Defaunation in the Anthropocene

TL;DR: Defaunation is both a pervasive component of the planet’s sixth mass extinction and also a major driver of global ecological change.

Abstract: We live amid a global wave of anthropogenically driven biodiversity loss: species and population extirpations and, critically, declines in local species abundance. Particularly, human impacts on animal biodiversity are an under-recognized form of global environmental change. Among terrestrial vertebrates, 322 species have become extinct since 1500, and populations of the remaining species show 25% average decline in abundance. Invertebrate patterns are equally dire: 67% of monitored populations show 45% mean abundance decline. Such animal declines will cascade onto ecosystem functioning and human well-being. Much remains unknown about this “Anthropocene defaunation”; these knowledge gaps hinder our capacity to predict and limit defaunation impacts. Clearly, however, defaunation is both a pervasive component of the planet’s sixth mass extinction and also a major driver of global ecological change.

Summary

Defaunation: a pervasive phenomenon

• This does not consider population extirpations and declines in animal abundance within populations.
• From an abundance perspective, vertebrate data indicate a mean decline of 28% in number of individuals across species in the last four decades (14, 21, 22) Loss of invertebrate biodiversity has received much less attention and data are extremely limited.
• Data suggest that the rates of decline in numbers, species extinction, and range contraction among terrestrial invertebrates are at least as severe as among vertebrates (23, 24) .
• Long term distribution data on moths and four other insect Orders in the UK show that a substantial proportion of species have experienced severe range declines in the last several decades (19, 25).

Patterns of defaunation

• Though the authors are beginning to understand the patterns of species loss, they still have a limited understanding of how compositional changes in communities following defaunation and associated disturbance will affect phylogenetic community structure and phylogenetic diversity (26) .
• Notably, certain lineages appear to be particularly susceptible to human impact.
• In their evaluation of mammals (1437 species) and birds (4263 species), the number of species per 10,000 km 2 in decline (IUCN population status "decreasing") varied across regions from a few to 75 in mammals and 125 in birds (Fig 2 ), with highest numbers in tropical regions.
• Similarly, the authors now recognize that extinction risk is often a synergistic function of both intrinsic species traits and the nature of threat (32, (34) (35) (36) (37) .
• Large body size is more important for predicting risk in island birds than mainland birds (34) , and for tropical mammals than for temperate ones (36) .

Multiple, unaddressed drivers of defaunation

• The long-established major proximate drivers of wildlife population decline and extinction in terrestrial ecosystems, namely overexploitation, habitat destruction, and impacts from invasive species remain pervasive (18) .
• Rather, all show increasing trajectories in recent decades (14) .
• Moreover, several newer threats have recently emerged, most notably anthropogenic climate disruption, which will likely soon compete with habitat loss as the most important driver of defaunation (44) .
• Disease, primarily involving human introduced pathogens, is also a major, and growing threat (46) .
• Feedbacks amongst these and other drivers seem more likely to amplify the effects of defaunation, than to dampen them (11) .

Consequences of defaunation

• A recent meta-analyses of biodiversity-ecosystem function studies suggests that the impact of biodiversity losses on ecosystem functions is comparable in scale with that of other global changes (e.g. pollution, nutrient deposition) (9) .
• Most efforts to quantify this relationship have focused largely on effects of reduced producer diversity, which may typically have much lower functional impacts than does consumer loss (49, 50) .
• Efforts to quantify effects of changes in animal diversity on ecosystem function, particularly terrestrial vertebrate diversity, remain more limited (supplementary online methods) (51) .

Impacts on ecosystem functions and services

• Here the authors examine several ecosystem functions and services for which the impacts of defaunation have been documented, either as a direct result of anthropogenic extirpation of service-providing animals, or indirectly through cascading effects (Fig 5 ).
• Pollinators appear to be strongly declining globally in both abundance and diversity (53) .
• Global declines in amphibian populations increase algae and fine detritus biomass, reduce nitrogen uptake, and greatly reduce whole stream respiration (Fig 5E; (63) ).
• Between 23-36% of all birds, mammals and amphibians used for food or medicine are now threatened with extinction (14) .
• More work is urgently needed to understand the mechanisms and context dependence of defaunation-disease relationships in order to identify how defaunation will impact human disease.

Impacts on evolutionary patterns

• The effects of defaunation appear not just proximally important to the ecology of impacted species and systems, but also have evolutionary consequences.
• Several studies have detected rapid evolutionary changes in morphology or life history of short-lived organisms (72) , or human exploited species (73) .
• Still poorly studied are the indirect evolutionary effects of defaunation on other species, not directly impacted by human defaunation.
• Changes in abundance or composition of pollinators or seed dispersers can cause rapid evolution in plant mating systems and seed morphology (75, 76) .
• There is a pressing need to understand the ubiquity and significance of such "evolutionary cascades" (77) .

Synthesis and ways forward

• This review indicates that a widespread and pervasive defaunation crisis, with farreaching consequences, is upon us.
• Cumulatively, systematic defaunation clearly threatens to fundamentally alter basic ecological functions and is contributing to push us towards global-scale "tipping points" from which the authors may not be able to return (7) .
• Ultimately, both reduced and more evenly distributed global resource consumption will be necessary to sustainably change ongoing trends in defaunation and, hopefully, eventually open the door to refaunation.
• (C) Globally, a compiled index of all invertebrate population declines over the last 40 years shows an overall 45% decline, although decline for Lepidoptera is less severe than for other taxa (19) .
• Data in panels B-D are effect size (ln(exclosure metric/control metric)) after large wildlife removal.

Full text

Defaunation in the Anthropocene
1
2
Rodolfo Dirzo
1*
, Hillary S Young
2
, Mauro Galetti
3
, Gerardo Ceballos
4
, Nick JB Isaac
5
,
3
Ben Collen
6
4
5
1
Department of Biology, Stanford University, Stanford, CA 94305, USA
6
2
University of California Santa Barbara, Santa Barbara, CA 93106, USA
7
3
Departamento de Ecologia, Universidade Estadual Paulista, Rio Claro, SP, 13506-900,
8
Brazil
9
4
Instituto de Ecología, Universidad Nacional Autonoma de Mexico, AP 70-275, Mexico
10
D.F. 04510, Mexico
11
5
NERC Centre for Ecology & Hydrology, Benson Lane, Crowmarsh Gifford,
12
Oxfordshire, OX10 8BB, UK
13
6
Centre for Biodiversity & Environment Research, Department of Genetics, Evolution &
14
Environment, University College London, Gower Street, London WC1E 6BT, UK
15
16
17
18
*
To whom correspondence should be addressed. E-mail: rdirzo@stanford.edu
19
Word count: 4807 words, 80 references, 5 figures
20

We live amidst a global wave of anthropogenically driven biodiversity loss: species
21
and population extirpations and, critically, declines in local species abundance. Human
22
impacts on animal biodiversity, particularly, are an under-recognized form of global
23
environmental change. Among terrestrial vertebrates 322 species have become
24
extinct since 1500, while populations of the remaining species show 25% average
25
decline in abundance. Invertebrate patterns are equally dire: 67% of monitored
26
populations show 45% mean abundance decline. Such animal declines will cascade
27
onto ecosystem functioning and human well-being. Much remains unknown about
28
this “Anthropocene defaunation”; these knowledge gaps hinder our capacity to
29
predict and limit defaunation impacts. Clearly, however, defaunation is both a
30
pervasive component of the planet’s sixth mass extinction, and also a major driver of
31
global ecological change.
32
33
In the past 500 years, humans have triggered a wave of extinction, threat, and local
34
population declines that may be comparable in both rate and magnitude to the five
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previous mass extinctions of Earth’s history (1). Similar to other mass extinction events,
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the effects of this “sixth extinction wave” extend across taxonomic groups, but are also
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selective, with some taxonomic groups and regions being particularly affected (2). Here,
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we review the patterns and consequences of contemporary anthropogenic impact on
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terrestrial animals. We aim to portray the scope and nature of declines of both species and
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abundance of individuals, and examine the consequences of these declines. So profound
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is this problem, that we have applied the term defaunation to describe it. This recent pulse
42

of animal loss, hereafter referred to as the Anthropocene defaunation, is not only a
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conspicuous consequence of human impacts on the planet, but also a primary driver of
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global environmental change in its own right. In comparison, we highlight the profound
45
ecological impacts of the much more limited extinctions, predominantly of larger
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vertebrates, that occurred during the end of the last Ice Age. These extinctions altered
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ecosystem processes and disturbance regimes at continental scales, triggering cascades of
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extinction thought to still reverberate today (3, 4).
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The term defaunation, used to denote the loss of both species and populations of
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wildlife (5), as well as local declines in abundance of individuals, needs to be considered
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in the same sense as deforestation, a term that is now readily recognized and influential in
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focusing scientific and general public attention on biodiversity issues (5). However,
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whilst remote sensing technology provides rigorous quantitative information and
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compelling images of the magnitude, rapidity and extent of patterns of deforestation,
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defaunation remains a largely cryptic phenomenon. It can occur even in large protected
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habitats (6) and, yet, some animal species are able to persist in highly modified habitats,
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making it difficult to quantify without intensive surveys.
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Analyses of the impacts of global biodiversity loss typically base their
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conclusions on data derived from species extinctions (1, 7, 8) and typically evaluations of
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the effects of biodiversity loss draw heavily from small scale manipulations of plants and
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small sedentary consumers (9). Both of these approaches likely underestimate the full
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impacts of biodiversity loss. While species extinctions are of great evolutionary
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significance, declines in the number of individuals in local populations and changes in the
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composition of species in a community will generally cause greater immediate impacts
65

on ecosystem function (8, 10). Moreover, while the extinction of a species often proceeds
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slowly (11), abundance declines within populations to functionally extinct levels can
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occur rapidly (2, 12). Actual extinction events are also hard to discern, and IUCN threat
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categories amalgamate symptoms of high risk, conflating declining population and small
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populations, such that counts of threatened species do not necessarily translate into
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extinction risk, much less ecological impact (13). Whilst the magnitude and frequency of
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extinction events remain a potent way of communicating conservation issues, they are
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only a small part of the actual loss of biodiversity (14).
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The Anthropocene Defaunation Process
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Defaunation: a pervasive phenomenon
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Of a conservatively estimated 5-9 million animal species on the planet, we are likely
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losing ~11,000 to 58,000 species annually (15, 16). However, this does not consider
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population extirpations and declines in animal abundance within populations.
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Across vertebrates, 16% to 33% of all species are estimated to be globally
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threatened or endangered (17, 18), and at least 322 vertebrate species have become
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extinct since 1500 (a date representative of onset of the recent wave of extinction, as
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formal definition of the start of the Anthropocene still being debated) (17, 19, 20) (Table
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S1). From an abundance perspective, vertebrate data indicate a mean decline of 28% in
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number of individuals across species in the last four decades (14, 21, 22) (Fig S1A), with
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populations of many iconic species such as elephant (Fig S1B) rapidly declining towards
86
extinction (19).
87
Loss of invertebrate biodiversity has received much less attention and data are
88

extremely limited. However, data suggest that the rates of decline in numbers, species
89
extinction, and range contraction among terrestrial invertebrates are at least as severe as
90
among vertebrates (23, 24). Although less than 1% of the 1.4 million described
91
invertebrate species have been assessed for threat by the IUCN, of those assessed, around
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40% are considered threatened (17, 23, 24). Similarly, IUCN data on the status of 203
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insect species in five orders reveals vastly more species in decline than increasing (Fig
94
1A). Likewise, for the invertebrates where trends have been evaluated in Europe, there is
95
a much higher proportion of species with numbers decreasing rather than increasing (23).
96
Long term distribution data on moths and four other insect Orders in the UK show that a
97
substantial proportion of species have experienced severe range declines in the last
98
several decades (19, 25) (Fig 1B). Globally, long-term monitoring data on a sample of
99
452 invertebrate species indicate that there has been an overall decline in abundance of
100
individuals since 1970 (19) (Fig 1C). Focusing on just the Lepidoptera (butterflies and
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moths), for which the best data are available, there is strong evidence of declines in
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abundance globally (35% over 40 years, Fig 1C). Non-Lepidopteran invertebrates
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declined significantly more, indicating that estimates of decline of invertebrates based on
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Lepidoptera data alone are conservative (19) (Fig 1C). Likewise, among pairs of
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disturbed and undisturbed sites globally, Lepidopteran species richness is on average 7.6
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times higher in undisturbed than disturbed sites, and total abundance is 1.6 times greater
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(19) (Fig 1D).
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Patterns of defaunation
110
Though we are beginning to understand the patterns of species loss, we still have a
111
limited understanding of how compositional changes in communities following
112

Frequently asked questions

Q1. What have the authors contributed in "Defaunation in the anthropocene" ?

Rodolfo Dirzo et al. this paper, Hillary S Young, Mauro Galetti, Gerardo Ceballos, Nick JB Isaac5, Ben Collen6 4 5 1 Department of Biology, Stanford University, Stanford, CA 94305, USA 6 2 University of California Santa Barbara, Santa Barbara CA 93106, USA 7 3 Departamento de Ecologia, Universidade Estadual Paulista, Rio Claro, SP, 13506-900, 8 Brazil 

Q2. What are the main drivers of defaunation in terrestrial ecosystems?

156 157Multiple, unaddressed drivers of defaunation 158extinction in terrestrial ecosystems, namely overexploitation, habitat destruction, and 160 impacts from invasive species remain pervasive (18). 

Q3. What is the impact of defaunation on the ecosystem?

176 177Consequences of defaunation 178As animal loss represents a major change in biodiversity, it is likely to have important 179 effects on ecosystem functioning. 

Q4. What is the impact of decomposition on the ecosystem?

The diversity of invertebrate communities, 209 particularly their functional diversity, can have dramatic impacts on decomposition rates 210 and nutrient cycling (59-61). 

Q5. What is the impact of defaunation on other species?

Since defaunation of vertebrates often 248 selects on body size, and smaller individuals are often unable to replace fully the 249 ecological services their larger counterparts provide, there is strong potential for 250studied are the indirect evolutionary effects of defaunation on other species, not directly 252 impacted by human defaunation. 

Q6. What are the effects of a devaunation on human health?

Defaunation will affect human health in many other ways, via 222 reductions in ecosystem goods and services (65) including pharmaceutical compounds, 223 livestock species, biocontrol agents, food resources and disease regulation. 

Q7. Why have these ‘extinction models’ made little impact on conservation management?

these ‘extinction models’ have made 131 little impact on conservation management, in part because trait correlations are often 132 idiosyncratic and context dependent (31). 

Q8. What is the important thing to know about the extinction of invertebrates?

87 Loss of invertebrate biodiversity has received much less attention and data are 88extinction, and range contraction among terrestrial invertebrates are at least as severe as 90 among vertebrates (23, 24). 

Q9. How does the use of statistical models help to understand patterns of biodiversity loss?

124 The use of statistical models based on life history characteristics (traits) has 125 gained traction as a way to understand patterns of biodiversity loss (31). 

Q10. How many species have experienced severe range declines in the last 98 several decades?

96 Long term distribution data on moths and four other insect Orders in the UK show that a 97 substantial proportion of species have experienced severe range declines in the last 98 several decades (19, 25) (Fig 1B). 

Q11. What is the effect of large wildlife removal on the ecosystem?

Changes 351 in animal abundance from low (blue, L) to high (red, H) within a region have been shown 352 to affect a wide range of ecological processes and services (19) including: A) seed 353 dispersal (flying foxes), B) litter respiration and decomposition (seabirds), C) carrion 354 removal (vultures), D) herbivory (large mammals), E) water quality and stream 355 restoration (amphibians), F) trampling of seedlings (mammals), G) dung removal (dung 356 beetles), H) pollination and plant recruitment (birds), I) carbon cycling (nematodes), and 357 J) soil erosion and cattle fodder (prairie dogs). 

Q12. What is the effect of defaunation on the environment?

the effects of defaunation will be much less about 271 the loss of absolute diversity than about local shifts in species compositions and 272 functional groups within a community (80). 

Q13. What are the impacts of defaunation on the ecology of a species?

242243 Impacts on evolutionary patterns 244The effects of defaunation appear not just proximally important to the ecology of 245 impacted species and systems, but also have evolutionary consequences.