Bushmeat Hunting and Extinction Risk to the World's Mammals

Terrestrial mammals are experiencing a massive collapse in their population sizes and geographical ranges around the world, but many of the drivers, patterns and consequences of this decline remain poorly understood. Here we provide an analysis showing that bushmeat hunting for mostly food and medicinal products is driving a global crisis whereby 301 terrestrial mammal species are threatened with extinction. Nearly all of these threatened species occur in developing countries where major coexisting threats include deforestation, agricultural expansion, human encroachment and competition with livestock. The unrelenting decline of mammals suggests many vital ecological and socio-economic services that these species provide will be lost, potentially changing ecosystems irrevocably. We discuss options and current obstacles to achieving effective conservation, alongside consequences of failure to stem such anthropogenic mammalian extirpation. We propose a multipronged conservation strategy to help save threatened mammals from immediate extinction and avoid a collapse of food security for hundreds of millions of people.

rsos.royalsocietypublishing.org
Research
Cite this article: Ripple WJ et al. 2016
Bushmeat hunting and extinction risk to the
world’s mammals R. Soc. open sci. 3: 160498.
http://dx.doi.org/10.1098/rsos.160498
Received: 10 July 2016
Accepted: 20 September 2016
Subject Category:
Biology (whole organism)
Subject Areas:
ecology
Keywords:
wild meat, bushmeat, hunting, mammals,
extinction
Author for correspondence:
William J. Ripple
e-mail: [e-mail]
Electronic supplementary material is available
onlineat http://dx.doi.org/10.6084/m9.
figshare.c.3500397.
Bushmeat hunting an
extinction risk to the
mammals
William J. Ripple1,2, Katharine Abernethy4,5,
Matthew G. Betts1,2, Guillaume Chapron6,
Rodolfo Dirzo7, Mauro Galetti8,9, Taal Levi1,2,3,
Peter A. Lindsey10,11, David W. Macdonald12,
Brian Machovina13, Thomas M. Newsome1,14,15,16,
Carlos A. Peres17, Arian D. Wallach18,
Christopher Wolf1,2and Hillary Young19
1GlobalTrophic Cascades Program, Department of Forest Ecosystem
2Forest Biodiversity Research Network, Department of Forest Ecosy
and3Department of Fisheries and Wildlife, Oregon State University, C
OR 97331, USA
4School of Natural Sciences, University of Stirling, Stirling FK9 4LA,
5Institut de Recherche en Ecologie Tropicale, CENAREST, BP 842 Lib
6Grimsö Wildlife Research Station, Department of Ecology, Swedish
Agricultural Sciences, 73091 Riddarhyttan, Sweden
7Department of Biology, Stanford University, Stanford, CA 94305, U
8Universidade Estadual Paulista (UNESP), Instituto Biociências, Dep
Ecologia, 13506-900 Rio Claro, São Paulo, Brazil
9Department of Bioscience, Ecoinformatics and Biodiversity, Aarhu
8000 Aarhus, Denmark
10Panthera, 8 West 40th Street, 18th Floor, New York, NY 10018, US
11Mammal Research Institute, Department of Zoology and Entomolo
Pretoria, Pretoria, Gauteng, South Africa
12Wildlife Conservation Research Unit, Department of Zoology, Univ
The Recanati-Kaplan Centre, Tubney House, Tubney, Abingdon OX
13Department of Biological Sciences, Florida International University
USA
14School of Life and Environmental Sciences, Centre for Integrative
Deakin University, Burwood campus, Geelong, Victoria 3125, Austr
15School of Life and Environmental Sciences, The University of Sydn
Wales 2006, Australia
16School of Environmental and Forest Sciences, University of Washi
WA 98195, USA
17School of Environmental Sciences, University of East Anglia, Norw
18Centre for Compassionate Conservation, School of Life Sciences, U
Technology Sydney, PO Box 123 Broadway, New South Wales 2007
2016 The Authors. Published by the Royal Society under the terms o
Attribution License http://creativecommons.org/licenses/by/4.0/,which permits unrestricted
use, provided the original author and source are credited.

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19Department of Ecology and Evolutionary Biology, University of California Santa Barbara, Santa Barbara
WJR, 0000-0001-6557-3043; TMN, 0000-0003-3457-3256;
CW, 0000-0002-5519-3845; HY, 0000-0003-0449-8582
Terrestrial mammals are experiencing a massive collapse in their population sizes and geographical
ranges around the world,but many of the drivers,patterns and consequences ofthis decline
remain poorly understood. Here we provide an analysis showing that bushmeat hunting for mostly
food and medicinal products is driving a global crisis whereby 301 terrestrial mammal species are
threatened with extinction.Nearly allof these threatened species occur in developing countries
where major coexisting threats include deforestation,agricultural expansion,human encroachment
and competition with livestock. The unrelenting decline of mammals suggests many vital ecological
and socio-economic services that these species provide will be lost, potentially changing ecosystems
irrevocably. We discuss options and current obstacles to achieving effective conservation, alongside
consequences of failure to stem such anthropogenic mammalian extirpation.We propose a multi-
pronged conservation strategy to help save threatened mammals from immediate extinction and
avoid a collapse of food security for hundreds of millions of people.
1.Introduction
Rapid loss of biodiversity in recent times indicates that a sixth mass extinction event is underway on
the Earth,whereby the average rate of vertebrate species loss is now up to 1000 times higher than
background rates [1]. Population sizes of vertebrate species have been declining, mainly due to the tw
threats of direct exploitation and habitat destruction [2,3]. Unsustainable hunting for consumption and
trade of wild meat (also known as bushmeat) by humans represents a significant extinction threat to
wild terrestrial mammal populations, perhaps most notably in parts of Asia, Africa and South America
[4–6]. Here, we refer to predominantly unregulated (and often illegal and unsustainable) harvesting of
wildlife for human consumption as ‘bushmeat hunting’ or ‘wild meat’ hunting.This is distinguished
from legal or regulated hunting of wildlife which can be sustainable. This global bushmeat hunting cri
is a fundamentally distressing problem to address because it is intimately tied to human development
challenges such as food insecurity, emergent disease risks and land-use changes [7]. While many ethn
groups have hunted wildlife for subsistence over millennia,often with highly detrimental effects [8],
the unsustainablility of this practice has accelerated in many areas due to growing human populations
an increasing tendency for wild meat to be traded commercially [9],and the widespread adoption of
firearms and motorized transport that increase the efficiency and spatial extent of hunting [10,11]. La
species are typically targeted by bushmeat hunters first and are also the least able to bear hunting off
[12–14]. As wildlife populations outside protected areas decline, poaching pressure is increasing in ma
parks and reserves. As a consequence many forests, savannahs, grasslands and deserts in the develop
world are now becoming ‘empty landscapes’ [14] devoid of harvest-sensitive wild mammals [15–17].
Herein,we present the first comprehensive global assessment of hunting on the world’s terrestrial
mammals, and provide new data and insights based on our analysis (box 1). We report on the species
most severely threatened by bushmeat hunting and review trends in their endangerment status.We
analyse the geographicaldistributions ofcritically overhunted mammals and determine the extent
to which their ranges are protected.We highlighthow spatially and taxonomically biased research
efforts have impeded recognition of both the declines of smaller or less iconic species and also the
importance of their ecological roles. In some cases, these species may already be ecologically defunct
ecosystem interactions virtually absent. We discuss growing evidence that ecological functionality can
necessarily be replaced, leading to cascading alterations of ecosystems, the loss of ecological interacti
and the loss of other ecosystem and social services [18,19]. We conclude by outlining pathways to bett
understand human predatory behaviour and we provide a conservation plan for the twenty-first centur
Only bold changes will substantially diminish the imminent possibility of humans consuming many of
the world’s wild mammals to the point of functional [20] or global [19,21] extinction.
2.Severe impacts of hunting on mammal species
According to the InternationalUnion for Conservation of Nature (IUCN),1169 of the world’s 4556
assessed terrestrial mammals (approx.26%) are listed as threatened with extinction [22].Here,using

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. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Dermoptera (colugos) − 0/2
Hyracoidea (hyraxes) − 0/5
Microbiotheria (monito del monte) − 0/1
Tubulidentata (aardvark) − 0/1
Didelphimorphia (opossums) − 0/81
Scandentia (treeshrews) − 0/17
Dasyuromorphia (quolls and dunnarts) − 0/69
Chiroptera (bats) − 27/942
Cingulata (armadillos) − 3/16
Rodentia (rodents) − 21/1854
Lagomorpha (rabbits, hares and pikas) − 1/84
Eulipotyphla (shrews, moles and hedgehogs) − 0/366
Macroscelidea (elephant shrews) − 0/13
Carnivora (carnivores) − 12/232
Pilosa (anteaters and sloths) − 0/10
Diprotodontia (diprotodont marsupials) − 26/137
Paucituberculata (shrew opposums) − 0/6
Afrosoricida (tenrecs and golden moles) − 0/50
Peramelemorphia (bilbies and bandicoots) − 1/16
Cetartiodactyla (even-toed ungulates) − 65/217
Monotremata (platypus and echidnas) − 3/5
Primates (primates) − 126/406
Perissodactyla (odd-toed ungulates) − 8/16
Pholidota (pangolins) − 8/8
Proboscidea (elephants) − 0/2
0% 20% 40% 60% 80% 100%
per cent of species
species threatened by hunting for human consumption
other threatened species
Figure 1. The percentage of species threatened by hunting for human consumption and other
order. The values on the x-axis refer to the percentage of species out of all mammal species i
species’ consists of the other threatened mammal species where hunting for consumption is n
are sorted from highest to lowest total percentage of threatened species in each order. Numb
the number of species threatened by hunting followed by the total number of species in the o
but not listed here because they are predominately killed for their ornamental ivory and not fo
(see [14]). The order Notoryctemorphia (marsupial moles) was omitted as it contains only dat
mass (kg)
(a) (b)
0.01
0.1
1
10
100
1000
10 000
0255075100125
no. species
0 20 40 60 80 100
per cent of species
bats carnivores diprotodonts even-toed ungulates primates rodents other
no. threatened by hunting per cent threatened by hunting
Figure 2. Number (a) and percentage (b) of mammal species threatened by hunting grouped
correspond to species threatened by hunting out of all terrestrial mammals in each body mas
from [23–25].
individual species accounts from the IUCN Red List,we identify 301 threatened mammal species for
which a primary threat is hunting by humans (see materials and methods in electronic supplementary
material,table S1).This group of heavily hunted mammals represents 12 of the 26 extant terrestrial
orders, approximately 7% of all assessed terrestrial mammals and approximately 26% of all threatened

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Box 1. Overview.
Our assessment revealed the following:
— This is the first global assessment of mammal hunting and results show evidence of a global crisis
— 301 terrestrial mammal species are threatened with extinction due to hunting by humans. All of
these species occur in developing countries.
— Orders with the most species threatened by hunting include primates, even-toed ungulates, bats,
diprotodont marsupials, rodents and carnivores.
— The primary reason for hunting and trapping these mammals is to acquire meatfor human
consumption, medicinal products, ornamental use and pet trade.
— The likelihood of extinction threat of heavily hunted mammals is proportional to body size.
— Only 2% of the mammals threatened by hunting have populations considered stable or increasing
— These heavily hunted mammalspecies have,on average,only 10.5% oftheir ranges within
protected areas.
— Regions with the most species threatened by hunting include Asia (especially SE Asia) and Africa.
— Countries with the most endemic species threatened by hunting include Madagascar, Indonesia,
Philippines, Brazil, Papua New Guinea, India and China.
— Species affected by severe hunting are also often victims of habitatdeterioration,expanding
agriculture, human settlement encroachment and livestock competition.
— Through cascading effects, the loss of these mammals is altering the structure and function of the
environments in which they occur, and this could result in a loss of food security for humans.
— Based on the number of published articles, there is a research bias favouring the heavier species
and those found in Africa.
— There has been little conservation progress in reversing the fate of these threatened mammals
despite several major summits convened on biodiversity conservation and protected areas.
terrestrialmammalspecies on the Earth (figure 1).Endangermentcategories for these 301 species
include 115 vulnerable (VU = 38%), 114 endangered (EN = 38%) and 72 critically endangered (CR =
Orders with the most species threatened by hunting include primates (126 species), even-toed ungulat
(Cetartiodactyla,65 species),bats (Chiroptera,27 species),diprotodontmarsupials (Diprotodontia,
26 species),rodents (Rodentia,21 species)and carnivores (Carnivora,12 species).Orders with the
highest percentages of species threatened by hunting include pangolins (Pholidota,100%),platypus
and echidnas (Monotremata, 60%), odd-toed ungulates (Perissodactyla, 50%), primates (31%) and eve
toed ungulates (30%).Mammal species threatened by hunting consist predominantly of ungulates for
large-sized mammals (more than 10 kg),primates for medium-sized mammals (1–10 kg) and bats for
small-sized mammals (less than 1 kg) (figure 2a).
2.1.Drivers of mammal hunting
The primary reason for hunting and trapping these 301 threatened mammalspecies is to acquire
meat for human consumption (n = 285) and this occurs nearly entirely in developing countries across
Africa,South America and particularly Southeast Asia (electronic supplementary material,figure S3).
Other major reasons for hunting include consumption of body parts as traditionalmedicine (n = 67
species),live animals for the pet trade (n = 46) and ornamental uses of body parts (n = 36) (electronic
supplementary material,figure S4).Species hunted for medicinaluse primarily involves primates
(n = 25) and ungulates (n = 25),but also various other taxa such as carnivores (n = 8) and pangolins
(n = 8). Live trade mostly includes primates (n = 31), while ornamental uses (ivory, horns, antlers, ski
etc.) largely involve ungulate (n = 17),carnivore (n = 7) and primate (n = 6) species.Ornamentaluse
includes animalparts from trophy hunts.Live trade and ornamentaluse of wild mammals occurs
primarily in SoutheastAsia and secondarily in Africa and Latin America (South America,Central
America, Caribbean).
2.2.Distribution of impacts by body size
Mammalspecies threatened by hunting in the 1–10 kg mass group are the most numerous (n = 120)
while those weighing 10–100 kg rank second (n = 54) compared with other body mass classes (figure
However,considering the percentage ofspecies within each mass category,the likelihood ofthreat

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is proportionalto body size with a higher proportion oflarger species particularly threatened by
hunting,culminating in close to 60% of our largest terrestrial mammals (more than 1000 kg) being at
risk of extinction from human consumption (figure 2b). Mammals threatened by hunting include specie
with a multitude of ecologicalroles from different levels of the food web,including apex predators,
mesopredators, herbivores in all size classes, seed dispersal agents, pollinators and prey species.
2.3.Population trends of hunted species
Population trends of these species continue to worsen over time,with only 2% of these populations
considered stable or increasing (electronic supplementary material, table S1 and S2). Between 1996 a
2008 (or later for more recently updated species), the conservation status of 23% of the heavily hunted
mammal species deteriorated (63 of 270 species with data available), while only one species improved
and the rest(n = 206;76%)remained stable.However,40 species were already classed as critically
endangered by 1996, indicating there has been little or no conservation progress in reversing their fat
since then despite several major summits convened on biodiversity conservation and protected areas
(electronic supplementary material, table S2). Indeed, primates and even-toed ungulates had the high
number of species whose status deteriorated between 1996 and 2008 (23 and 16, respectively).
2.4.Geographical distribution of hunting impacts
The impact of mammal hunting on species endangerment differs among continents, and does not refle
closely parallel global patterns of mammal richness [26] (figure 3, S1). There are 113 species threaten
by hunting in Southeast Asia (13% of all threatened mammals are east of India and south of China), 91
in Africa (8%),61 in the rest of Asia (7%),38 in Latin America (3%) and 32 in Oceania (7%) (figure 3,
electronic supplementary material,figure S1).Notably,all of the 301 mammals that are threatened by
hunting are found in developing countries, and only eight of these species are also found in developed
countries, suggesting a huge contrast in dietary patterns, wildlife management and conservation effor
between the developing and developed world.However,part of this difference may be an artefact
of humans extirpating megafauna in developed temperate regions during the Late Pleistocene [27].
Countries with the most endemic species (present in a single country) threatened by hunting include
Madagascar (n = 46), Indonesia (n = 37), Philippines (n = 14), Brazil (n = 10), Papua New Guinea (n =
India (n = 6) and China (n = 5) (electronic supplementary material, figure S2).
Of the 301 hunted threatened species, three are already possibly extinct including the kouprey (Bos
sauveli),Wondiwoi tree-kangaroo (Dendrolagus mayri) and little earth hutia (Mesocapromys sanfelipens
(electronic supplementary material,table S1).The remaining 298 species have an average of 10.5% of
their ranges within IUCN Class I–III protected areas and the majority (n = 162) have less than 5% of t
ranges within protected areas (electronic supplementary material, figure S5 and table S3); 65 have ra
falling entirely outside protected areas.
2.5.Effects of unselective hunting methods
In some regions,wild meat is primarily obtained with traps and snares,but this is almost completely
unselective and generates substantialbycatch [28].In CentralAfrica,snare losses to scavengers and
decomposition of the target species result in the wastage of up to a quarter of total captures [29]. This
is also an important animal welfare problem, because up to one-third of animals escape with injury an
unknown subsequent fates [29].A study in Zimbabwe indicated that more than 1400 large mammals
rotted and were wasted in snares over a 4-year period [30],with more animals rotting in snare-lines
far from human settlements [31].Unselective traps result in the capture of females and young,which
confers much greater impacts for the many polygynous ungulate species than if harvests were restrict
to adult males [17] (although for species that practise infanticide, such as bears and lions, killing male
can be just as problematic). Even traditional forms of subsistence hunting can result in over-exploitati
of particular species when human population density increases [32,33].
2.6.Additional factors exacerbating extinction risk
As hunting is facilitated by access to land [16] and the human footprint is increasing across the globe
[34,35],species and regions affected by severe hunting are also often victims of habitat deterioration

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richness
index
1−38
39−71
72−116
117−175
176−291
richness
index
1−4
5−9
10−14
15−18
19−24
(a)
(b)
Figure 3. Species richness maps for (a) all terrestrial mammals and (b) mammals threatened
of many types including forest loss and fragmentation (n = 184 hunted species), expanding agriculture
(n = 152),human settlementencroachment(n = 34)and livestock competition (n = 27)(electronic
supplementary material,figure S6).Geographically these contributory factorsvary; deforestation
predominantly affects mammals of Southeast Asia, Central and West Africa, Madagascar, Amazonia an
the Atlantic Forest of South America; agriculture and human settlement encroachment are major thre
in Southeast Asia; and competition with livestock occurs across southern Asia, much of Africa and par
of South America (electronic supplementary material, figure S7).
3.Consequences of overhunting
Hunting and the trade of wild meat and body parts has long been recognized as a severe problem for
a range of mammal species. This pervasive pressure on ecosystems can have wide-ranging effects that
cascade beyond the loss of the hunted species, altering the structure and function of the environments
which they occur and the services they provide [36,37]. Wild meat is currently an important food sour
for humans worldwide. An estimated 89 000 metric tons of meat with a market value of approximately
$200 million are harvested annually in the Brazilian Amazon [38],and exploitation rates oflarge
mammals in the Congo basin are estimated to be five times higher than in the Brazilian Amazon [4]. W
this trend, the loss of mammal populations thus affects the livelihoods and food security for hundreds
millions of rural people across the globe [39].

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3.1.Cascading effects: large mammals
Mammals dominate the larger size classes of the modern animal kingdom and the severe overhunting
describe here is having a disproportionate impact on the largest species (figure 2b). This is contributin
to dramatic global-scale population declines and range contractions for many large-bodied mammals
[14,40–44]. As human hunters on all continents target mammals [45], and especially large-bodied ones
the ecological disruption of unsustainable human hunting is extensive—whether driven by subsistence
or commercial hunting [46,47]. Since the Pleistocene, extinction has affected larger mammals more th
smaller ones [19] and we suggest that contemporary extinction risk from overhunting is still a primary
threat for the largest terrestrial mammals.
Large-bodied predators and herbivores provide ‘top-down’control on ecosystems,which helps to
balance the effects of environmental,or ‘bottom-up’factors,such as primary productivity or climate.
Their roles are crucial to ecosystem stability and their loss can result in particularly rapid, widespread
and potentially irrevocable changes [13,14,18,48].As no other taxonomic group contains terrestrial
animals in the size classes of the large modern mammals, the functional loss of large mammals can ra
be compensated, leading to permanent ecosystem changes [49]. Even in the absence of targeted hunti
large predators may not survive competition with humans as their prey base is depleted by hunting
[17,50,51].Some large mammals perform non-redundant seed dispersal services for very large-seeded
plants [52,53] and their local extirpation may lead to an increase in rodent populations and seed preda
[54]. All of these examples highlight not only the importance of mammals for ecosystem functioning, b
for ecosystem services to humans.
3.2.Cascading effects: small mammals
Hunting smaller mammals can also drive insidious alterations ofecosystems,as they can provide
critical ecological functions including seed dispersal, consumption of vegetation and invertebrates, soi
disturbance and prey items for other species. Of these functions, the role of smaller frugivorous mamm
as seed dispersers,particularly primates and bats,has been the most clearly documented.Removal of
these seed dispersers can initiate widespread changes in forest regeneration, composition and structu
[55–57], and despite the overlap in their body size with birds and reptiles, studies show that the ecolog
role of mammals is not always replaceable by other taxa [58,59].Likewise,some bat species serve as
specialized pollinators and seed dispersers that are unlikely to be replaced. Yet bats are the largest gr
of mammals under 1 kg threatened by hunting [60].
Some smaller species are not targeted by human hunters (less than 1 kg,figure 2a) and as hunting
removes the larger mammals from ecosystems,especially large herbivores that compete with smaller
species [14],these smallspecies can experience ecologicalrelease with some populations increasing
substantially [54,61].However,even super-abundantsmall prey cannotsustain large predators,as
the energy required to catch and process multiple carcasses is notreplaced because oftheir small
biomass [62].As such,the smallmammalpopulation remains unchecked,changing a wide range of
species interactions and contact rates. The release of smaller mammals, particularly rodents, can beco
a dominantmechanism by which the effects ofhuman hunting can cascade into transformation of
invertebrate and plant communities [19].
3.3.Behavioural changes in target species
Mammals can employ complex predator avoidance strategies when faced with severe hunting pressure
by humans. However, these survival strategies can have eco-evolutionary implications if direct costs a
incurred from increased energy expenditure and reduced foraging time in human-mediated ‘landscape
of fear’ [62,63]. Changing hunter avoidance behaviours to become more nocturnal or more cryptic, ca
for example, lead to a reduction in hunting success for other predators competing with humans. Hunte
avoidance that involves prey species moving to a perceived sanctuary area can also lead to conservatio
dilemmas [64]. In the last few decades, fencing of protected areas has been used as a tool to help cont
overhunting,in an attempt to reduce human incursions and prevent the movement of wildlife into
unprotected landscapes. However, fencing restricts animal movements, reduces effective park sizes an
destroys ecological connectivity [65,66].
3.4.Zoonotic diseases
The loss of large mammals,and in particular,the selective loss ofprimates,large ungulates and
carnivores,may have strong consequences for zoonotic disease transmission.In the short term,high

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levels of contact with these species during the exploitation phase may increase transmission risk to
humans. Hunting and butchering allow for high levels of direct contact of body fluids and are thought
to have been important in emergence of Ebola,HIV-1 and -2,Anthrax,Salmonellosis,Simian foamy
virus and other zoonotic diseases [67]. Given high rates of international trade in wild meat and human
movement,this could easily have important short-term global health consequences [68].However,in
the longer run the extirpation and endangerment of these species willalmost certainly result in the
co-extinction of many parasites and pathogens,likely to include some potentialzoonotic pathogens
[69,70].Yet,hunting in particular may continue to cause increases in zoonotic disease risk because of
the selective nature of losses following hunting.The selective loss of large herbivores,for instance,is
known to cause relatively systematic increases in abundance of rodents [71],which are thought to be
particularly effective at hosting and transmitting human-borne zoonoses, thus driving landscape-level
increases in rodent-borne disease [72].Increases of rodents following large herbivore loss appear to
be much more systematic than following other types of disturbance [73] probably due to generalized
competitive release of herbivorous and granivorous rodents.This pattern may result in more rodent-
borne diseases.Systematic predator loss may also tend to cause increases in disease risk,although
mesopredator release could counter such a pattern in some systems [74]. There is also some evidence
smaller hosts, with faster life histories, tend to be more competent reservoirs for some common zoono
regardless of trophic cascades; as hunting favours these species both directly and indirectly, this may
to systematic increases in zoonotic disease prevalence [75]. Certainly, smaller species are likely to be
abundant and in closer contact with humans, allowing more transmission opportunities.
3.5.Loss of food security for humans
The effects of unsustainable hunting are borne not just by the target species and their ecosystems, but
unsustainability becomes apparent and hunting returns decline, by the hunter communities themselve
Our analysis shows that overhunting of threatened mammals is most common in developing countries,
which is driving many of these mammals towards extinction. These countries by definition have poorer
populations, generally lower food security than richer countries, and less capacity to deliver conservat
[76].Ensuring current food security without changing current hunting practices will inevitably fail to
provide food security in years to come [39,77]. As hunters using unsustainable practices become unab
to make ends meet,they may leave the hunting community and migrate [78],switch to less preferred
species, increasing ecological impacts [45] or, with their families, begin to suffer malnutrition and crit
poverty [77]. None of these scenarios are appealing as future situations for these people. In addition, l
mammalcommunities offer potentialto generate human food security with their income-generating
capacity through tourism. Such potential is increasingly forgone as wildlife populations are overhunte
for a much lower value product: meat [16].
4.Research and knowledge gaps
To achieve better conservation policies and practices for our surviving mammals,science must first
provide a better platform for decision-making in identifying changes in wildlife populations and
ecosystems. Our analysis of the mammals endangered by hunting shows a significant bias in the regio
and species benefitting from research effort(figure 4).Many of the mammalspecies threatened by
hunting remain poorly studied and are greatly in need ofbasic biologicaland ecologicalresearch,
including simple evaluation of their remaining numbers.For example,some pangolin species may be
approaching extinction in numerous areas due to hunting for medicinal products,but little is known
about their remaining numbers [79].Likewise,many populations are likely to have been already
impacted when first assessed,leaving them vulnerable to the ‘shifting baseline’ effect, which prevents
robust evaluation of the loss of their ecological role (electronic supplementary material, table S1).
Scientific research effort,as measured by the number ofpublished articles on each species,has
been relatively low in Southeast Asia (figure 4).The relative lack of research effort in this region is a
major conservation issue as Southeast Asia has many more threatened and harvest-sensitive mammal
species than mostother regions (electronic supplementary material,figure S1).The generalpublic
prefers larger species [80],which also get more attention from researchers.Proportionally,research as
depicted by the number of articles per threatened mammal species is positively correlated to species b
mass (p < 0.001) (electronic supplementary material, figure S8). Therefore, designing sound conserva
policies, or predicting the ecosystem effects of loss of the species with lower body masses, particularly
outside Africa,is hampered.There is also a greatneed for comprehensive research on the world’s

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. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
median
articles
0−80
81−161
161−241
242−422
423−938
published articles on species threatened by hunting
Figure 4. Research effort for mammal species threatened by hunting. The variable shown is th
between 1965 and 2016 for all of the species threatened by hunting found in each hexagon (s
birds and reptiles, which are often threatened by hunting, also with strong ecological and evolutionary
consequences, but not covered in this review.
The geography of risk posed by hunting is likely to be biased by the fact that data for this study are
derived from IUCN Red List data. These data are likely to place disproportionate emphasis on those ar
which have long-standing problems with hunting, restricted species ranges and where there are multip
threats facing wildlife. Thus, our IUCN-derived spatial data on risks to mammals do not completely ali
with data on those areas that are experiencing extraordinarily high,and increasing,take in bushmeat
such as in the Congo basin [4]. However, the ground-level data needed for comparative rates of harves
are unfortunately not available on a global scale.
Good conservation paradigms cannotbe built only on ecologicalunderstanding;they require a
sophisticated evaluation of the drivers of human behaviour and insight and innovation as to how that
behaviour may be changed. Understanding the drivers of human behaviour is a key step to designing
effective alternatives [81]. Research into human drivers of unsustainable harvesting is a relatively new
field and more cross-disciplinary exchange is needed between ecologists, socio-economists and human
behaviour specialists in order to tackle mammal over-harvesting.
5.Moving forward with five conservation actions
Growing human populations,increasing middle-classwealth, accessto hunting technologiesin
developing nations and the modern ease of transporting goods around the planet are facilitating a glob
demand for wild animals as food and other products that simply cannot be met by current global wildl
populations. Furthermore, the growing penetration of remote landscapes by road networks is resulting
in a lack of faunal refugia. The brunt of this overconsumption is borne by mammals, though many othe
taxa are also impacted (e.g. birds, fish, reptiles). In order to maintain viable and functional population
of these species, we must find ways to curb our unsustainable consumption of mammal species that ar
threatened or dramatically declining. In the absence of actions, the survival of wildlife will depend on
the balance between supply and demand—to halt the over-exploitation of mammals we must work to
stem demand through regulation,persuasion or provision of alternatives,and by increasing wildlife
numbers through adequately enforced protection ofexisting populations and wild spaces.Science-
based management of wildlife populations for sustained use can benefit both conservation and human
livelihoods, but this is very difficult and requires the installation of expensive bureaucracies to monitor
and manage hunting. For the preservation of these species, conservation research is essential. Below w
suggest a five-pronged cross-disciplinary approach to reducing wildlife mortality and demand for wild
meat (box 2). We briefly touch on some of the relevant considerations for these complex issues.Given
space constraints, the following discussion is not exhaustive.

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Box 2. Five Conservation Steps.
1. Increase legal protection of wild mammals by:
(i) Creating clearer laws.
(ii) Increasing penalties.
(iii) Regulating formal harvests in some cases.
(iv) Increasing regulatory support from developed countries.
2. Implement legal user rights for wildlife utilization
(i) Empower local communities to capture the benefits from wildlife conservation with legal
user rights over wildlife.
3. Provide alternative foods
(i) Shift to hunting species resilient to hunting pressure.
(ii) Provide incentives for communities to switch to traditionally grown protein-rich plant
foods rather than wild meat.
4. Increase education and family planning
(i) Support programmes helping to lower human birth rates, especially those in rural areas
that enhance education opportunities for young women.
(ii) Meetthe need for family planning in areas where women wantto avoid or delay
pregnancy.
5. Change international policy
(i) Wealthier nations must stop exacerbating the problem by inflating demand and price for
meat, trophy, medicinal and ornamental products from wild mammals.
(ii) Currentattempts to reforming policies have been weak due to loopholes and poor
governance.International agreements must include conventions to share the financial
burden of responsibility among nations, especially the developed ones.
5.1.Legal protection of wild mammals
Enforcement of existing legal wildlife protection or improvement of legal instruments has a key role
to play in reducing excessive harvests of wildlife in many contexts.Such solutions need to involve
clearer laws governing the circumstances under which harvestof wildlife for meatis permissible,
strong penalties for infringements, education of judiciaries and law enforcement. In some cases, outsid
of protected areas and for non-threatened species,regulation of formal legal harvests may provide a
partial solution. However, developing countries often lack resources and the strength of governance to
implement such regulation [76,82,83], so logistical and financial support from developed countries wil
be needed. Immediate protection for our most threatened mammals will also require functional protec
areas with national support, professional staff, necessary funding and insightful governance [84]. Law
enforcementto regulate hunting outside protected areas comprises multiple steps,including anti-
poaching patrols, anti-trafficking controls designed to intercept wild meat during transit and regulatio
or suppression atpoints of sale.There is evidence,particularly from Africa,that well-funded and
organized law enforcement can be effective at suppressing illegal hunting to sustainable levels [85]. B
to achieve effective law enforcement substantially more funding is required than is available at presen
with deficits being particularly acute in the tropics. Given the vast extent of protected area networks i
many parts of the tropics, the size of their burden to the host countries and the scale of the threat from
illegal hunting, there is a likely need for a significant future elevation in international funding for man
parks to function effectively [86,87], and the costs of effective regulation outside protected areas are l
to be even higher [82]. Increasing funding and reducing corruption are ongoing and extremely difficul
challenges.
5.2.Legal user rights for wildlife management
In many areas,particularly in Africa and South America,wildlife occurs on communal lands without
clear ownership over land and wildlife resources,resulting in open access systems whereby itis
advantageous for community members to harvest before someone else does [14].Empowering local

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. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
people to capture legalbenefits from wildlife conservation can be an importantstep in reducing
excessive illegalharvests,when efforts to provide alternative livelihoods are unsuccessfulor at least
inefficient levers for change in hunting behaviour [88]. Addressing the land rights of individuals within
communities is an importantstep in avoiding the tragedy ofthe commons (actions ofindividuals
depleting the common resource)[89].The definition ofthe rights to resources atindividual and
community levels is a key prerequisite to empowering people to benefitlegally from wildlife [90].
Wildlife can have a much higher value if used legally, either for tourism or sport hunting [30], and und
the right conditions of land tenure and legislation, large quantities of legal wild meat can be produced
without depleting populations or losing wild species in other areas [91]. In places where legal user rig
over wildlife have been granted to either private land owners or communities in parts of southern Afri
wildlife populations have generally increased dramatically [92,93]. However, such approaches can also
impart problems if poorly managed, as in cases of evolutionary consequences driven by selective huma
harvesting for particular phenotypic traits [94], exacerbation of exploitation of rare species due to hig
prices [95], fragmentation of populations with fencing [65], overstocking of large wild herbivores [91],
increased intolerance towards carnivores [91] and violations to animal welfare [96].
5.3.Alternative foods
Providing alternative foods or incomes for communities who depend unsustainably on wildlife hunting
is of key importance as research shows thatsubsistence hunting is a ‘poor person’s game’,often
conducted when the hunter has no viable alternatives [47].Attempts to provide subsistence hunters
access to livestock husbandry projects have rarely been successful in reducing hunting offtakes [97]. O
problem is that hunting returns tend to be highly biased,with a few individuals responsible for most
of the harvest.The most successful hunters are the hardest to engage in alternatives,having the most
to lose, and can maintain the community’s unsustainable offtakes even if other hunters move to other
activities [78].Shifting to alternative prey species that are more resilient to hunting is also an option,
particularly in post-depletion scenarios where the most susceptible target species are no longer availa
in exploitable densities [41,98].
Although justifications for wild meat harvest in terms of food for impoverished communities must be
weighed seriously, it is critical to acknowledge that the terms ‘protein’ and ‘meat’ are not synonymous
Historically,many cultures from around the world obtained the vast majority of protein calories from
plants and not animals—either wild or domestic [99,100].Consumption of high-protein plant foods
such as soy,pulses,cereals and tubers can satisfy protein requirements that are associated with fewer
environmental impacts than livestock or wild meat,while yielding significant human health benefits
[100–102].In some areas,using traditionally grown protein-rich plant foods rather than wild meat as
a primary protein source for humans could help mitigate the wildlife crisis if cropland is available or
plant-based food products can be imported. Additionally, plant-based meat substitutes (meat analogue
driven by technological advances,are now well established in developed countries,but probably not
yet commonly available in many developing countries.Furthermore,novel sources ofprotein and
miconutrient-rich plant foods such as microalgae or seaweed could also be environmentally sustainabl
and useful in overcoming unsustainable hunting,hunger and malnutrition [103].Compared with the
production of animal protein from large-bodied livestock which is fraught with many downfalls and
negative environmental impacts [13,14], invertebrates, which require little land and tend to have lowe
environmental impacts,and more regular returns,may provide a critical alternative form of protein-
rich food [103]. Integrated agriculture–aquaculture systems, historically common especially in Southe
Asia can have high food efficiencies and diverse sources of aquatic protein production [104]. Ultimatel
reducing globalconsumption ofmeat is a key step necessary to reduce both negative impacts of
human hunting on wild animals and environmental problems associated with livestock production [96]
In addition to reducing meat consumption,improving cropping efficiencies,curtailing tropicalforest
conversion to agriculture and curbing food wastes would sustainably help improve food security while
protecting the environment [105–107].
5.4.Education and family planning
Environmental education campaigns can reduce demand for highly valuable species. For example, sha
fin commerce has apparently declined substantially subsequentto effective socialmedia campaigns
featuring appeals by Chinese basketballcelebrity Yao Ming [108].For charismatic or iconic wildlife
species threatened by commercial hunting (figure 5), well-organized pleas by celebrities could be help

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. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(a) predators
(b) herbivores
(c) insectivores
(d) frugivores
and granivores
Figure 5. Mammal species threatened by hunting span a range of taxonomic and trophic grou
roles,ranging from seed dispersalto pest controlto ecosystem engineering and regulation.Endangerment classification for ea
species noted on the image. Status categories are vulnerable (VU), endangered (EN) and criti
supplementary material for photo credits. See electronic supplementary material, table S1 for
category definition and trends.(a) Predators,left to right:clouded leopard (Neofelis nebulosa),tiger (Panthera tigris),marbled cat
(Pardofelis marmorata).(b) Herbivores,left to right:Bactrian camel(Camelus ferus),takin (Camelus ferus),Nilgiritahr (Nilgiritragus
hylocrius). (c) Insectivores, left to right: long-beaked echidna (Zaglossus bruijnii), giant groun
(Daubentonia madagascariensis). (d) Frugivores & granivores, left to right: Madagascan fruit
(Eulemur collaris) and Sulawesi giant squirrel (Rubrisciurus rubriventer).
for reducing demand,but this is unlikely to be effective for species relied upon for food security.
However,it is notable that in many instances,particularly in urban areas,bushmeat consumption is
positively correlated with wealth [109].In this case,bushmeat is consumed in large part as a cultural
legacy,being a delicacy or sign of affluence,not as a survival necessity,and thus this behaviour may
be more vulnerable to socialpressure.Culture is a strong force in shaping human behaviours and
preferences,but is slow to change and usually unreceptive to formaleducation programmes unless
there are financial incentives.Even in the face of the immediate danger of emerging diseases,hunters
and wild meat consumers have been resistantto changing their culturalroutines [110].However,
cultural norms can change rapidly given strong pressure, as was the case for reducing the demand for
shark fins.
In regions with rapidly growing human populations, programmes helping to lower human birth rate
are needed,especially those in ruralareas that enhance education opportunities for young women.
For example,this need is obvious in Madagascar where the human population has almost doubled
in the last20 years and many ofthe ruralpeople,living under conditions ofpoverty,are severely
impacting the remaining forest habitat fragments while overhunting and eating numerous threatened
lemur (Lemuroidea) species [111]. Likewise, there is an unmet need for family planning in sub-Sahara
Africa where 25% of women ages 15–49 reported that they wanted to avoid or delay pregnancy but ha
not used contraceptives [112]. Furthermore, at the global scale, some 225 million women want to avoi
pregnancies but do not have an effective contraceptive method [113]. Providing adequate contraceptio
in developing countries as a top priority would costonly an additional$5.3 billion annually [113].
In addition to reducing pressure on the world’s hunted species,lowering human fertility rates would
yield other public health, environmental and climate change mitigation co-benefits [114].

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5.5.International policy
Although overhunting of wild meat is primarily a problem in developing countries, wealthier nations
exacerbate or even drive the problem by inflating demand and prices for meat,trophy,medicinal and
ornamentalproducts.For example,there is massive demand for various wildlife products in China
and severalother Asian nations for both traditionalmedicine and for food,resulting in significant
illegal hunting of a number of species,including iconic animals such as elephants,rhinos and tigers.
More than 260 tons of wild meat per year were estimated to be smuggled in personalbaggage into
just one European airport (Paris Roissy-Charles de Gaulle) in 2008 [115].Furthermore,multinational
companies extracting naturalresources in developing countries have a responsibility to ensure that
increasing access to wild lands and wild animals does notintroduce new non-subsistence hunting
impacts.Overfishing by commercialfishing activities affectnot only marine ecosystems butmay
also inadvertently drive hunting on land,because fish representa dietary substitute for bushmeat
[116].The explosive increase of both non-domestic (e.g.heavily subsidized European Union) fishing
and its harvestin African waters appears to be an unexpected driver ofthe wild meat crisis by
forcing local populations to depend on terrestrial bushmeat instead of historically sustainable marine
resources.The good governance offorums and multilateralagreements such as the Convention on
Biodiversity,the London Declaration on IllegalWildlife Trade,and the Convention on International
Trade in Endangered Species (CITES) will be important in determining our ability to stem global trade
and to share the financialand governmentalburden ofresponsibility between the hunting nations
and the demanding nations.Further,the United Nations Reducing Emissions from Deforestation and
Degradation (REDD+)programme,which strives to attribute financialvalue to the carbon stored
in forests,also offers potentialto serve as a toolfor biodiversity conservation.Incentives to reduce
emissions are intended to be implemented in ways that are consistent with the conservation of biologic
diversity [117].Though there are currently no explicit bushmeat-related components to REDD+ [118],
this mechanism neverthelessoffers potentialto reduce bushmeatexploitation both indirectly,via
reducing the prevalence of logging roads (and hunter access),and directly,via formalized limitations
to hunting.
6.Concluding remarks
Our analysis illustrates how human hunting for consumption of food and medicine is contributing to
extinction risk for many terrestrial mammal species.The complexity of managing the wild meat trade
lies in the fact that while rural dependency on wild meat is often a necessity under current conditions
[77],the commodity is frequently a luxury in urban areas [119] and these two scenarios require very
different management tools. In addition, the demand for wild meat is often exacerbated by simultaneo
demand for the same species for medicinal,ornamental or trophy use,particularly in Asia [120],and
so the same hunter or trader may be responding to multiple drivers. Our options for changing human
demand for threatened wildlife must be encapsulated in internationally cohesive,pragmatic policies
and action plans such as those proposed in the recent London Declaration (2014), which was signed b
46 countries. These call for a broad array of actions to stem illegal wildlife trade including eradicating
markets for illegal wildlife products, ensuring effective legal frameworks and deterrents, strengthenin
law enforcementand promoting sustainable livelihoods and development.Furthermore,developed
countries committed to providing significant funding for biodiversity in the tropics at the Rio 1992 Ear
Summit,but have not fulfilled those promises.If such funding were to become available,developed
countries could play a significant role in helping developing countries protect their wildlife from illega
hunting for meat and other body parts. All of these actions, along with several others are embedded in
the five conservation actions that we describe above for reducing both wildlife mortality and demand
for wild meat and products.
Wild meat provides a primary food source for many millions of people throughout the developing
world,especially where other food options are not readily available [39].Unsustainable hunting has
now metamorphosed into a global hunting crisis taking the form of a serious threat to the food securit
of many people as wellas the immediate survivalof hundreds ofmammalspecies,other wildlife
and altered ecological cascades rippling through ecosystems.Averting this global crisis requires bold,
ambitious and prompt actions involving many mainstream economic and policy sectors. New actions a
needed to address all aspects of the crisis. Approaches that benefit both local people and wildlife will b
required to avoid a future of hungry desperate people inhabiting ‘empty landscapes’ across much of th
planet Earth.

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. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Data accessibility.All data needed to evaluate the conclusions in the paper are present in the paper and the electronic
supplementary material. Additional data related to this paper can be downloaded from the IUCN Red List website a
http://www.iucnredlist.org/.
Authors’ contributions.W.J.R. coordinated the project and W.J.R. and C.W. conducted the analysis. All authors participated
in writing the manuscript and gave final approval for publication.
Competing interests.We have no competing interests.
Funding.We have no funding sources to report.
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