the pairwise combi-
Systematic literature searching nations of drivers, this general search string was then combined with
The search of natural science studies in the literature was performed each of the partial search strings from table S1 to identify studies
using search strings covering the two main aspects of our overarch- assessing the impact of multiple drivers on each indicator.
ing question, i.e., the “impact of human-caused direct drivers” on Table S3 provides different examples of full search strings that were

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the “changes in the state of biodiversity.” We elaborated partial used to identify studies examining the impacts of different drivers
search strings to capture (i) change in the state of biodiversity and on several dimensions of biodiversity change. After accounting for
(ii) the human-caused direct drivers of this change, and we then duplicates across the outcomes of different search strings, we ex-
combined them to produce full search strings. These search strings tracted 45,162 potentially useful studies.
were used in Web of Science on 5 September 2018 to find published
studies based on their titles, keywords, and abstracts. Inclusion of studies from additional sources
Partial search strings for changes in the state of biodiversity A further 138 potentially relevant studies were included manually,
Biodiversity change was captured with a series of large-scale indica- which fell into three categories: (i) scientific studies not captured by
tors currently endorsed by global biodiversity–related initiatives, the search strings developed in tables S1 and S2 but considered as
such as the CBD, Future Earth, and the IPBES (table S1). Indicators potentially relevant by experts and stakeholders involved in the suc-
intrinsically related to a single direct driver or to a limited subset of cessive phases of the external reviewing process of the IPBES report,
drivers were not retained because our objective was to rank the im- (ii) other important studies from the gray literature (not directly
pacts of multiple direct drivers on changes in the state of biodiversity. available through searches in Web of Science) such as reports [e.g.,
Partial search strings used to capture each of the indicators are re- CBD or Food and Agriculture Organization of the United Nations
ported in table S1. (FAO) reports], and (iii) source databases directly documenting the
Selected indicators reflected temporal changes in different dimen- impact of drivers on particular indicators (i.e., Living Planet Index
sions of biodiversity and were classified into the six classes of EBVs and Red List Index).
(22), i.e., genetic composition, species populations, species traits,
community composition, ecosystem structure, and ecosystem function Screening of studies extracted from literature
(table S4). We gathered information for several indicators within and other sources
EBV classes to rank drivers as comprehensively as possible (see the Screening of abstracts, titles, and keywords
“Scoring driver importance” section). The schedule of the IPBES Global Assessment Report precluded de-
Partial search strings for direct drivers tailed scrutiny of the entire evidence base. Our rapid evidence as-
Direct drivers were classified according to five main categories rep- sessment therefore prioritized search results for consideration as
resenting the main human-caused proximate pressures on biodiversity follows. For each indicator, studies obtained from the 10 driver-pair
(9): (i) land/sea use change, (ii) direct exploitation of natural resources, searches and the broader multidriver search were pooled, with studies
(iii) climate change, (iv) pollution, and (v) invasive alien species. ordered first by the number of searches that returned them and second
Direct threats that do not fit clearly into one of the five main catego- by recency of publication, on the grounds that more frequently re-
ries, such as fires or disturbances from recreational activities, were turned and more recent studies were more likely to be relevant. We
excluded from consideration. A list of search terms was first estab- then screened the titles, keywords, and abstracts of the 200 top-ranked
lished on the basis of the description of each direct driver within the search results for each indicator; for indicators yielding fewer than
IPBES Global Assessment Report (2, 9). The IUCN classification of 200 studies, we assessed them all. All studies included as additional
direct threats to biodiversity (65) was then used to extend the list of source of information were also screened in the same way (N = 138).
search terms for each driver, with further terms added from reviews A total of 3822 studies were screened.
of threats in freshwater (66) and marine (67) realms. Table S2 gives Selection of potentially suitable studies
the partial search strings used for each driver. During this screening, studies were retained for further consider-
To find studies that compared the impacts of at least two drivers ation if they appeared likely to meet three initial criteria: (i) they
on biodiversity, search strings from different rows in table S2 were had compared the impacts of at least two of the direct drivers, (ii)

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SCIENCE ADVANCES | RESEARCH ARTICLE

on at least one of the indicators or one of the EBV classes, and (iii) each indicator); (v) EBV class (see table S4 for definitions and table S1
in the past or present (rather than in the future). Reviews and for numbers of assessments within each EBV class); (vi) higher taxon
meta-analyses were retained if they met these criteria. A total of (see table S6; note, this is not applicable for, for example, assess-
575 studies were retained as potentially suitable for further analysis. ments of measures of ecosystem structure); (vii) drivers (using the
typology of table S2); and (viii) impact of each driver: integer to
Assessment of eligibility for inclusion in the meta-analysis rank the impact of the drivers (starting with 1 for the driver with
The 575 studies retained after screening were read in full to evaluate highest impact) on an ordinal scale (ties allowed). Too few studies
their eligibility for inclusion in the analysis based on the following compared the impacts of multiple drivers quantitatively to support
attributes: (i) type of analysis: analysis of empirical data (studies using an analysis of these estimates.
any sort of data, even if from an existing database), review (qualitative/
descriptive synthesis of existing literature), and meta-analysis (quan- Scoring driver importance
titative synthesis of existing literature or analysis of multiple data- We converted the driver ranks from each assessment into scores
sets from other studies); (ii) indicator(s) targeted by the analysis that could be synthesized to produce an overall ranking that was not
(table S1); (iii) EBV class(es) targeted by the analysis (table S4); (iv) affected by differences in research attention among drivers. Table
assessment of temporal changes in the indicators: not applicable S5 shows how the information contained in an assessment’s ranking
(studies not directly based on empirical data—e.g., reviews), not as- of multiple drivers can readily be partitioned into a set of nonre-
sessed (studies not reporting on observed biodiversity changes), and dundant pairwise comparisons between drivers. In each such head-
assessed (studies reporting on indicators with a direct or indirect to-head comparison, the more important driver is scored as 1 and
estimation of temporal changes in the state of biodiversity); (v) number the less important driver 0; equally ranked drivers each score 0.5.
of drivers analyzed or assessed (table S2): between 0 and 5; (vi) as- This scoring is simply another representation of the original rank-
sessment of the impacts of different drivers: none (impacts of drivers ing, containing exactly the same information (see table S5).

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not compared), nominal scale (list of drivers affecting indicators We multiplied the scores from each assessment by weights to
without qualitative or quantitative comparison), ordinal scale (quali- reflect two ways in which assessments vary in the amount of rele-
tative comparison, i.e., drivers ranked based on their impact), and vant information they contribute to an analysis, as follows:
ratio scale (quantitative comparison, i.e., impact of each driver 1) Spatial coverage. Assessments encompassing a larger geographic
quantified—e.g., partitioning approaches); (vii) and publication year area should contribute more information, other things being equal.
Empirical studies published in/after 2005 and estimating (on at Assessments within each study were therefore assigned an analysis
least an ordinal scale) the impacts of at least two drivers on the tem- weight based on their spatial coverage such that an assessment at a
poral change of biodiversity indicator(s) or EBV class(es) were con- larger scale would just outweigh two assessments at the next scale
sidered as eligible. Reviews and meta-analyses of original studies down: local assessments received a “scale weight” of 1, regional as-
that satisfy the aforementioned rules were also considered as eligi- sessments a scale weight of 3, continental assessments a scale weight
ble. Eligibility rules included the year of publication as to focus on of 7, and global assessments a scale weight of 15.
novel information produced since the Millennium Ecosystem As- 2) Representation of indicator in dataset. Because the 22 biodi-
sessment (68). If studies about particular indicator(s) published versity indicators in table S1 were not equally represented within
after 2005 were lacking, we also considered studies published before the data (either overall or within any of the subsets we analyzed),
2005 as eligible. A total of 189 studies were considered eligible and assessments of less well-represented indicators should be upweighted
were then checked for redundancy as follows. If several studies re- to avoid results being skewed by research biases toward particular
ported on results obtained from the same source of information, indicators. For each dataset (including each bootstrap replicate)
only the most recent was retained for the next stage of the analysis. being analyzed, we first summed the scale weights for all assess-
After this procedure, 163 studies were used to extract information ments of each indicator represented within it. Each assessment was
on the impacts of drivers (see data S1). then given an “indicator weight” inversely proportional to the sum
of that indicator’s scale weights. The sums of the scale weights for
Extraction of information from eligible studies each indicator ranged from 6 (for the area of mangrove forest cover)
Eligible studies may report separately on the impacts of drivers on to 244 (for the IUCN Red List).
several indicators from the same or different EBV classes, in a num- Each head-to-head score was multiplied by the product of its
ber of regions or for different realms. They may also assess the im- scale weight and indicator weight. Studies that considered more
pacts of drivers on the same indicator but for different taxonomic drivers also contribute more information to the synthesis by dint of
groups. Each of these different levels of analysis was considered as a yielding more pairwise comparisons; this reflects their greater in-
separate assessment within the studies and, for each individual as- formation content without the need for any additional weighting. A
sessment, the following attributes were extracted from reading the consequence of this is that indicators for which more drivers tended
full text and associated files: (i) spatial coverage: local (smaller than to be compared had more total weight in each analysis. This effect
a country), regional (between a single country and several coun- was slight, however; for example, in the overall analysis (Fig. 1A),
tries), continental (covering all or a representative set of countries the total weight of each indicator varied only by a factor of 4.
within a continent), or global; (ii) IPBES region (21): Africa, Americas,
Asia and the Pacific, Europe and Central Asia, several regions (with Statistical analysis of driver scores
an option to select regions), all regions, unclear, or not specified; (iii) To infer the hierarchy of drivers for a set of assessments, we first summed
realm: freshwater, marine, terrestrial, several realms (with an op- the pairwise scores (weighted as above) across the assessments.
tion to select realms), all realms, unclear, or not specified; (iv) indi- From the resulting matrices, we calculated each driver’s dominance
cator (see table S1 for definitions and numbers of assessments for as its normalized David’s score (20), using the DS function in the

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SCIENCE ADVANCES | RESEARCH ARTICLE

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