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Marine defaunation: Animal loss in the global ocean
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DOI: 10.1126/science.1255641 · Source: PubMed
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REVIEW SUMMARY
◥
MARINE CONSERVATION
Marine defaunation: Animal loss in
the global ocean
Douglas J. McCauley,* Malin L. Pinsky, Stephen R. Palumbi, James A. Estes,
Francis H. Joyce, Robert R. Warner
BACKGROUND: Comparing patterns of ter-
restrial and marine defaunation helps to
place human impacts on marine fauna in
context and to navigate toward recovery. De-
faunation began in ear-
nest tens of thousands of
years later in the oceans
than it did on land. Al-
though defaunation has
been less severe in the
oceans than on land, our
effects on marine animals are increasing in
pace and impact. Humans have caused few
complete extinctions in the sea, but we are
responsible for many ecological, commercial,
and local extinctions. Despite our late start,
humans have already powerfully changed
virtually all major marine ecosystems.
ADVANCES: Humans have profoundly de-
creased the abundance of both large (e.g.,
whales) and small (e.g., anchovies) marine
fauna. Such declines can generate waves of
ecological change that travel both up and
down marine food webs and can alter ocean
ecosystem functioning. Human harvesters
have also been a major force of evolutionary
change in the oceans and have reshaped the
genetic structure of marine animal popula-
tions. Climate change threatens to accelerate
marine defaunation over the next century.
The high mobility of many marine animals
offers some increased, though limited, ca-
pacity for marine species to respond to cli-
mate stress, but it also exposes many species
to increased risk from other stressors. Be-
cause humans are intensely reliant on ocean
ecosystems for food and other ecosystem ser-
vices, we are deeply affected by all of these
forecasted changes.
Three lessons emerge when comparing
the marine and terrestrial defaunation ex-
periences: (i) today’s low rates of marine
extinction may be the prelude to a major
extinction pulse, similar to that observed
on land during the industrial revolution, as
the footprint of human ocean use widens;
(ii) effectively slowing ocean defaunation
requires both protected areas and care-
ful management of the intervening ocean
matrix; and (iii) the terrestrial experience
and current trends in ocean use suggest
that habitat destruction is likely to become
an increasingly dominant threat to ocean
wildlife over the next 150 years.
OUTLOOK: Wildlife populations in the oceans
have been badly damaged by human activ-
ity. Nevertheless, marine fauna generally
are in better condition than terrestrial fauna:
Fewer marine animal extinctions have oc-
curred; many geographic ranges have shrunk
less; and numerous ocean ecosystems re-
main more wild than terrestrial ecosystems.
Consequently, meaningful rehabilitation of
affected marine animal populations remains
within the reach of managers. Human depen-
dency on marine wildlife and the linked
fate of marine and terrestrial fauna necessi-
tate that we act quickly to slow the advance
of marine defaunation.
▪
RESEARCH
SCIENCE sciencemag.org 16 JANUARY 2015 • VOL 347 ISSUE 6219 247
Timeline (log scale) of marine and terrestrial defaunation. The marine defaunation experience is much less advanced, even though humans have
been harvesting ocean wildlife for thousands of years.The recent industrialization of this harvest, however, initiated an era of intense marine wildlife declines.
If left unmanaged, we predict that marine habitat alteration, along with climate change (colored bar: IPCC warming), will exacerbate marine defaunation.
The list of author affiliations is available in the full article online.
*Corresponding author. E-mail: douglas.mccauley@lifesci.
ucsb.edu Cite this article as D. J. McCauley et al., Science
347, 1255641 (2015). DOI: 10.1126/science.1255641
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REVIEW
◥
MARINE CONSERVATION
Marine defaunation: Animal loss in
the global ocean
Douglas J. McCauley,1* Malin L. Pinsky,2
Stephen R. Palumbi,3
James A. Estes,4
Francis H. Joyce,1
Robert R. Warner1
Marine defaunation, or human-caused animal loss in the oceans, emerged forcefully only
hundreds of years ago, whereas terrestrial defaunation has been occurring far longer.
Though humans have caused few global marine extinctions, we have profoundly affected
marine wildlife, altering the functioning and provisioning of services in every ocean.
Current ocean trends, coupled with terrestrial defaunation lessons, suggest that marine
defaunation rates will rapidly intensify as human use of the oceans industrializes. Though
protected areas are a powerful tool to harness ocean productivity, especially when designed
with future climate in mind, additional management strategies will be required. Overall,
habitat degradation is likely to intensify as a major driver of marine wildlife loss. Proactive
intervention can avert a marine defaunation disaster of the magnitude observed on land.
S
everal decades of research on defaunation
in terrestrial habitats have revealed a serial
loss of mammals, birds, reptiles, and inver-
tebrates that previously played important
ecological roles (1). Here, we review the
major advancements that have been made in
understanding the historical and contemporary
processes of similar defaunation in marine envi-
ronments. We highlight patterns of similarity
and difference between marine and terrestrial
defaunation profiles to identify better ways to
understand, manage, and anticipate the effects of
future defaunation in our Anthropocene oceans.
Patterns of marine defaunation
Delayed defaunation in the oceans
Defaunation on land began 10,000 to 100,000 years
ago as humans were expanding their range and
coming into first contact with novel faunal
assemblages (2–4). By contrast, the physical prop-
erties of the marine environment limited our
capacity early on to access and eliminate marine
animal species. This difficulty notwithstanding,
humans began harvesting marine animals at least
40,000 years ago, a development that some have
suggested was a defining feature in becoming
“fully modern humans” (5). Even this early harvest
affected local marine fauna (6). However, global
rates of marine defaunation only intensified in
the last century with the advent of industrial
fishing and the rapid expansion of coastal popu-
lations (7). As a result, extant global marine faunal
assemblages remain today more Pleistocene-like,
at least with respect to species composition, than
terrestrial fauna. The delayed onset of intensive
global marine defaunation is most visible in a
comparative chronology of faunal extinctions in
which humans are likely to have directly or in-
directly played a role (8) (Fig. 1).
Comparing rates of animal extinction
Despite the recent acceleration of marine defau-
nation, rates of outright marine extinction have
been relatively low. The International Union for
Conservation of Nature (IUCN) records only 15
global extinctions of marine animal species in
the past 514 years (i.e., limit of IUCN temporal
coverage) and none in the past five decades (8, 9).
By contrast, the IUCN recognizes 514 extinctions
of terrestrial animals during the same period
(Fig. 1). While approximately six times more an-
imal species have been cataloged on land than in
the oceans (10), this imbalance does not explain
the 36-fold difference between terrestrial and
marine animal extinctions.
It is important to note that the status of only a
small fraction of described marine animal spe-
cies have been evaluated by the IUCN, and many
assessed species were determined to be data defi-
cient (11) (Fig. 2). This lack of information neces-
sitates that officially reported numbers of extinct
and endangered marine fauna be considered as
minimum estimates (11). There remain, however,
a number of data-independent explanations for
the lower extinction rates of marine fauna. Ma-
rine species, for instance, tend to be more wide-
spread, exhibit less endemism, and have higher
dispersal (12, 13).
Complacency about the magnitude of contem-
porary marine extinctions is, however, ill-advised.
If we disregard the >50,000-year head start of
intense terrestrial defaunation (Fig. 1) and com-
pare only contemporary rates of extinction on land
and in the sea, a cautionary lesson emerges. Ma-
rine extinction rates today look similar to the
moderate levels of terrestrial extinction observed
before the industrial revolution (fig. S1). Rates of
extinction on land increased dramatically after this
period, and we may now be sitting at the precipice
of a similar extinction transition in the oceans.
Three other kinds of extinction
The small number of species known to be perma-
nently lost from the world’s oceans inadequately
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SCIENCE sciencemag.org 16 JANUARY 2015 • VOL 347 ISSUE 6219 1255641-1
1
Department of Ecology, Evolution, and Marine Biology,
University of California, Santa Barbara, CA 93106, USA.
2
Department of Ecology, Evolution, and Natural Resources,
Institute of Marine and Coastal Sciences, Rutgers University,
New Brunswick, NJ 08901, USA. 3
Department of Biology,
Stanford University, Hopkins Marine Station, Pacific Grove,
CA 93950, USA. 4
Department of Ecology and Evolutionary
Biology, University of California, Santa Cruz, CA 95060, USA.
*Corresponding author. E-mail: douglas.mccauley@lifesci.ucsb.edu
Fig. 1. Comparative chronology of human-associated
terrestrial and marine animal extinctions. Green bars
indicate animal extinctions that occurred on land, and blue
bars indicate marine animal extinctions. Timeline mea-
sures years before 2014 CE. Only extinctions occurring less than 55,000 years ago are depicted.
Defaunation has ancient origins on land but has intensified only within the last several hundred years in the
oceans. See details in (8).

reflects the full impacts of marine defaunation.
We recognize three additional types of defaunation-
induced extinction.
Local extinction
Defaunation has caused numerous geographic
range constrictions in marine animal species,
driving them locally extinct in many habitats.
These effects have been particularly severe among
large pelagic fishes, where ~90% of studied spe-
cies have exhibited range contractions (8, 14)
(Fig. 3). Local extinctions, however, are not unique
to large pelagic predators. Close to a third of the
marine fishes and invertebrates off the North
American coasts that can be reliably sampled in
scientific trawl surveys (often small to medium-
bodied species) have also exhibited range con-
tractions (Fig. 3). Such contractions can result
from the direct elimination of vulnerable subpop-
ulations or from region-wide declines in abundance
(14). Available data suggest that the magnitude
of the range contractions for this diverse set of
trawl-surveyed marine species is, on average,
less than the contractions observed for terrestrial
animals such as mammals, birds, and butterflies.
Though data deficiencies are abundant, most ma-
rine animal species also do not yet seem to exhibit
some of the most extreme range contractions
recorded for terrestrial animals. Asian tigers, for
example, have lost ~93% of their historical range
(15), whereas tiger sharks still range across the
world’s oceans (16).
Ecological extinction
Reductions in the abundance of marine animals
have been well documented in the oceans (17).
Aggregated population trend data suggest that in
the last four decades, marine vertebrates (fish,
seabirds, sea turtles, and marine mammals) have
declined in abundance by on average 22% (18).
Marine fishes have declined in aggregate by
38% (17), and certain baleen whales by 80 to 90%
(19). Many of these declines have been termed
ecological extinctions—although the species in
question are still extant, they are no longer suf-
ficiently abundant to perform their functional
roles. Ecological extinctions are well known in
terrestrial environments and have been demon-
strated to be just as disruptive as species extinc-
tions (20). On land, we know of the phenomenon
of “empty forests” where ecological extinctions of
forest fauna alter tree recruitment, reshape plant
dispersal, and cause population explosions of
small mammals (1, 20, 21). We are now observ-
ing the proliferation of “empty reefs,” “empty
estuaries,” and “empty bays” (7, 14, 22).
Commercial extinction
Species that drop below an abundance level at
which they can be economically harvested are ex-
tinct from a commercial standpoint. On land, com-
mercial extinctions affected species ranging from
chinchilla to bison (23). Cases of commercial ex-
tinction are also common in the oceans. Gray whales
were commercially hunted starting in the 1840s.
By 1900, their numbers were so depleted that
targeted harvest of this species was no longer re-
gionally tenable (24). Likewise, the great whales
in Antarctica were serially hunted to commer-
cial extinction (25).
Not all species, however, are so “lucky” as to
have human harvesters desist when they become
extremely rare. Demand and prices for certain
highly prized marine wildlife can continue to in-
crease as these animals become less abundant—a
phenomenon termed the anthropogenic Allee
effect (26). Individual bluefin tuna can sell for
>US$100,000, rare sea cucumbers >US$400/kg,
and high-quality shark fins for >US$100/kg. Such
species are the rhinos of the ocean—they may
never be too rare to be hunted.
Differential vulnerability to defaunation
Are certain marine animals more at risk than
others to defaunation? There has been consider-
able attention given to harvester effects on large
marine animals (27). Selective declines of large-
bodied animals appear to be evident in certain
contexts (28, 29). As a result of such pressures,
turtles, whales, sharks, and many large fishes are
now ecologically extinct in many ecosystems, and
the size spectra (abundance–body mass relation-
ships) of many communities have changed consid-
erably (7, 30, 31). Marine defaunation, however,
has not caused many global extinctions of large-
bodied species. Most large-bodied marine animal
species still exist somewhere in the ocean. By
contrast, on land, we have observed the extinc-
tion of numerous large terrestrial species and a
profound restructuring of the size distribution of
land-animal species assemblages. The mean body
mass for the list of surviving terrestrial mammal
species, for example, is significantly smaller than
the body mass of terrestrial mammal species that
lived during the Pleistocene (1, 32). Such effects,
however, are not evident for marine mammals (8)
(fig. S2). Recent reviews have drawn attention to
the fact that humans can also intensely and ef-
fectively deplete populations of smaller marine
animals (29, 33). These observations have inspired
a belated surge in interest in protecting small
forage fishes in the oceans.
A review of modern marine extinctions and list-
ings of species on the brink of extinction reveals
further insight into aggregate patterns of differen-
tial defaunation risk in the oceans (Fig. 2). Sea
turtles have the highest proportion of endangered
species among commonly recognized groupings of
marine fauna. No modern sea turtle species, how-
ever, have yet gone extinct. Pinnipeds and marine
mustelids, followed very closely by seabirds and
shorebirds, have experienced the highest propor-
tion of species extinctions. Many of the most threat-
ened groups of marine animals are those that
directly interact with land (and land-based humans)
during some portion of their life history (Fig. 2). Ter-
restrial contact may also explain why diadromous/
brackish water fishes are more threatened than
exclusively marine fishes (Fig. 2).
Although many marine animal species are
clearly affected negatively by marine defauna-
tion, there also appears to be a suite of defau-
nation “winners,” or species that are profiting in
Anthropocene oceans. Many of these winners are
smaller and “weedier” (e.g., better colonizing and
faster reproducing) species. Marine invertebrates,
in particular, have often been cited as examples of
1255641-2 16 JANUARY 2015 • VOL 347 ISSUE 6219 sciencemag.org SCIENCE
Fig. 2. Marine defaunation threat.Threat from defaunation is portrayed for different groups of marine fauna
as chronicled by the IUCN Red List (113).Threat categories include “extinct” (orange), “endangered” (red; IUCN
categories “critically endangered” + “endangered”), “data deficient” (light gray), and “unreviewed” (dark gray).
Groups that contact land during some portion of their life history (green) are distinguished from species that do
not (light blue).The total number of species estimated in each group is listed below the graph. Species groupings
are coded as follows: ST, sea turtles; PO, pinnipeds and marine mustelids; SS, seabirds and shorebirds; SSL, sea
snakes and marine lizard; CS, cetaceans and sirenians; DBRF, diadromous/brackish ray-finned fishes; CF,
cartilaginous fishes; MRF,exclusively marine ray-finned fishes; MI, marine invertebrates. See further details in (8).
RESEARCH | REVIEW

species that are succeeding in the face of intense
marine defaunation: lobster proliferated as pred-
atory groundfish declined (34), prawns increased
and replaced the dominance of finfish in land-
ings (35), and urchin populations exploded in the
absence of their predators and competitors (36).
Numerous mid-level predators also appear to ben-
efit from the loss of top predators [e.g., small sharks
and rays; (37)]—a phenomenon analogous to meso-
predator release observed in terrestrial spheres
(38). The status held by some of these defaunation
winnersinthe oceans may, however, beephemeral.
Many of the marine species that have initially
flourished as a result of defaunation have them-
selvesbecometargetsforharvest by prey-switching
humans as is evidenced by the recent global ex-
pansion of marine invertebrate fisheries (39).
Spatial patterns of vulnerability
Patterns of marine defaunation risk track differ-
ences in the physical environment. Global assess-
ments of human impact on marine ecosystems
suggest that coastal wildlife habitats have been
more influenced than deep-water or pelagic ecosys-
tems (40). The vulnerability of coastal areas pre-
sumably results from ease of access to coastal zones.
This relationship between access and defaunation
risk manifests itself also at smaller spatial scales,
with populations of marine wildlife closest to trade
networks and human settlements appearing often
to be more heavily defaunated (41, 42). The relative
insulation that animal populations in regions like
the deep oceans presently experience, however,
may be short-livedbecause depletions of shallow-
water marine resources and the development
of new technologies have created both the ca-
pacity and incentive to fish, mine, and drill oil
in some of the deepest parts of the sea (28, 43).
Coral reefs, in particular, have consistently
been highlighted as marine ecosystems of special
concern to defaunation. Coral reefs have been
exposed to a wide range of impacts and distur-
bances, including sedimentation and pollution,
thermal stress, disease, destructive fishing, and
coastal development (44, 45). Such stressors nega-
tively influence both corals and the millions of
species that live within and depend upon reefs
(46). Risk, however, is not uniform, even across a
reefscape. Shallow backreef pools, for example,
routinely overheat, and consequently, corals in
these parts of the reef are more resistant to ocean
warming (47). Environmentally heterogeneous
areas may in fact act as important natural fac-
tories of adaptation that will buffer against some
types of marine defaunation.
Effects of marine defaunation
Extended consequences of
marine defaunation
Marine defaunation has had far-reaching effects
on ocean ecosystems. Depletions of a wide range
of ecologically important marine fauna such as
cod, sea otters, great whales, and sharks have
triggered cascading effects that propagate across
marine systems (37, 48–51). Operating in the op-
posite direction from trophic cascades are changes
that travel from the bottom to the top of food
chains as a result of the declining abundance of
lower–trophic level organisms (52). Depletions of
fauna such as anchovies, sardines, and krill cause
reductions in food for higher-trophic level animals
such as seabirds and marine mammals, poten-
tially resulting in losses in reproduction or reduc-
tions in their population size (33, 53).
The extended effects of defaunation on marine
ecosystems also occur beyond the bounds of these
top-down or bottom-up effects. Defaunation can
reduce cross-system connectivity (54, 55), decrease
ecosystem stability (56), and alter patterns of bio-
geochemical cycling (57). The ill effects of food
web disarticulation can be further amplified when
they occur in association with other marine dis-
turbances. For example, mass releases of dis-
carded plant fertilizers into marine ecosystems
from which defaunation has eliminated important
consumers can create “productivity explosions” by
fueling overgrowth of microbes and algae that
fail to be routed into food webs (58, 59).
The selective force of human predation has
also been sufficiently strong and protracted so
as to have altered the evolutionary trajectory of
numerous species of harvested marine fauna
(60). Harvest has driven many marine animal
species to become smaller and thinner, to grow
more slowly, to be less fecund, and to reproduce
at smaller sizes (61). There is also evidence that
harvest can reduce the genetic diversity of many
marine animal populations (62). The genetic ef-
fects of defaunation represent a loss of adaptive
potential that may impair the resilient capacity
of ocean wildlife (63).
Importance of marine defaunation
to humans
Marine defaunation is already affecting human
well-being in numerous ways by imperiling food
sustainability, increasing social conflict, impair-
ing storm protection, and reducing flows of other
ecosystem services (64, 65). The most conspicu-
ous service that marine fauna make to society is
the contribution of their own bodies to global
diets. Marine animals, primarily fishes, make up
a large proportion of global protein intake, and
this contribution is especially strong for impov-
erished coastal nations (66). According to the
U.N. Food and Agriculture Organization (FAO),
40 times more wild animal biomass is harvested
from the oceans than from land (67). Declines in
this source of free-range marine food represent a
major source of concern (65).
A diverse array of nonconsumptive services
are also conferred to humanity from ocean ani-
mals, ranging from carbon storage that is facil-
itated by whales and sea otters to regional cloud
formation that appears to be stimulated by coral
emissions of dimethylsulphoniopropionate (DMSP)
(57, 68, 69). Another key service, given forecasts
of increasingly intense weather events and sea-
level rise, is coastal protection. Coral, oyster, and
other living reefs can dissipate up to 97% of the
wave energy reaching them, thus protecting built
structures and human lives (70). In some cases,
corals are more than just perimeter buffers; they
also serve as the living platform upon which en-
tire countries (e.g., the Maldives, Kiribati, the
Marshall Islands) and entire cultures have been
founded. Atoll-living human populations in these
areas depend on the long-term health of these
animate pedestals to literally hold their lives
together.
Outlook and ways forward
Will climate change exacerbate
marine defaunation?
The implications of climate change upon marine
defaunation are shaped by ocean physics. Marine
species live in a vast, globally connected fluid
Fig. 3. Comparisons of range contractions for select marine and terrestrial fauna.Terrestrial (green)
and marine cases (blue) include evaluations of geographical range change for: 43 North American
mammals over the last ~200 years (NM) (114), 18 Indian mammals over the last 30 years (IM) (115), 201
British birds from ~1970 to 1997 (BB) and 58 British butterflies from ~1976 to 1997 (BF) (116), 12 global
large pelagic fishes from the 1960s to 2000s (PF) (14), and 327 trawl-surveyed North American marine
fish and invertebrates from the 1970s to 2000s (TFI). (A) Percent of species whose ranges have
contracted with binomial confidence intervals and (B) distribution of percent contraction for those species
that have contracted (violin plot). Sample sizes are shown above each data point,white horizontal lines (B)
show the medians, and thick vertical black lines display the interquartile range. See details in (8).
RESEARCH | REVIEW

medium that has immense heat-storage capacity
and has exhibited a historically robust capability
to buffer temperature change over daily, annual,
and even decadal time scales (71). While this buf-
fering capacity at first seems to confer an advan-
tage to marine fauna, the thermal stability of the
oceans may have left many subtidal marine an-
imals poorly prepared, relative to terrestrial coun-
terparts, for the temperature increases associated
with global warming. The same logic supports
related predictions that terrestrial fauna living in
more thermally stable environments will be more
vulnerable to warming than those found in areas
of greater temperature variability (72).
Ocean warming presents obvious challenges
to polar marine fauna trapped in thermal dead
ends (73). Tropical marine species are, however,
also highly sensitive to small increases in temper-
ature. For example, coastal crabs on tropical
shores live closer to their upper thermal maxima
than do similar temperate species (74). Likewise,
the symbiosis of corals and dinoflagellates is
famously sensitive to rapid increases of only 1° to
2°C (75). Even though corals exhibit the capacity
for adaptation (47), coral bleaching events are
expected to be more common and consequently
more stressful by the end of the century (76). The
effects of rising ocean temperature extend well
beyond coral reefs and are predicted to affect
both the adult and juvenile stages of a diverse set
of marine species (77), to reshuffle marine com-
munity composition (78), and to potentially alter
the overall structure and dynamics of entire ma-
rine faunal communities (79).
The wide range of other climate change-
associated alterations in seawater chemistry
and physics—including ocean acidification, anoxia,
ocean circulation shifts, changes in stratification,
and changes in primary productivity—will fun-
damentally influence marine fauna. Ocean acid-
ification, for example, makes marine animal
shell building more physiologically costly, can
diminish animal sensory abilities, and can alter
growth trajectories (80, 81). Climate change im-
pacts on phytoplankton can further accentuate
defaunation risk (82). At the same time that
humans are reducing the abundance of marine
forage fish through direct harvest, we also may
be indirectly reducing the planktonic food for
forage fish and related consumers in many
regions.
Mobility and managing defaunation
Many marine animals, on average, have signifi-
cantly larger home ranges as adults [Fig. 4 and
figs. S3 and S4; (8)] and disperse greater dis-
tances as juveniles than their terrestrial counter-
parts (13). This wide-ranging behavior of many
marine species complicates the management of
ocean wildlife as species often traverse multiple
management jurisdictions (83–85). On the other
hand, the greater mobility of many marine ani-
mal species may help them to better follow the
velocity of climate change and to colonize and
recolonize habitats, so long as source population
refuges are kept available (71, 73, 78, 86, 87).
Marine protected areas can offer this sort of
refuge for animal populations (88). The establish-
ment of protected areas in the oceans lags far
behind advancements made on land, with an
upper-bound estimate of only about 3.6% of the
world’s oceans now protected (8) (fig. S5). One
source of optimism for slowing marine defauna-
tion, particularly for mobile species, is that the
mean size of marine protected areas has in-
creased greatly in recent years (fig. S5). However,
most marine protected areas remain smaller (me-
dian 4.5 km2
) than the home range size of many
marine animals (Fig. 4). Though much is lost in
this type of crude comparison, this observation
highlights what may be an important discon-
nect between the scales at which wildlife use
the oceans and the scale at which we typically
manage the oceans.
This spatial mismatch is just one of many
reasons why protected areas cannot be the full
solution for managing defaunation (83). We
learned this lesson arguably too late on land.
Protected areas can legitimately be viewed as
some of our proudest conservation achievements
on land (e.g., Yosemite, Serengeti, Chitwan Natio-
nal Parks), and yet with four times more terres-
trial area protected than marine protected area,
we have still failed to satisfactorily rein in ter-
restrial defaunation (1) (fig. S5). The realization
that more was needed to curb terrestrial defau-
nation inspired a wave of effort to do conserva-
tion out of the bounds of terrestrial protected
areas (e.g., conservation easements and corridor
projects). The delayed implementation of these
strategies has, however, often relegated terres-
trial conservation to operating more as a retroac-
tive enterprise aimed at restoringdamaged habitats
and triaging wildlife losses already underway. In
the oceans, we are uniquely positioned to pre-
emptively manage defaunation. We can learn
from the terrestrial defaunation experience that
protected areas are valuable tools, but that we
must proactively introduce measures to manage
our impacts on marine fauna in the vast majority
of the global oceans that is unprotected.
Strategies to meet these goals include incentive-
based fisheries management policies (89), spa-
tially ambitious ecosystem-based management
plans (83), and emerging efforts to preemptively
zone human activities that affect marine wildlife
(90, 91). There have been mixed responses among
marine managers as to whether and how to em-
brace these tools, but more complete implementa-
tion of these strategies will help chart a sustainable
future for marine wildlife (43, 90, 91). A second,
complementary set of goals is to incorporate cli-
mate change into marine protected area schemes
to build networks that will provide protection for
ocean wildlife into the next century (92). Such
built-in climate plans were unavailable, and even
unthinkable, when many major terrestrial parks
were laid out, but data, tools, and opportunity
exist to do this thoughtfully now in the oceans.
Habitat degradation: The coming threat
to marine fauna
Many early extinctions of terrestrial fauna are
believed to have been heavily influenced by hu-
man hunting (2, 93), whereas habitat loss ap-
pears to be the primary driver of contemporary
defaunation on land (1, 11, 86, 94). By contrast,
marine defaunation today remains mainly driv-
en by human harvest (95, 96). If the trajectory of
terrestrial defaunation is any indicator, we should
anticipate that habitat alteration will ascend
in importance as a future driver of marine
defaunation.
Signs that the pace of marine habitat modifi-
cation is accelerating and may be posing a grow-
ing threat to marine fauna are already apparent
(Fig. 5). Great whale species, no longer extensively
hunted, are now threatened by noise disruption,
oil exploration, vessel traffic, and entanglement
with moored marine gear (fig. S6) (97). Habitat-
modifying fishing practices (e.g., bottom trawling)
Fig. 4. Mobility of ter-
restrial and marine
fauna. Because mobil-
ity shapes defaunation
risk, we compare the
size-standardized
home range size of a
representative selec-
tion of marine (blue)
and terrestrial (green)
vertebrates. Data are
presented for adults
over a full range of
animal body sizes,
plotted on a logarith-
mic scale. Species
include seabirds,
marine reptiles, marine
fishes, marine mam-
mals, terrestrial birds,
terrestrial reptiles, and
terrestrial mammals (see details in (8); table S2 and fig. S3). Regression lines enclosed by shaded
confidence intervals are plotted for all marine and all terrestrial species. The dotted red line demarcates
the current median size of all marine protected areas (MPAs).
RESEARCH | REVIEW

have affected ~50 million km2
of seafloor (40).
Trawling may represent just the beginning of our
capacity to alter marine habitats. Development
of coastal cities, where ~40% of the human pop-
ulation lives (98), has an insatiable demand for
coastal land. Countries like the United Arab
Emirates and China have elected to meet this
demand by “seasteading”—constructing ambitious
new artificial lands in the ocean (99). Technolog-
ical advancement in seafloor mining, dredging,
oil and gas extraction, tidal/wave energy gener-
ation, and marine transport is fueling rapid ex-
pansion of these marine industries (43, 100).
Even farming is increasing in the sea. Projections
now suggest that in less than 20 years, aquacul-
ture will provide more fish for human consump-
tion than wild capture fisheries (101). Fish farming,
like crop farming, can consume or drastically alter
natural habitats when carried out carelessly (102).
Many of these emerging marine development
activities are reminiscent of the types of rapid
environmental change observed on land during
the industrial revolution that were associated
with pronounced increases in rates of terrestrial
defaunation. Marine habitats may eventually join
the ranks of terrestrial frontier areas, such as
the American West, the Brazilian Amazon, and
Alaska, which were once believed to be imper-
vious to development, pollution, and degradation.
Land to sea defaunation connections
The ecologies of marine and terrestrial systems
are dynamically linked. Impacts on terrestrial
fauna can perturb the ecology of marine fauna
(54) and vice versa (103). Furthermore, the health
of marine animal populations is interactively
connected to the health of terrestrial wildlife
populations—and to the health of society. People
in West Africa, for example, exploit wild terres-
trial fauna more heavily in years when marine
fauna are in short supply (104). It is not yet clear
how these linkages between marine and terres-
trial defaunation will play out at the global level.
Will decreasing yields from marine fisheries, for
example, require that more terrestrial wildlands
be brought into human service as fields and
pastures to meet shortfalls of ocean-derived foods?
Marine ecosystem managers would do well to
better incorporate considerations of land-to-sea
defaunation connections in decision making.
Not all bad news
It is easy to focus on the negative course that
defaunation has taken in the oceans. Humans
have, however, demonstrated a powerful capac-
ity to reverse some of the most severe impacts
that we have had on ocean fauna, and many
marine wildlife populations demonstrate immense
potential for resilience (47, 105–107). The sea otter,
the ecological czar of many coastal ecosystems,
was thought to be extinct in the early 1900s but
was rediscovered in 1938, protected, and has
resumed its key ecological role in large parts of
the coastal North Pacific and Bering Sea (108).
The reef ecosystems of Enewetak and Bikini
Atolls present another potent example. The
United States detonated 66 nuclear explosions
above and below the water of these coral reefs
in the 1940s and 1950s. Less than 50 years later,
the coral and reef fish fauna on these reefs
recovered to the point where they were being
described as remarkably healthy (109).
There is great reason to worry, however, that
we are beginning to erode some of the systemic
resilience of marine animal communities (110).
Atomic attacks on local marine fauna are one
thing, but an unimpeded transition toward an
era of global chemical warfare on marine eco-
systems (e.g., ocean acidification, anoxia) may
retard or arrest the intrinsic capacity of marine
fauna to bounce back from defaunation (75, 111).
Conclusions
On many levels, defaunation in the oceans has, to
date, been less severe than defaunation on land.
Developing this contrast is useful because our
more advanced terrestrial defaunation experi-
ence can serve as a harbinger for the possible
future of marine defaunation (3). Humans have
had profoundly deleterious impacts on marine
animal populations, but there is still time and
there exist mechanisms to avert the kinds of
defaunation disasters observed on land. Few
marine extinctions have occurred; many subtidal
marine habitats are today less developed, less
polluted, and more wild than their terrestrial
counterparts; global body size distributions of
extant marine animal species have been mostly
unchanged in the oceans; and many marine fauna
have not yet experienced range contractions as
severe as those observed on land.
We are not necessarily doomed to helplessly
recapitulate the defaunation processes observed
on land in the oceans: intensifying marine hunt-
ing until it becomes untenable and then embarking
on an era of large-scale marine habitat modifi-
cation. However, if these actions move forward
in tandem, we may finally trigger a wave of ma-
rine extinctions of the same intensity as that
observed on land. Efforts to slow climate change,
rebuild affected animal populations, and intelli-
gently engage the coming wave of new marine
development activities will all help to change the
Fig. 5. Habitat change in the global oceans. Trends in six indicators of marine habitat modification
suggest that habitat change may become an increasingly important threat to marine wildlife: (A) change in
global percent cover of coral reef outside of marine protected areas [percent change at each time point
measured relative to percent coral cover in 1988 (44)]; (B) global change in mangrove area (percent
change each year measured relative to mangrove area in 1980) (117); (C) change in the cumulative number
of marine wind turbines installed worldwide (118); (D) change in the cumulative area of seabed under
contract for mineral extraction in international waters (119); (E) trends in the volume of global container
port traffic (120); and (F) change in the cumulative number of oxygen depleted marine “dead zones.” See
details and data sources in (8).
RESEARCH | REVIEW

present course of marine defaunation. We must
play catch-up in the realm of marine protected
area establishment, tailoring them to be opera-
tional in our changing oceans. We must also
carefully construct marine spatial management
plans for the vast regions in between these areas
to help ensure that marine mining, energy devel-
opment, and intensive aquaculture take impor-
tant marine wildlife habitats into consideration,
not vice versa. All of this is a tall order, but the
oceans remain relatively full of the raw faunal
ingredients and still contain a sufficient degree
of resilient capacity so that the goal of reversing
the current crisis of marine defaunation remains
within reach. The next several decades will be
those in which we choose the fate of the future of
marine wildlife.
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ACKNOWLEDGMENTS
We thank A. Barnosky, N. Dulvy, M. Galetti, C. Golden, T. Rogier,
E. Selig, T. White, the World Database on Protected Areas,
B. Worm, and H. Young. Figure images were contributed by
T. Llobet, A. Musser, and IAN/UMCES (112). Funding was provided
by the National Science Foundation and the Gordon and
Betty Moore Foundation.
SUPPLEMENTARY MATERIALS
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Tables S1 and S2
References (121–298)
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