Corrected 2 May 2017. See full text.

REVIEW and invertebrates that have been systematically as-

sessed cover a similar range to vertebrates (Fig. 1D),

Biodiversity losses and conservation

suggesting that vertebrates provide a useful
yardstick for patterns of species decline and ex-
tinction among less well-studied organisms. Sys-

responses in the Anthropocene tematic monitoring of birds and mammals shows

that global levels of threat are increasing by 1 to
2% per decade (Fig. 1D). This masks rates of
Christopher N. Johnson,1* Andrew Balmford,2 Barry W. Brook,1 Jessie C. Buettel,1 population decline that are often far greater.
Mauro Galetti,3 Lei Guangchun,4 Janet M. Wilmshurst5,6 For example, coastal wetlands are fast disap-
pearing because of encroachment by people (15).
Biodiversity is essential to human well-being, but people have been reducing biodiversity Among 155 species of coastal waterbirds from
throughout human history. Loss of species and degradation of ecosystems are likely to east Asia, populations are declining at rates of
further accelerate in the coming years. Our understanding of this crisis is now clear, and 5 to 9% per year and as much as 26% for some
world leaders have pledged to avert it. Nonetheless, global goals to reduce the rate of species (16).
biodiversity loss have mostly not been achieved. However, many examples of conservation Comparison of trends in recent extinctions with
success show that losses can be halted and even reversed. Building on these lessons to current levels of threat suggests that the rate of
turn the tide of biodiversity loss will require bold and innovative action to transform extinction may be about to increase. Extrapola-
historical relationships between human populations and nature. tion of recent trends suggests that there will be-
tween 269 and 350 further extinctions of birds

E
xtinction has always been a feature of life of mammals, more than 10% of the global total, and mammals by 2100 (fig. S1). However, 1341
on Earth, but the domination of global eco- were lost over the 100,000 years to 1500 CE (table birds and mammals are currently classed as Crit-
systems by people has caused a sharp rise S1), a pace of extinction that far exceeds back- ically Endangered or Endangered and are there-
in the rate of extinctions to far above pre- ground rates estimated from the fossil record (4). fore likely to be extinct by 2100 if the processes

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human levels. Loss of biodiversity affects Similarly, 23% of the world’s turtle and tortoise causing their endangerment continue to operate;
the functioning of natural ecosystems and threatens species have disappeared over approximately the the fact that most (85%) of these species are cur-
human well-being. In this Review, we place the past 300,000 years (5). Prehistoric occupation of rently decreasing suggests that is the case (details
current extinction crisis in the context of long- Pacific islands alone was associated with extinc- are provided in the supplementary materials). That
term impacts of humanity and assess current trends tion of at least 1000 bird species, which is around is, our knowledge of current threats suggests that
in biodiversity loss. We identify successes as well 10% of all birds (6). In New Zealand, 36% (44 of the rate of extinction could soon rise to at least
as failures in our response to this crisis and draw the original 117) of land bird species have gone five times higher than it has been in the recent
lessons on what is needed to turn the tide of bio- extinct since human settlement began 750 years past (Fig. 1C).
diversity loss. ago, most of them in the prehistoric period be-
tween Polynesian and European arrival (Fig. 1B). Species loss and
A brief history of human-caused extinction Most prehistoric extinctions were of terrestrial ecosystem change
The imprint of humanity on biodiversity reaches animal species, but marine biodiversity also All species are connected to others through eco-
back 2 million years, when our ancestors in the declined because of local extirpations and loss of logical interactions. Extinctions therefore rever-
genus Homo began to use the large-carnivore niche abundance as human use of the oceans expan- berate through ecosystems, as do extirpations of
in Africa. This was associated with a two-thirds ded (7). local populations and declines in abundance,
decline in other large carnivores, as species such Prehistoric extinctions are predominantly asso- which are widespread even in species not close
as sabretooth cats and long-legged hyenas dis- ciated with human arrival rather than climate to extinction (17). Past extinctions and popula-
appeared (1). Diversity of large herbivores also change (8) and are best explained by the impacts tion declines were apparently concentrated on
declined. For example, the 12 species of elephants of hunting (9). Habitat modification and preda- large-bodied vertebrates (9). Disappearance of
and their relatives living in Africa around 3 million tion by alien species were additional factors in these animals removed powerful consumers with
years ago were reduced to two (2). Similar disappear- some places, especially islands. Throughout the strong effects on ecosystem composition and
ances began elsewhere as species of Homo spread Pacific and Indian Oceans, human-lit fires trans- function, both on land and in the oceans (9, 18).
beyond Africa (3), then accelerated in step with formed island ecosystems with unprecedented More generally, species declines disrupt many
the global expansion of H. sapiens through the speed (10); in New Zealand, anthropogenic fire interactions, with far-reaching consequences
past 60,000 years (Fig. 1A). saw the loss of over 40% of forest cover in the drier for ecosystems (19). For example, many woody
Even before the dawn of the modern era of lowland regions within 10 to 70 years of human plants produce large fruits and rely on large
extinctions in 1500 CE, the wave of extinctions arrival (11). The main causes of recent extinctions vertebrates for seed dispersal (20). Large seed
that followed our species around the world had and declines continue to be overexploitation and size is positively correlated with wood density
large impacts on biodiversity. At least 140 genera conversion of habitat, along with invasive spe- and hence high carbon-storage capacity. Loss of
cies, disease, and urban development (12). Global mutualistic partners can therefore lead to trop-
climate change is already causing large disrup- ical forests dominated by fast-growing, small-
1
tions to ecosystems (13) and is likely to grow in seeded plants with lower carbon stores (20). Growth
School of Biological Sciences and Australian Research
Council Centre of Excellence for Australian Biodiversity and
importance as a cause of extinction. of reef-building corals depends partly on abun-
Heritage, University of Tasmania, Private Bag 55, Hobart, Estimates of the recent rate of extinction are dance of large herbivorous fish. In the Carib-
Tasmania 7001, Australia. 2Conservation Science Group, limited by poor knowledge of most species. Our bean, overfishing of these keystone herbivores
Department of Zoology, University of Cambridge, Downing best information is for vertebrates: At least 363 over the past thousand years caused shifts from
Street, Cambridge CB2 3EJ, UK. 3Instituto de Biociências,
Universidade Estadual Paulista (UNESP), Departamento de
vertebrate species have gone extinct since 1500 CE, coral to algal dominance of reef habitat (21).
Ecologia, 13506-900 Rio Claro, São Paulo, Brazil. 4School of according to the International Union for the Con- The stability and productivity of commercial
Nature Conservation, Beijing Forestry University, 100083 servation of Nature (IUCN) Red List (14). The rate fisheries are enhanced by diversity of both fished
Beijing, People’s Republic of China. 5Long-Term Ecology of extinction of vertebrates rose through the past and unfished species. Large declines in diversity
Laboratory, Landcare Research, Post Office Box 69040, Lincoln
7640, New Zealand. 6School of Environment, University of
two centuries as human populations industrial- over the past two centuries correlate with lower
Auckland, Private Bag 92019, Auckland, New Zealand. ized and grew (Fig. 1C and fig. S1). Levels of cur- catches, lack of resilience to exploitation, and
*Corresponding author. Email: [email protected] (C.N.J.) rent threat of extinction in those groups of plants higher incidence of collapse of stocks, along

Johnson et al., Science 356, 270–275 (2017) 21 April 2017 1 of 5

 Corrected 2 May 2017. See full text.
E C OS YS TE M EA R TH

with degradation of other values such as quality First, responses to biodiversity decline are being
of coastal and estuarine waters (22). more than offset by rising pressures, related ulti-
“[O]ur knowledge of current mately to increasing human population size and
Global responses
Several international initiatives have attempted
threats suggests that the per capita consumption. Between 1993 and 2009,
the Human Footprint index, a measure of cumu-
to coordinate action to halt or reverse biodiversity rate of extinction could soon lative human impacts on land, increased by 9%,
loss. The most important is the Convention on rise to at least five times mostly because of conversion of habitat for agri-
Biological Diversity (CBD; www.cbd.int), to which
196 nations are party. In 2002, world leaders
higher than it has been in culture (Fig. 2) (32), whereas the total area of forest
landscapes unmodified by human use fell by 7.2%
pledged through the CBD “to achieve by 2010 a the recent past.” between 2000 and 2013 (33). The area of ocean
significant reduction of the current rate of bio- fished at high intensity (that is, removing >30%
diversity loss.” The 2010 target was succeeded of available primary productivity) has increased
by the “Aichi Biodiversity targets” for 2011–2020, ical changes over long periods (31) but are since 1950 (34). A recent leveling off in that
a more complex plan to reduce loss of species currently underused in assessments of global trend may represent the limit of productivity of
and natural habitats and safeguard ecosystem change. wild fisheries as well as improvements in fishery
services, while also improving planning, financing, management (34, 35), but cumulative human
knowledge, and benefits from sustainable manage- Causes of failure impacts continue to increase across two-thirds
ment of the natural world. Why have we failed to stem the tide of biodiver- of the world’s oceans, mainly owing to intensify-
The 2010 target was not reached (23), and thus sity loss? We suggest four interrelated reasons. ing effects of climate change (35).
far there has been too little progress
on most of the Aichi targets for them
to be met by 2020 (24–26). Most indi-
cators of the global state of species
and ecosystems show continuing de-

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terioration, with little or no evidence of
recent slowdown in rates of change
(24). Indicators of the capacity of
ecosystems to provide ecological ser-
vices also show declines, despite in-
creases in the benefits that human
populations derive from them, sug-
gesting that the natural capital on
which human populations depend is
being rapidly run down (25).
The continuing decline of global
biodiversity is clear despite weak-
nesses in our ability to monitor prog-
ress against targets (27, 28). We lack
good indicators for some of the Aichi
targets, and available indicators often
give somewhat inconsistent signals.
For example, The Biodiversity Inta-
ctness Index, based on models of
effects of land use on species abun-
dances (29), suggests that all human
land use to date has reduced the
abundance of species by a global
average of ~15%. In contrast, the
Living Planet Index estimates an ave-
rage 58% population decline in moni-
tored vertebrates worldwide since
1970 (30). In response to such prob-
lems, work is under way on a con-
sistent set of Essential Biodiversity
Variables (EBVs; http://geobon.org) to
capture spatial and temporal change Fig. 1. Human-caused extinctions through time, and current levels of extinction risk. (A) Cumulative extinction
at the levels of genetics, species abun- of mammalian genera over the past 60,000 years. (B) Cumulative extinctions of vertebrate species in New Zealand
GRAPHIC ADAPTED BY N. CARY/SCIENCE

dances, species traits, community over the past 1000 years. (C) Cumulative extinctions of vertebrate species worldwide since 1500 CE: birds (blue),
composition, and ecosystem struc- mammals (red), and other vertebrates (green). Data are from the IUCN Red List (www.iucnredlist.org) and include
ture and function (28). There is also listed species for which a date of last record or estimate of date of extinction is given in the species account. The gray
much potential for improved use of line shows the number of species of mammals that should have gone extinct according to the background extinction
existing ecological records, such as rate estimated from the fossil record—two extinctions per million/species/years (68). (D) Recent trends in percent of
the International Long-Term Ecologi- species threatened in birds, mammals, and amphibians, compared with percent of species threatened in other groups
cal Research Sites network (ILTERS; of organisms that have been systematically assessed by using IUCN Red List criteria: 1, sea cucumbers; 2, Odonata; 3,
www.ilternet.edu). These networks reptiles; 4, seagrasses; 5, Bryophytes; 6, mangroves; 7, pteridophytes; 8, freshwater crabs; 9, sharks and rays; 10,
have broad coverage (Fig. 2) and use freshwater shrimps; 11, freshwater crayfish; 12, reef-building corals; 13, cactuses; 14, freshwater fish; and 15, gymnosperms.
shared protocols to record ecolog- Data sources are provided in the supplementary materials.

Johnson et al., Science 356, 270–275 (2017) 21 April 2017 2 of 5

 Corrected 2 May 2017. See full text.

Second, interactions and synergies among

threatening processes often amplify their effects,
producing large and accelerating combined im-
pacts (36). Policy responses and actions tend to
tackle threatening processes separately and are
therefore often not appropriately scaled to pres-
sures. A related problem is that some changes
have large effects in catalyzing disparate threats
(37). For example, road development in tropical
forests has direct impacts by fragmenting habitat
and causing mortality to wildlife but also triggers
rapid escalation of a complex of threats, including
overexploitation, conversion of marginal habitats
for farming, fire, and invasive species (37–39).
Climate change is likely to amplify impacts of
other drivers of species decline; for example, there
is evidence that rising temperature variability
increases the susceptibility of amphibians to dis-
ease (40).
Third, funding for global conservation is in-
adequate. Total world spending on conserva-
tion for the period 2001–2008 was estimated at
$21.5 billion per year (in 2005 U.S. dollars) (41).
Most was domestic spending, of which 94% was

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in high-income countries. The developing world
relies heavily on international aid for biodiversity-
conservation projects, but the sums available are
typically insufficient for effective action (42). To
make matters worse, threatened biodiversity is
concentrated in those parts of the world where
conservation is most underfunded (41). The Aichi
targets include further mobilization of conserva-
tion finance, but evidence for recent increases in
funding is equivocal at best (24).
Fourth, in most societies conservation is not
mainstreamed into economic and social planning
and human behavior (43). Conservation remains
largely a discrete sector, which reacts as best it
can to threats generated by other, more power-
ful sectors such as transport and agriculture. Con-
servation and sustainable use of ecosystems need
to be embedded as primary societal concerns, like
prevention of slavery and child labor. The mar-
ginalization of conservation means that funda-
mental drivers of biodiversity decline—such as
rising per capita consumption, naïve economic
models, and disconnection of people from nature—
are often ignored while the conservation sector
does battle with their downstream effects. Analyses
that include values of ecosystem services along
with market values of products generated after
habitat conversion demonstrate large net economic
benefits from biodiversity conservation (44).

Effective conservation action

Amid the gloom, there are bright spots that show
that conservation efforts can have impact. One of
the brightest is the growth of protected areas,
GRAPHIC ADAPTED BY N. CARY/SCIENCE

which should mean that the Aichi target of 17%

coverage of the land surface by 2020 will be
achieved (24, 26). Not all protected areas are
effective, however, and evaluations give mixed
results. Abundance of large land mammals in Af-
rican protected areas declined by 59% between
Fig. 2. Changes in the human footprint, representing cumulative land-use pressures, across Asia, 1970 and 2005 (45), whereas a global synthesis
1993–2009. Green is low pressure, and red is high pressure. Data are from (32). Black dots show the concluded that wildlife populations are on average
locations of Long-Term Ecological Research (LTER) sites; data are from www.ilternet.edu. stable in terrestrial protected areas (46). Marine

Johnson et al., Science 356, 270–275 (2017) 21 April 2017 3 of 5

 Corrected 2 May 2017. See full text.
E C OS YS TE M EA R TH

protected areas are most successful if they have

effective enforcement of no-take policies and if
the reserves are long-established, large, and iso-
lated by deep water or sand (47). Future priorities
are to use protected areas to maintain large con-
tiguous natural areas with only limited human
impact; to achieve representative coverage of
habitats and species currently at high risk (48);
and to secure key areas for provision of ecosystem
services (49).
Conservation science is a mature discipline
armed with knowledge and tools for effective
management of populations and habitats. For
example, analysis of the IUCN Red List showed
that although the threat status of birds and
mammals worsened over the two decades prior to
2008 (Fig. 1D), without recent conservation actions
the situation would now be 18% worse still (Fig. 3,
A and B) (50). In western Europe, the millennia-
long decline of large-bodied vertebrates has at
last been turned around, as populations of large
carnivores recover and large herbivores return to
habitats from which they have been long absent.
This is due to a combination of factors, includ-

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ing nature policy and legislation of the European
Union, improved public attitudes, and rewilding
of abandoned agricultural landscapes (51, 52).
These successes have come from management
of high-priority species and landscapes. Tackling
overexploitation and habitat loss over large regions
is more difficult, but there have been successes.
In waters of the United States and the northeast
Atlantic, many large, highly managed fisheries
have undergone reductions in fishing pressure
and consequent increases in biomass since the
1990s (53). Attention is now turning to interven-
tions such as catch shares and comanagement
arrangements (54) to improve smaller, unassessed
fisheries common in developing countries. More
generally, community-based conservation (CBC)
projects, which engage communities as stakeholders
and devolve control over natural resources to them
while improving access to benefits from sustainable
use, show promise in reducing overexploitation
and improving livelihoods (55).
Deforestation in the Brazilian Amazon has
been reduced to around one-third of its peak in
2004, despite a recent spike (56). This was evi-
dently due to many factors, including expansion
of protected areas, improved enforcement of forest-
protection codes and incentives for compliance
with those codes, intensification of production of
beef and soy on already cleared areas, and market
embargoes against product from newly cleared
lands (57). Production of soy and beef continued
to grow as deforestation fell after 2005, and the
retention of forest avoided the emission of 3.2 Gt Fig. 3. Responses to biodiversity decline. (A) The cumulative number of islands on which one or
of CO2 and should confer other benefits, includ- more species of invasive vertebrates have been eradicated, since 1950. Data are from the Database
GRAPHIC ADAPTED BY N. CARY/SCIENCE

ing stabilization of river discharge and reduced of Island Invasive Species Eradications (http://diise.islandconservation.org). Island eradications of in-
risk of inhibition of rainfall, as well as retained vasive predators have been essential in preventing the extinction of species such as the kakapo Strigops
biodiversity (57). habroptilus [Photo: Andrew Digby, NZ Deparment of Conservation] (B) Recovery of the golden lion tamarin
Efforts to sustain biodiversity in farmed land- in Brazil. Reintroduction of captive-bred animals and restoration of corridors linking forest fragments have
scapes have produced mixed results (58, 59). Con- resulted in a dramatic increase in the wild population; shown are population estimates and intervention
servation measures on farmland are often costly, timeline from Associação Mico-Leão-Dourado. [Photo: Andreia Martins] (C) China’s National Ecosystem
and although some succeed, they typically reduce Function Zoning scheme, developed by the Ministry of Environment Protection and Chinese Academy of
farm yields and hence are likely to displace pro- Sciences, to identify areas with key ecosystem functions and where development is restricted to protect
duction elsewhere (60). This has led instead to those functions (source, www.mep.gov.cn/gkml/hbb/bgg/201511/t20151126_317777.htm).

Johnson et al., Science 356, 270–275 (2017) 21 April 2017 4 of 5

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Supplementary Text
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Johnson et al., Science 356, 270–275 (2017) 21 April 2017 5 of 5

 Biodiversity losses and conservation responses in the Anthropocene
Christopher N. JohnsonAndrew BalmfordBarry W. BrookJessie C. BuettelMauro GalettiLei GuangchunJanet M. Wilmshurst

Science, 356 (6335), • DOI: 10.1126/science.aam9317

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