REVIEW SUMMARY

MARINE CONSERVATION

Marine defaunation Animal loss inthe global oceanDouglas J McCauley Malin L Pinsky Stephen R Palumbi James A EstesFrancis H Joyce Robert R Warner

BACKGROUND Comparing patterns of ter-restrial and marine defaunation helps toplace human impacts on marine fauna incontext and to navigate toward recovery De-

faunation began in ear-nest tens of thousands ofyears later in the oceansthan it did on land Al-though defaunation hasbeen less severe in theoceans than on land our

effects on marine animals are increasing inpace and impact Humans have caused fewcomplete extinctions in the sea but we areresponsible for many ecological commercialand local extinctions Despite our late starthumans have already powerfully changedvirtually all major marine ecosystems

ADVANCES Humans have profoundly de-creased the abundance of both large (eg

whales) and small (eg anchovies) marinefauna Such declines can generate waves ofecological change that travel both up anddown marine food webs and can alter oceanecosystem functioning Human harvestershave also been a major force of evolutionarychange in the oceans and have reshaped thegenetic structure of marine animal popula-tions Climate change threatens to acceleratemarine defaunation over the next centuryThe high mobility of many marine animalsoffers some increased though limited ca-pacity for marine species to respond to cli-mate stress but it also exposes many speciesto increased risk from other stressors Be-cause humans are intensely reliant on oceanecosystems for food and other ecosystem ser-vices we are deeply affected by all of theseforecasted changesThree lessons emerge when comparing

the marine and terrestrial defaunation ex-

periences (i) todayrsquos low rates of marineextinction may be the prelude to a majorextinction pulse similar to that observedon land during the industrial revolution asthe footprint of human ocean use widens(ii) effectively slowing ocean defaunationrequires both protected areas and care-ful management of the intervening oceanmatrix and (iii) the terrestrial experienceand current trends in ocean use suggestthat habitat destruction is likely to becomean increasingly dominant threat to oceanwildlife over the next 150 years

OUTLOOKWildlife populations in the oceanshave been badly damaged by human activ-ity Nevertheless marine fauna generallyare in better condition than terrestrial faunaFewer marine animal extinctions have oc-curred many geographic ranges have shrunkless and numerous ocean ecosystems re-main more wild than terrestrial ecosystemsConsequently meaningful rehabilitation ofaffected marine animal populations remainswithin the reach of managers Human depen-dency on marine wildlife and the linkedfate of marine and terrestrial fauna necessi-tate that we act quickly to slow the advanceof marine defaunation

RESEARCH

SCIENCE sciencemagorg 16 JANUARY 2015 bull VOL 347 ISSUE 6219 247

Timeline (log scale) of marine and terrestrial defaunation The marine defaunation experience is much less advanced even though humans havebeen harvesting oceanwildlife for thousands of yearsThe recent industrialization of this harvest however initiated an era of intensemarine wildlife declinesIf 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 onlineCorresponding author E-mail douglasmccauleylifesciucsbedu Cite this article as D J McCauley et al Science347 1255641 (2015) DOI 101126science1255641

ON OUR WEB SITE

Read the full articleat httpdxdoiorg101126science1255641

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REVIEW

MARINE CONSERVATION

Marine defaunation Animal loss inthe global oceanDouglas J McCauley1 Malin L Pinsky2 Stephen R Palumbi3 James A Estes4

Francis H Joyce1 Robert R Warner1

Marine defaunation or human-caused animal loss in the oceans emerged forcefully onlyhundreds of years ago whereas terrestrial defaunation has been occurring far longerThough humans have caused few global marine extinctions we have profoundly affectedmarine wildlife altering the functioning and provisioning of services in every oceanCurrent ocean trends coupled with terrestrial defaunation lessons suggest that marinedefaunation rates will rapidly intensify as human use of the oceans industrializes Thoughprotected areas are a powerful tool to harness ocean productivity especially when designedwith future climate in mind additional management strategies will be required Overallhabitat degradation is likely to intensify as a major driver of marine wildlife loss Proactiveintervention can avert a marine defaunation disaster of the magnitude observed on land

Several decades of research on defaunationin terrestrial habitats have revealed a serialloss of mammals birds reptiles and inver-tebrates that previously played importantecological roles (1) Here we review the

major advancements that have been made inunderstanding the historical and contemporaryprocesses of similar defaunation in marine envi-ronments We highlight patterns of similarityand difference between marine and terrestrialdefaunation profiles to identify better ways tounderstand manage and anticipate the effects offuture defaunation in our Anthropocene oceans

Patterns of marine defaunation

Delayed defaunation in the oceans

Defaunation on land began 10000 to 100000 yearsago as humans were expanding their range andcoming into first contact with novel faunalassemblages (2ndash4) By contrast the physical prop-erties of the marine environment limited ourcapacity early on to access and eliminate marineanimal species This difficulty notwithstandinghumans began harvestingmarine animals at least40000 years ago a development that some havesuggested was a defining feature in becomingldquofully modern humansrdquo (5) Even this early harvestaffected local marine fauna (6) However globalrates of marine defaunation only intensified inthe last century with the advent of industrialfishing and the rapid expansion of coastal popu-lations (7) As a result extant globalmarine faunal

assemblages remain todaymore Pleistocene-likeat least with respect to species composition thanterrestrial fauna The delayed onset of intensiveglobal marine defaunation is most visible in acomparative chronology of faunal extinctions inwhich 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 havebeen relatively low The International Union forConservation of Nature (IUCN) records only 15

global extinctions of marine animal species inthe past 514 years (ie limit of IUCN temporalcoverage) and none in the past five decades (8 9)By contrast the IUCN recognizes 514 extinctionsof terrestrial animals during the same period(Fig 1) While approximately six times more an-imal species have been cataloged on land than inthe oceans (10) this imbalance does not explainthe 36-fold difference between terrestrial andmarine animal extinctionsIt is important to note that the status of only a

small fraction of described marine animal spe-cies have been evaluated by the IUCN andmanyassessed species were determined to be data defi-cient (11) (Fig 2) This lack of information neces-sitates that officially reported numbers of extinctand endangered marine fauna be considered asminimum estimates (11) There remain howevera number of data-independent explanations forthe lower extinction rates of marine fauna Ma-rine species for instance tend to be more wide-spread exhibit less endemism and have higherdispersal (12 13)Complacency about the magnitude of contem-

porary marine extinctions is however ill-advisedIf we disregard the gt50000-year head start ofintense terrestrial defaunation (Fig 1) and com-pare only contemporary rates of extinction on landand in the sea a cautionary lesson emerges Ma-rine extinction rates today look similar to themoderate levels of terrestrial extinction observedbefore the industrial revolution (fig S1) Rates ofextinction on land increased dramatically after thisperiod and wemay now be sitting at the precipiceof 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 worldrsquos oceans inadequately

RESEARCH

SCIENCE sciencemagorg 16 JANUARY 2015 bull VOL 347 ISSUE 6219 1255641-1

1Department of Ecology Evolution and Marine BiologyUniversity of California Santa Barbara CA 93106 USA2Department of Ecology Evolution and Natural ResourcesInstitute of Marine and Coastal Sciences Rutgers UniversityNew Brunswick NJ 08901 USA 3Department of BiologyStanford University Hopkins Marine Station Pacific GroveCA 93950 USA 4Department of Ecology and EvolutionaryBiology University of California Santa Cruz CA 95060 USACorresponding author E-mail douglasmccauleylifesciucsbedu

Fig 1 Comparative chronology of human-associatedterrestrial and marine animal extinctions Green barsindicate animal extinctions that occurred on land and bluebars indicate marine animal extinctions Timeline mea-

sures years before 2014 CE Only extinctions occurring less than 55000 years ago are depictedDefaunation has ancient origins on land but has intensified only within the last several hundred years in theoceans See details in (8)

reflects the full impacts of marine defaunationWe recognize three additional types of defaunation-induced extinction

Local extinction

Defaunation has caused numerous geographicrange constrictions in marine animal speciesdriving them locally extinct in many habitatsThese effects have been particularly severe amonglarge pelagic fishes where ~90 of studied spe-cies have exhibited range contractions (8 14)(Fig 3) Local extinctions however are not uniqueto large pelagic predators Close to a third of themarine fishes and invertebrates off the NorthAmerican coasts that can be reliably sampled inscientific trawl surveys (often small to medium-bodied species) have also exhibited range con-tractions (Fig 3) Such contractions can resultfrom the direct elimination of vulnerable subpop-ulations or from region-wide declines in abundance(14) Available data suggest that the magnitudeof the range contractions for this diverse set oftrawl-surveyed marine species is on averageless than the contractions observed for terrestrialanimals such as mammals birds and butterfliesThough data deficiencies are abundant most ma-rine animal species also do not yet seem to exhibitsome of the most extreme range contractionsrecorded for terrestrial animals Asian tigers forexample have lost ~93 of their historical range(15) whereas tiger sharks still range across theworldrsquos oceans (16)

Ecological extinction

Reductions in the abundance of marine animalshave been well documented in the oceans (17)Aggregated population trend data suggest that inthe last four decades marine vertebrates (fishseabirds sea turtles and marine mammals) havedeclined in abundance by on average 22 (18)Marine fishes have declined in aggregate by38 (17) and certain baleen whales by 80 to 90(19) Many of these declines have been termedecological extinctionsmdashalthough the species inquestion are still extant they are no longer suf-ficiently abundant to perform their functionalroles Ecological extinctions are well known interrestrial environments and have been demon-strated to be just as disruptive as species extinc-tions (20) On land we know of the phenomenonof ldquoempty forestsrdquo where ecological extinctions offorest fauna alter tree recruitment reshape plantdispersal and cause population explosions ofsmall mammals (1 20 21) We are now observ-ing the proliferation of ldquoempty reefsrdquo ldquoemptyestuariesrdquo and ldquoempty baysrdquo (7 14 22)

Commercial extinction

Species that drop below an abundance level atwhich they can be economically harvested are ex-tinct from a commercial standpoint On land com-mercial extinctions affected species ranging fromchinchilla to bison (23) Cases of commercial ex-tinction are also common in the oceans Gray whaleswere commercially hunted starting in the 1840sBy 1900 their numbers were so depleted thattargeted harvest of this species was no longer re-

gionally tenable (24) Likewise the great whalesin Antarctica were serially hunted to commer-cial extinction (25)Not all species however are so ldquoluckyrdquo as to

have human harvesters desist when they becomeextremely rare Demand and prices for certainhighly prized marine wildlife can continue to in-crease as these animals become less abundantmdashaphenomenon termed the anthropogenic Alleeeffect (26) Individual bluefin tuna can sell forgtUS$100000 rare sea cucumbers gtUS$400kgand high-quality shark fins for gtUS$100kg Suchspecies are the rhinos of the oceanmdashthey maynever be too rare to be hunted

Differential vulnerability to defaunation

Are certain marine animals more at risk thanothers to defaunation There has been consider-able attention given to harvester effects on largemarine animals (27) Selective declines of large-bodied animals appear to be evident in certaincontexts (28 29) As a result of such pressuresturtles whales sharks andmany large fishes arenow ecologically extinct inmany ecosystems andthe size spectra (abundancendashbody mass relation-ships) of many communities have changed consid-erably (7 30 31) Marine defaunation howeverhas not caused many global extinctions of large-bodied speciesMost large-bodiedmarine animalspecies still exist somewhere in the ocean Bycontrast on land we have observed the extinc-tion of numerous large terrestrial species and aprofound restructuring of the size distribution ofland-animal species assemblages Themean bodymass for the list of surviving terrestrial mammal

species for example is significantly smaller thanthe bodymass of terrestrial mammal species thatlived during the Pleistocene (1 32) Such effectshowever are not evident formarinemammals (8)(fig S2) Recent reviews have drawn attention tothe fact that humans can also intensely and ef-fectively deplete populations of smaller marineanimals (29 33) These observations have inspireda belated surge in interest in protecting smallforage fishes in the oceansA review of modern marine extinctions and list-

ings of species on the brink of extinction revealsfurther insight into aggregate patterns of differen-tial defaunation risk in the oceans (Fig 2) Seaturtles have the highest proportion of endangeredspecies among commonly recognized groupings ofmarine fauna No modern sea turtle species how-ever have yet gone extinct Pinnipeds and marinemustelids followed very closely by seabirds andshorebirds have experienced the highest propor-tion of species extinctionsMany of themost threat-ened groups of marine animals are those thatdirectly interact with land (and land-based humans)during some portion of their life history (Fig 2) Ter-restrial contactmay also explainwhy diadromousbrackish water fishes are more threatened thanexclusively 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 ldquowinnersrdquo or species that are profiting inAnthropocene oceansMany of thesewinners aresmaller and ldquoweedierrdquo (eg better colonizing andfaster reproducing) speciesMarine invertebratesin particular have often been cited as examples of

1255641-2 16 JANUARY 2015 bull VOL 347 ISSUE 6219 sciencemagorg SCIENCE

Fig 2 Marine defaunation threatThreat from defaunation is portrayed for different groups of marine faunaas chronicled by the IUCNRed List (113)Threat categories include ldquoextinctrdquo (orange) ldquoendangeredrdquo (red IUCNcategories ldquocritically endangeredrdquo + ldquoendangeredrdquo) ldquodata deficientrdquo (light gray) and ldquounreviewedrdquo (dark gray)Groups that contact land during some portion of their life history (green) are distinguished from species that donot (light blue)The total numberof species estimated in each group is listed below the graphSpecies groupingsare coded as follows ST sea turtles PO pinnipeds andmarinemustelids SS seabirds and shorebirds SSL seasnakes and marine lizard CS cetaceans and sirenians DBRF diadromousbrackish ray-finned fishes CFcartilaginous fishesMRF exclusivelymarine ray-finned fishesMImarine invertebrates See furtherdetails in (8)

RESEARCH | REVIEW

species that are succeeding in the face of intensemarine defaunation lobster proliferated as pred-atory groundfish declined (34) prawns increasedand replaced the dominance of finfish in land-ings (35) and urchin populations exploded in theabsence of their predators and competitors (36)Numerousmid-level predators also appear to ben-efit from the loss of top predators [eg small sharksand rays (37)]mdasha phenomenon analogous tomeso-predator release observed in terrestrial spheres(38) The status held by some of these defaunationwinners in the oceansmay however be ephemeralMany of the marine species that have initiallyflourished as a result of defaunation have them-selves become targets forharvest by prey-switchinghumans 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 ecosystemssuggest that coastal wildlife habitats have beenmore influenced than deep-water or pelagic ecosys-tems (40) The vulnerability of coastal areas pre-sumably results fromease of access to coastal zonesThis relationship between access and defaunationrisk manifests itself also at smaller spatial scaleswith populations ofmarinewildlife closest to tradenetworks and human settlements appearing oftento bemore heavily defaunated (41 42) The relativeinsulation that animal populations in regions likethe deep oceans presently experience howevermay be short-livedbecausedepletions of shallow-water marine resources and the developmentof new technologies have created both the ca-pacity and incentive to fish mine and drill oilin some of the deepest parts of the sea (28 43)Coral reefs in particular have consistently

been highlighted asmarine ecosystems of special

concern to defaunation Coral reefs have beenexposed to a wide range of impacts and distur-bances including sedimentation and pollutionthermal stress disease destructive fishing andcoastal development (44 45) Such stressors nega-tively influence both corals and the millions ofspecies that live within and depend upon reefs(46) Risk however is not uniform even across areefscape Shallow backreef pools for exampleroutinely overheat and consequently corals inthese parts of the reef aremore resistant to oceanwarming (47) Environmentally heterogeneousareas may in fact act as important natural fac-tories of adaptation that will buffer against sometypes of marine defaunation

Effects of marine defaunation

Extended consequences ofmarine defaunation

Marine defaunation has had far-reaching effectson ocean ecosystems Depletions of a wide rangeof ecologically important marine fauna such ascod sea otters great whales and sharks havetriggered cascading effects that propagate acrossmarine systems (37 48ndash51) Operating in the op-posite direction from trophic cascades are changesthat travel from the bottom to the top of foodchains as a result of the declining abundance oflowerndashtrophic level organisms (52) Depletions offauna such as anchovies sardines and krill causereductions in food for higher-trophic level animalssuch 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 onmarine

ecosystems also occur beyond the bounds of thesetop-down or bottom-up effects Defaunation canreduce cross-system connectivity (54 55) decreaseecosystem stability (56) and alter patterns of bio-geochemical cycling (57) The ill effects of food

webdisarticulation can be further amplifiedwhenthey occur in association with other marine dis-turbances For example mass releases of dis-carded plant fertilizers into marine ecosystemsfromwhich defaunation has eliminated importantconsumers can create ldquoproductivity explosionsrdquo byfueling overgrowth of microbes and algae thatfail to be routed into food webs (58 59)The selective force of human predation has

also been sufficiently strong and protracted soas to have altered the evolutionary trajectory ofnumerous species of harvested marine fauna(60) Harvest has driven many marine animalspecies to become smaller and thinner to growmore slowly to be less fecund and to reproduceat smaller sizes (61) There is also evidence thatharvest can reduce the genetic diversity of manymarine animal populations (62) The genetic ef-fects of defaunation represent a loss of adaptivepotential that may impair the resilient capacityof ocean wildlife (63)

Importance of marine defaunationto humans

Marine defaunation is already affecting humanwell-being in numerous ways by imperiling foodsustainability increasing social conflict impair-ing stormprotection and reducing flows of otherecosystem services (64 65) The most conspicu-ous service that marine fauna make to society isthe contribution of their own bodies to globaldiets Marine animals primarily fishes make upa large proportion of global protein intake andthis contribution is especially strong for impov-erished coastal nations (66) According to theUN Food and Agriculture Organization (FAO)40 times more wild animal biomass is harvestedfrom the oceans than from land (67) Declines inthis source of free-range marine food represent amajor 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 cloudformation that appears to be stimulated by coralemissions of dimethylsulphoniopropionate (DMSP)(57 68 69) Another key service given forecastsof increasingly intense weather events and sea-level rise is coastal protection Coral oyster andother living reefs can dissipate up to 97 of thewave energy reaching them thus protecting builtstructures and human lives (70) In some casescorals are more than just perimeter buffers theyalso serve as the living platform upon which en-tire countries (eg the Maldives Kiribati theMarshall Islands) and entire cultures have beenfounded Atoll-living human populations in theseareas depend on the long-term health of theseanimate pedestals to literally hold their livestogether

Outlook and ways forward

Will climate change exacerbatemarine defaunation

The implications of climate change upon marinedefaunation are shaped by ocean physicsMarinespecies live in a vast globally connected fluid

SCIENCE sciencemagorg 16 JANUARY 2015 bull VOL 347 ISSUE 6219 1255641-3

Fig 3 Comparisons of range contractions for select marine and terrestrial faunaTerrestrial (green)and marine cases (blue) include evaluations of geographical range change for 43 North Americanmammals over the last ~200 years (NM) (114) 18 Indian mammals over the last 30 years (IM) (115) 201British birds from ~1970 to 1997 (BB) and 58 British butterflies from ~1976 to 1997 (BF) (116) 12 globallarge pelagic fishes from the 1960s to 2000s (PF) (14) and 327 trawl-surveyed North American marinefish and invertebrates from the 1970s to 2000s (TFI) (A) Percent of species whose ranges havecontractedwith binomial confidence intervals and (B) distribution of percent contraction for those speciesthat have contracted (violin plot) Sample sizes are shown above each data pointwhite 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 capacityand has exhibited a historically robust capabilityto buffer temperature change over daily annualand 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 theoceans may have left many subtidal marine an-imals poorly prepared relative to terrestrial coun-terparts for the temperature increases associatedwith global warming The same logic supportsrelated predictions that terrestrial fauna living inmore thermally stable environmentswill bemorevulnerable to warming than those found in areasof greater temperature variability (72)Ocean warming presents obvious challenges

to polar marine fauna trapped in thermal deadends (73) Tropical marine species are howeveralso highly sensitive to small increases in temper-ature For example coastal crabs on tropicalshores live closer to their upper thermal maximathan do similar temperate species (74) Likewisethe symbiosis of corals and dinoflagellates isfamously sensitive to rapid increases of only 1deg to2degC (75) Even though corals exhibit the capacityfor adaptation (47) coral bleaching events areexpected to be more common and consequentlymore stressful by the end of the century (76) Theeffects of rising ocean temperature extend wellbeyond coral reefs and are predicted to affectboth the adult and juvenile stages of a diverse setof marine species (77) to reshuffle marine com-munity composition (78) and to potentially alterthe overall structure and dynamics of entire ma-rine faunal communities (79)The wide range of other climate change-

associated alterations in seawater chemistryand physicsmdashincluding ocean acidification anoxiaocean circulation shifts changes in stratificationand changes in primary productivitymdashwill fun-damentally influence marine fauna Ocean acid-ification for example makes marine animalshell building more physiologically costly can

diminish animal sensory abilities and can altergrowth trajectories (80 81) Climate change im-pacts on phytoplankton can further accentuatedefaunation risk (82) At the same time thathumans are reducing the abundance of marineforage fish through direct harvest we also maybe indirectly reducing the planktonic food forforage fish and related consumers in manyregions

Mobility and managing defaunation

Many marine animals on average have signifi-cantly larger home ranges as adults [Fig 4 andfigs S3 and S4 (8)] and disperse greater dis-tances as juveniles than their terrestrial counter-parts (13) This wide-ranging behavior of manymarine species complicates the management ofocean wildlife as species often traverse multiplemanagement jurisdictions (83ndash85) On the otherhand the greater mobility of many marine ani-mal species may help them to better follow thevelocity of climate change and to colonize andrecolonize habitats so long as source populationrefuges 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 farbehind advancements made on land with anupper-bound estimate of only about 36 of theworldrsquos oceans now protected (8) (fig S5) Onesource of optimism for slowing marine defauna-tion particularly for mobile species is that themean size of marine protected areas has in-creased greatly in recent years (fig S5) Howevermostmarine protected areas remain smaller (me-dian 45 km2) than the home range size of manymarine animals (Fig 4) Though much is lost inthis type of crude comparison this observationhighlights what may be an important discon-nect between the scales at which wildlife usethe oceans and the scale at which we typicallymanage the oceans

This spatial mismatch is just one of manyreasons why protected areas cannot be the fullsolution for managing defaunation (83) Welearned this lesson arguably too late on landProtected areas can legitimately be viewed assome of our proudest conservation achievementson land (eg Yosemite Serengeti ChitwanNatio-nal Parks) and yet with four times more terres-trial area protected than marine protected areawe have still failed to satisfactorily rein in ter-restrial defaunation (1) (fig S5) The realizationthat more was needed to curb terrestrial defau-nation inspired a wave of effort to do conserva-tion out of the bounds of terrestrial protectedareas (eg conservation easements and corridorprojects) The delayed implementation of thesestrategies has however often relegated terres-trial conservation to operatingmore as a retroac-tive enterprise aimedat restoringdamagedhabitatsand triaging wildlife losses already underway Inthe oceans we are uniquely positioned to pre-emptively manage defaunation We can learnfrom the terrestrial defaunation experience thatprotected areas are valuable tools but that wemust proactively introduce measures to manageour impacts onmarine fauna in the vast majorityof the global oceans that is unprotectedStrategies tomeet these goals include incentive-

based fisheries management policies (89) spa-tially ambitious ecosystem-based managementplans (83) and emerging efforts to preemptivelyzone human activities that affect marine wildlife(90 91) There have been mixed responses amongmarine managers as to whether and how to em-brace these tools but more complete implementa-tion of these strategies will help chart a sustainablefuture for marine wildlife (43 90 91) A secondcomplementary set of goals is to incorporate cli-mate change intomarine protected area schemesto build networks that will provide protection forocean wildlife into the next century (92) Suchbuilt-in climate plans were unavailable and evenunthinkable when many major terrestrial parkswere laid out but data tools and opportunityexist to do this thoughtfully now in the oceans

Habitat degradation The coming threatto marine fauna

Many early extinctions of terrestrial fauna arebelieved to have been heavily influenced by hu-man hunting (2 93) whereas habitat loss ap-pears to be the primary driver of contemporarydefaunation on land (1 11 86 94) By contrastmarine defaunation today remains mainly driv-en by human harvest (95 96) If the trajectory ofterrestrial defaunation is any indicator we shouldanticipate that habitat alteration will ascendin importance as a future driver of marinedefaunationSigns 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 extensivelyhunted are now threatened by noise disruptionoil exploration vessel traffic and entanglementwith moored marine gear (fig S6) (97) Habitat-modifying fishing practices (eg bottom trawling)

1255641-4 16 JANUARY 2015 bull VOL 347 ISSUE 6219 sciencemagorg SCIENCE

Fig 4 Mobility of ter-restrial and marinefauna Because mobil-ity shapes defaunationrisk we compare thesize-standardizedhome range size of arepresentative selec-tion of marine (blue)and terrestrial (green)vertebrates Data arepresented for adultsover a full range ofanimal body sizesplotted on a logarith-mic scale Speciesinclude seabirdsmarine reptiles marinefishes marine mam-mals terrestrial birdsterrestrial reptiles andterrestrial mammals (see details in (8) table S2 and fig S3) Regression lines enclosed by shadedconfidence intervals are plotted for all marine and all terrestrial species The dotted red line demarcatesthe current median size of all marine protected areas (MPAs)

RESEARCH | REVIEW

have affected ~50 million km2 of seafloor (40)Trawlingmay represent just the beginning of ourcapacity to alter marine habitats Developmentof coastal cities where ~40 of the human pop-ulation lives (98) has an insatiable demand forcoastal land Countries like the United ArabEmirates and China have elected to meet thisdemandby ldquoseasteadingrdquomdashconstructing ambitiousnew artificial lands in the ocean (99) Technolog-ical advancement in seafloor mining dredgingoil and gas extraction tidalwave energy gener-ation and marine transport is fueling rapid ex-pansion of these marine industries (43 100)Even farming is increasing in the sea Projectionsnow suggest that in less than 20 years aquacul-ture will provide more fish for human consump-tion thanwild capture fisheries (101) Fish farminglike crop farming can consume or drastically alternatural habitatswhen carried out carelessly (102)Many of these emerging marine developmentactivities are reminiscent of the types of rapidenvironmental change observed on land duringthe industrial revolution that were associated

with pronounced increases in rates of terrestrialdefaunationMarine habitatsmay eventually jointhe ranks of terrestrial frontier areas such asthe American West the Brazilian Amazon andAlaska which were once believed to be imper-vious to development pollution and degradation

Land to sea defaunation connections

The ecologies of marine and terrestrial systemsare dynamically linked Impacts on terrestrialfauna can perturb the ecology of marine fauna(54) and vice versa (103) Furthermore the healthof marine animal populations is interactivelyconnected to the health of terrestrial wildlifepopulationsmdashand to the health of society Peoplein West Africa for example exploit wild terres-trial fauna more heavily in years when marinefauna are in short supply (104) It is not yet clearhow these linkages between marine and terres-trial defaunation will play out at the global levelWill decreasing yields from marine fisheries forexample require that more terrestrial wildlandsbe brought into human service as fields and

pastures tomeet shortfalls of ocean-derived foodsMarine ecosystem managers would do well tobetter incorporate considerations of land-to-seadefaunation connections in decision making

Not all bad news

It is easy to focus on the negative course thatdefaunation has taken in the oceans Humanshave however demonstrated a powerful capac-ity to reverse some of the most severe impactsthat we have had on ocean fauna and manymarinewildlife populations demonstrate immensepotential for resilience (47 105ndash107) The sea otterthe ecological czar of many coastal ecosystemswas thought to be extinct in the early 1900s butwas rediscovered in 1938 protected and hasresumed its key ecological role in large parts ofthe coastal North Pacific and Bering Sea (108)The reef ecosystems of Enewetak and BikiniAtolls present another potent example TheUnited States detonated 66 nuclear explosionsabove and below the water of these coral reefsin the 1940s and 1950s Less than 50 years laterthe coral and reef fish fauna on these reefsrecovered to the point where they were beingdescribed as remarkably healthy (109)There is great reason to worry however that

we are beginning to erode some of the systemicresilience of marine animal communities (110)Atomic attacks on local marine fauna are onething but an unimpeded transition toward anera of global chemical warfare on marine eco-systems (eg ocean acidification anoxia) mayretard or arrest the intrinsic capacity of marinefauna to bounce back from defaunation (75 111)

Conclusions

Onmany levels defaunation in the oceans has todate been less severe than defaunation on landDeveloping this contrast is useful because ourmore advanced terrestrial defaunation experi-ence can serve as a harbinger for the possiblefuture of marine defaunation (3) Humans havehad profoundly deleterious impacts on marineanimal populations but there is still time andthere exist mechanisms to avert the kinds ofdefaunation disasters observed on land Fewmarine extinctions have occurredmany subtidalmarine habitats are today less developed lesspolluted and more wild than their terrestrialcounterparts global body size distributions ofextant marine animal species have been mostlyunchanged in the oceans andmanymarine faunahave not yet experienced range contractions assevere as those observed on landWe are not necessarily doomed to helplessly

recapitulate the defaunation processes observedon land in the oceans intensifying marine hunt-ing until it becomes untenable and then embarkingon an era of large-scale marine habitat modifi-cation However if these actions move forwardin tandem we may finally trigger a wave of ma-rine extinctions of the same intensity as thatobserved on land Efforts to slow climate changerebuild affected animal populations and intelli-gently engage the coming wave of new marinedevelopment activities will all help to change the

SCIENCE sciencemagorg 16 JANUARY 2015 bull VOL 347 ISSUE 6219 1255641-5

Fig 5 Habitat change in the global oceans Trends in six indicators of marine habitat modificationsuggest that habitat changemay become an increasingly important threat tomarine wildlife (A) change inglobal percent cover of coral reef outside of marine protected areas [percent change at each time pointmeasured relative to percent coral cover in 1988 (44)] (B) global change in mangrove area (percentchange each yearmeasured relative tomangrove area in 1980) (117) (C) change in the cumulative numberof marine wind turbines installed worldwide (118) (D) change in the cumulative area of seabed undercontract for mineral extraction in international waters (119) (E) trends in the volume of global containerport traffic (120) and (F) change in the cumulative number of oxygen depleted marine ldquodead zonesrdquo Seedetails and data sources in (8)

RESEARCH | REVIEW

present course of marine defaunation We mustplay catch-up in the realm of marine protectedarea establishment tailoring them to be opera-tional in our changing oceans We must alsocarefully construct marine spatial managementplans for the vast regions in between these areasto help ensure that marine mining energy devel-opment and intensive aquaculture take impor-tant marine wildlife habitats into considerationnot vice versa All of this is a tall order but theoceans remain relatively full of the raw faunalingredients and still contain a sufficient degreeof resilient capacity so that the goal of reversingthe current crisis of marine defaunation remainswithin reach The next several decades will bethose in which we choose the fate of the future ofmarine wildlife

REFERENCES AND NOTES

1 R Dirzo et al Defaunation in the Anthropocene Science345 401ndash406 (2014) doi 101126science1251817pmid 25061202

2 A D Barnosky P L Koch R S Feranec S L WingA B Shabel Assessing the causes of late Pleistoceneextinctions on the continents Science 306 70ndash75 (2004)doi 101126science1101476 pmid 15459379

3 P L Koch A D Barnosky Late Quaternary extinctions Stateof the debate Annu Rev Ecol Evol Syst 37 215ndash250(2006) doi 101146annurevecolsys34011802132415

4 A D Barnosky et al Prelude to the Anthropocene Two newNorth American land mammal ages (NALMAs) AnthropolRev (2014) doi 1011772053019614547433

5 S OrsquoConnor R Ono C Clarkson Pelagic fishing at 42000 yearsbefore the present and the maritime skills of modern humansScience 334 1117ndash1121 (2011) doi 101126science1207703pmid 22116883

6 H K Lotze et al Depletion degradation and recoverypotential of estuaries and coastal seas Science 3121806ndash1809 (2006) doi 101126science1128035pmid 16794081

7 J B C Jackson et al Historical overfishing and the recentcollapse of coastal ecosystems Science 293 629ndash637(2001) doi 101126science1059199 pmid 11474098

8 Materials and methods are available as supplementarymaterials on Science Online

9 IUCN The IUCN Red List of Threatened Species Version20142 (2014) available at wwwiucnredlistorg

10 C Mora D P Tittensor S Adl A G B Simpson B WormHow many species are there on Earth and in the oceanPLOS Biol 9 e1001127 (2011) doi 101371journalpbio1001127 pmid 21886479

11 S L Pimm et al The biodiversity of species and their ratesof extinction distribution and protection Science 3441246752 (2014) doi 101126science1246752 pmid 24876501

12 E Alison Kay S R Palumbi Endemism and evolution inHawaiian marine invertebrates Trends Ecol Evol 2 183ndash186(1987) doi 1010160169-5347(87)90017-6 pmid 21227847

13 B P Kinlan S D Gaines Propagule dispersal in marine andterrestrial environments A community perspective Ecology84 2007ndash2020 (2003) doi 10189001-0622

14 B Worm D P Tittensor Range contraction in large pelagicpredators Proc Natl Acad Sci USA 108 11942ndash11947(2011) doi 101073pnas1102353108 pmid 21693644

15 E Dinerstein et al The Fate of wild tigers Bioscience 57508ndash514 (2007) doi 101641B570608

16 S L Fowler et al Eds Sharks Rays and Chimaeras TheStatus of the Chondrichthyan Fishes Status Survey (IUCNCambridge UK 2005)

17 J A Hutchings C Minto D Ricard J K Baum O P JensenTrends in the abundance of marine fishes Can J Fish AquatSci 67 1205ndash1210 (2010) doi 101139F10-081

18 WWF Living Planet Report (WWF International GlandSwitzerland 2012) httpwwfpandaorglpr

19 A M Springer et al Sequential megafaunal collapse in theNorth Pacific Ocean An ongoing legacy of industrial whalingProc Natl Acad Sci USA 100 12223ndash12228 (2003)doi 101073pnas1635156100 pmid 14526101

20 K H Redford The empty forest Bioscience 42 412ndash422(1992) doi 1023071311860

21 H S Young et al Declines in large wildlife increaselandscape-level prevalence of rodent-borne disease in AfricaProc Natl Acad Sci USA 111 7036ndash7041 (2014)doi 101073pnas1404958111 pmid 24778215

22 D J McCauley et al Positive and negative effects of athreatened parrotfish on reef ecosystems Conserv Biol28 1312ndash1321 (2014) doi 101111cobi12314pmid 25065396

23 J E Jimeacutenez The extirpation and current status of wildchinchillas Chinchilla lanigera and C brevicaudata Biol Conserv77 1ndash6 (1996) doi 1010160006-3207(95)00116-6

24 R R Reeves T D Smith Commercial whaling especially forgray whales Eschrichtius robustus and humpback whalesMegaptera novaeangliae at California and Baja Californiashore stations in the 19th century (1854ndash1899) Mar FishRev 72 1ndash25 (2010)

25 R Hilborn et al State of the worldrsquos fisheries Annu RevEnviron Resour 28 359ndash399 (2003) doi 101146annurevenergy28050302105509

26 F Courchamp et al Rarity value and species extinctionThe anthropogenic Allee effect PLOS Biol 4 e415 (2006)doi 101371journalpbio0040415 pmid 17132047

27 D Pauly V Christensen J Dalsgaard R Froese F Torres JrFishing down marine food webs Science 279 860ndash863(1998) doi 101126science2795352860 pmid 9452385

28 S A Sethi T A Branch R Watson Global fisherydevelopment patterns are driven by profit but not trophiclevel Proc Natl Acad Sci USA 107 12163ndash12167 (2010)doi 101073pnas1003236107 pmid 20566867

29 M L Pinsky O P Jensen D Ricard S R PalumbiUnexpected patterns of fisheries collapse in the worldrsquosoceans Proc Natl Acad Sci USA 108 8317ndash8322 (2011)doi 101073pnas1015313108 pmid 21536889

30 J B C Jackson Ecological extinction and evolution in thebrave new ocean Proc Natl Acad Sci USA 105 (suppl 1)11458ndash11465 (2008) doi 101073pnas0802812105pmid 18695220

31 S Jennings J L Blanchard Fish abundance with no fishingPredictions based on macroecological theory J Anim Ecol73 632ndash642 (2004) doi 101111j0021-8790200400839x

32 S K Lyons F A Smith J H Brown Of mice mastodonsand men Human-mediated extinctions on four continentsEvol Ecol Res 6 339ndash358 (2004)

33 A D Smith et al Impacts of fishing low-trophic level specieson marine ecosystems Science 333 1147ndash1150 (2011)doi 101126science1209395 pmid 21778363

34 R S Steneck J Vavrinec A V Leland Accelerating trophic-level dysfunction in kelp forest ecosystems of the westernNorth Atlantic Ecosystems 7 323ndash332 (2004) doi 101007s10021-004-0240-6

35 B Worm R A Myers Meta-analysis of codndashshrimpinteractions reveals top-down control in oceanic food websEcology 84 162ndash173 (2003) doi 1018900012-9658(2003)084[0162MAOCSI]20CO2

36 D O Duggins C A Simenstad J A Estes Magnification ofsecondary production by kelp detritus in coastal marineecosystems Science 245 170ndash173 (1989) doi 101126science2454914170 pmid 17787876

37 R A Myers J K Baum T D Shepherd S P PowersC H Peterson Cascading effects of the loss of apexpredatory sharks from a coastal ocean Science 3151846ndash1850 (2007) doi 101126science1138657pmid 17395829

38 L R Prugh et al The Rise of the Mesopredator Bioscience59 779ndash791 (2009) doi 101525bio20095999

39 S C Anderson J Mills Flemming R Watson H K LotzeRapid global expansion of invertebrate fisheries Trendsdrivers and ecosystem effects PLOS ONE 6 e14735 (2011)doi 101371journalpone0014735 pmid 21408090

40 B S Halpern et al A global map of human impact on marineecosystems Science 319 948ndash952 (2008) doi 101126science1149345 pmid 18276889

41 D J McCauley et al Conservation at the edges of the worldBiol Conserv 165 139ndash145 (2013) doi 101016jbiocon201305026

42 J E Cinner N A J Graham C Huchery M A MacneilGlobal effects of local human population density and distanceto markets on the condition of coral reef fisheries Conserv Biol27 453ndash458 (2013) doi 101111j1523-1739201201933xpmid 23025334

43 K J Mengerink et al A call for deep-ocean stewardshipScience 344 696ndash698 (2014) doi 101126science1251458pmid 24833377

44 E R Selig K S Casey J F Bruno Temperature-drivencoral decline The role of marine protected areas Glob ChangeBiol 18 1561ndash1570 (2012) doi 101111j1365-2486201202658x

45 J F Bruno E R Selig Regional decline of coral cover in theIndo-Pacific Timing extent and subregional comparisonsPLOS ONE 2 e711 (2007) doi 101371journalpone0000711pmid 17684557

46 C M Roberts et al Marine biodiversity hotspots andconservation priorities for tropical reefs Science 2951280ndash1284 (2002) doi 101126science1067728pmid 11847338

47 S R Palumbi D J Barshis N Traylor-Knowles R A BayMechanisms of reef coral resistance to future climatechange Science 344 895ndash898 (2014) doi 101126science1251336 pmid 24762535

48 J A Estes et al Trophic downgrading of planet EarthScience 333 301ndash306 (2011) doi 101126science1205106pmid 21764740

49 D J McCauley et al Acute effects of removing large fishfrom a near-pristine coral reef Mar Biol 157 2739ndash2750(2010) doi 101007s00227-010-1533-2 pmid 24391253

50 J A Estes Whales Whaling and Ocean Ecosystems (Univ ofCalifornia Press Berkeley CA 2006)

51 J Terborgh J A Estes Trophic Cascades Predators Preyand the Changing Dynamics of Nature (Island PressWashington DC 2013)

52 D J McCauley F Keesing T P Young B F AllanR M Pringle Indirect effects of large herbivores on snakes inan African savanna Ecology 87 2657ndash2663 (2006)doi 1018900012-9658(2006)87[2657IEOLHO]20CO2pmid 17089673

53 P M Cury et al Global seabird response to forage fishdepletionmdashone-third for the birds Science 334 1703ndash1706(2011) doi 101126science1212928 pmid 22194577

54 D J McCauley et al From wing to wing The persistence oflong ecological interaction chains in less-disturbedecosystems Sci Rep 2 409 (2012) doi 101038srep00409

55 D J McCauley et al Assessing the effects of large mobilepredators on ecosystem connectivity Ecol Appl 221711ndash1717 (2012) doi 10189011-16531 pmid 23092009

56 G L Britten et al Predator decline leads to decreasedstability in a coastal fish community Ecol Lett 17 1518ndash1525(2014) doi 101111ele12354

57 J Roman et al Whales as marine ecosystem engineersFront Ecol Environ 12 377ndash385 (2014) doi 101890130220

58 J M Pandolfi et al Ecology Are US coral reefs on theslippery slope to slime Science 307 1725ndash1726 (2005)doi 101126science1104258 pmid 15774744

59 S R Palumbi A R Palumbi The Extreme Life of the Sea(Princeton Univ Press Princeton NJ 2014)

60 S R Palumbi Humans as the worldrsquos greatest evolutionaryforce Science 293 1786ndash1790 (2001) doi 101126science29355361786 pmid 11546863

61 C Joslashrgensen et al Ecology Managing evolving fish stocksScience 318 1247ndash1248 (2007) doi 101126science1148089 pmid 18033868

62 M L Pinsky S R Palumbi Meta-analysis reveals lowergenetic diversity in overfished populations Mol Ecol 2329ndash39 (2014) doi 101111mec12509 pmid 24372754

63 M R Walsh S B Munch S Chiba D O ConoverMaladaptive changes in multiple traits caused by fishingImpediments to population recovery Ecol Lett 9 142ndash148(2006) doi 101111j1461-0248200500858x pmid 16958879

64 B Worm et al Impacts of biodiversity loss on oceanecosystem services Science 314 787ndash790 (2006)doi 101126science1132294 pmid 17082450

65 J S Brashares et al Wildlife decline and social conflictScience 345 376ndash378 (2014) doi 101126science1256734pmid 25061187

66 Fisheries and Aquaculture Department FAO ldquoThe State ofWorld Fisheries and Aquaculture 2012rdquo (FAO Rome 2012)

67 FAO FAOSTAT (2012) available at httpfaostat3faoorgfaostat-gatewaygotohomeE

68 C C Wilmers J A Estes M Edwards K L LaidreB Konar Do trophic cascades affect the storage andflux of atmospheric carbon An analysis of sea otters andkelp forests Front Ecol Environ 10 409ndash415 (2012)doi 101890110176

69 J-B Raina et al DMSP biosynthesis by an animal and itsrole in coral thermal stress response Nature 502 677ndash680(2013) doi 101038nature12677 pmid 24153189

1255641-6 16 JANUARY 2015 bull VOL 347 ISSUE 6219 sciencemagorg SCIENCE

RESEARCH | REVIEW

reflects the full impacts of marine defaunationWe recognize three additional types of defaunation-induced extinction

Local extinction

Defaunation has caused numerous geographicrange constrictions in marine animal speciesdriving them locally extinct in many habitatsThese effects have been particularly severe amonglarge pelagic fishes where ~90 of studied spe-cies have exhibited range contractions (8 14)(Fig 3) Local extinctions however are not uniqueto large pelagic predators Close to a third of themarine fishes and invertebrates off the NorthAmerican coasts that can be reliably sampled inscientific trawl surveys (often small to medium-bodied species) have also exhibited range con-tractions (Fig 3) Such contractions can resultfrom the direct elimination of vulnerable subpop-ulations or from region-wide declines in abundance(14) Available data suggest that the magnitudeof the range contractions for this diverse set oftrawl-surveyed marine species is on averageless than the contractions observed for terrestrialanimals such as mammals birds and butterfliesThough data deficiencies are abundant most ma-rine animal species also do not yet seem to exhibitsome of the most extreme range contractionsrecorded for terrestrial animals Asian tigers forexample have lost ~93 of their historical range(15) whereas tiger sharks still range across theworldrsquos oceans (16)

Ecological extinction

Reductions in the abundance of marine animalshave been well documented in the oceans (17)Aggregated population trend data suggest that inthe last four decades marine vertebrates (fishseabirds sea turtles and marine mammals) havedeclined in abundance by on average 22 (18)Marine fishes have declined in aggregate by38 (17) and certain baleen whales by 80 to 90(19) Many of these declines have been termedecological extinctionsmdashalthough the species inquestion are still extant they are no longer suf-ficiently abundant to perform their functionalroles Ecological extinctions are well known interrestrial environments and have been demon-strated to be just as disruptive as species extinc-tions (20) On land we know of the phenomenonof ldquoempty forestsrdquo where ecological extinctions offorest fauna alter tree recruitment reshape plantdispersal and cause population explosions ofsmall mammals (1 20 21) We are now observ-ing the proliferation of ldquoempty reefsrdquo ldquoemptyestuariesrdquo and ldquoempty baysrdquo (7 14 22)

Commercial extinction

Species that drop below an abundance level atwhich they can be economically harvested are ex-tinct from a commercial standpoint On land com-mercial extinctions affected species ranging fromchinchilla to bison (23) Cases of commercial ex-tinction are also common in the oceans Gray whaleswere commercially hunted starting in the 1840sBy 1900 their numbers were so depleted thattargeted harvest of this species was no longer re-

gionally tenable (24) Likewise the great whalesin Antarctica were serially hunted to commer-cial extinction (25)Not all species however are so ldquoluckyrdquo as to

have human harvesters desist when they becomeextremely rare Demand and prices for certainhighly prized marine wildlife can continue to in-crease as these animals become less abundantmdashaphenomenon termed the anthropogenic Alleeeffect (26) Individual bluefin tuna can sell forgtUS$100000 rare sea cucumbers gtUS$400kgand high-quality shark fins for gtUS$100kg Suchspecies are the rhinos of the oceanmdashthey maynever be too rare to be hunted

Differential vulnerability to defaunation

Are certain marine animals more at risk thanothers to defaunation There has been consider-able attention given to harvester effects on largemarine animals (27) Selective declines of large-bodied animals appear to be evident in certaincontexts (28 29) As a result of such pressuresturtles whales sharks andmany large fishes arenow ecologically extinct inmany ecosystems andthe size spectra (abundancendashbody mass relation-ships) of many communities have changed consid-erably (7 30 31) Marine defaunation howeverhas not caused many global extinctions of large-bodied speciesMost large-bodiedmarine animalspecies still exist somewhere in the ocean Bycontrast on land we have observed the extinc-tion of numerous large terrestrial species and aprofound restructuring of the size distribution ofland-animal species assemblages Themean bodymass for the list of surviving terrestrial mammal

species for example is significantly smaller thanthe bodymass of terrestrial mammal species thatlived during the Pleistocene (1 32) Such effectshowever are not evident formarinemammals (8)(fig S2) Recent reviews have drawn attention tothe fact that humans can also intensely and ef-fectively deplete populations of smaller marineanimals (29 33) These observations have inspireda belated surge in interest in protecting smallforage fishes in the oceansA review of modern marine extinctions and list-

ings of species on the brink of extinction revealsfurther insight into aggregate patterns of differen-tial defaunation risk in the oceans (Fig 2) Seaturtles have the highest proportion of endangeredspecies among commonly recognized groupings ofmarine fauna No modern sea turtle species how-ever have yet gone extinct Pinnipeds and marinemustelids followed very closely by seabirds andshorebirds have experienced the highest propor-tion of species extinctionsMany of themost threat-ened groups of marine animals are those thatdirectly interact with land (and land-based humans)during some portion of their life history (Fig 2) Ter-restrial contactmay also explainwhy diadromousbrackish water fishes are more threatened thanexclusively 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 ldquowinnersrdquo or species that are profiting inAnthropocene oceansMany of thesewinners aresmaller and ldquoweedierrdquo (eg better colonizing andfaster reproducing) speciesMarine invertebratesin particular have often been cited as examples of

1255641-2 16 JANUARY 2015 bull VOL 347 ISSUE 6219 sciencemagorg SCIENCE

Fig 2 Marine defaunation threatThreat from defaunation is portrayed for different groups of marine faunaas chronicled by the IUCNRed List (113)Threat categories include ldquoextinctrdquo (orange) ldquoendangeredrdquo (red IUCNcategories ldquocritically endangeredrdquo + ldquoendangeredrdquo) ldquodata deficientrdquo (light gray) and ldquounreviewedrdquo (dark gray)Groups that contact land during some portion of their life history (green) are distinguished from species that donot (light blue)The total numberof species estimated in each group is listed below the graphSpecies groupingsare coded as follows ST sea turtles PO pinnipeds andmarinemustelids SS seabirds and shorebirds SSL seasnakes and marine lizard CS cetaceans and sirenians DBRF diadromousbrackish ray-finned fishes CFcartilaginous fishesMRF exclusivelymarine ray-finned fishesMImarine invertebrates See furtherdetails in (8)

RESEARCH | REVIEW

species that are succeeding in the face of intensemarine defaunation lobster proliferated as pred-atory groundfish declined (34) prawns increasedand replaced the dominance of finfish in land-ings (35) and urchin populations exploded in theabsence of their predators and competitors (36)Numerousmid-level predators also appear to ben-efit from the loss of top predators [eg small sharksand rays (37)]mdasha phenomenon analogous tomeso-predator release observed in terrestrial spheres(38) The status held by some of these defaunationwinners in the oceansmay however be ephemeralMany of the marine species that have initiallyflourished as a result of defaunation have them-selves become targets forharvest by prey-switchinghumans 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 ecosystemssuggest that coastal wildlife habitats have beenmore influenced than deep-water or pelagic ecosys-tems (40) The vulnerability of coastal areas pre-sumably results fromease of access to coastal zonesThis relationship between access and defaunationrisk manifests itself also at smaller spatial scaleswith populations ofmarinewildlife closest to tradenetworks and human settlements appearing oftento bemore heavily defaunated (41 42) The relativeinsulation that animal populations in regions likethe deep oceans presently experience howevermay be short-livedbecausedepletions of shallow-water marine resources and the developmentof new technologies have created both the ca-pacity and incentive to fish mine and drill oilin some of the deepest parts of the sea (28 43)Coral reefs in particular have consistently

been highlighted asmarine ecosystems of special

concern to defaunation Coral reefs have beenexposed to a wide range of impacts and distur-bances including sedimentation and pollutionthermal stress disease destructive fishing andcoastal development (44 45) Such stressors nega-tively influence both corals and the millions ofspecies that live within and depend upon reefs(46) Risk however is not uniform even across areefscape Shallow backreef pools for exampleroutinely overheat and consequently corals inthese parts of the reef aremore resistant to oceanwarming (47) Environmentally heterogeneousareas may in fact act as important natural fac-tories of adaptation that will buffer against sometypes of marine defaunation

Effects of marine defaunation

Extended consequences ofmarine defaunation

Marine defaunation has had far-reaching effectson ocean ecosystems Depletions of a wide rangeof ecologically important marine fauna such ascod sea otters great whales and sharks havetriggered cascading effects that propagate acrossmarine systems (37 48ndash51) Operating in the op-posite direction from trophic cascades are changesthat travel from the bottom to the top of foodchains as a result of the declining abundance oflowerndashtrophic level organisms (52) Depletions offauna such as anchovies sardines and krill causereductions in food for higher-trophic level animalssuch 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 onmarine

ecosystems also occur beyond the bounds of thesetop-down or bottom-up effects Defaunation canreduce cross-system connectivity (54 55) decreaseecosystem stability (56) and alter patterns of bio-geochemical cycling (57) The ill effects of food

webdisarticulation can be further amplifiedwhenthey occur in association with other marine dis-turbances For example mass releases of dis-carded plant fertilizers into marine ecosystemsfromwhich defaunation has eliminated importantconsumers can create ldquoproductivity explosionsrdquo byfueling overgrowth of microbes and algae thatfail to be routed into food webs (58 59)The selective force of human predation has

also been sufficiently strong and protracted soas to have altered the evolutionary trajectory ofnumerous species of harvested marine fauna(60) Harvest has driven many marine animalspecies to become smaller and thinner to growmore slowly to be less fecund and to reproduceat smaller sizes (61) There is also evidence thatharvest can reduce the genetic diversity of manymarine animal populations (62) The genetic ef-fects of defaunation represent a loss of adaptivepotential that may impair the resilient capacityof ocean wildlife (63)

Importance of marine defaunationto humans

Marine defaunation is already affecting humanwell-being in numerous ways by imperiling foodsustainability increasing social conflict impair-ing stormprotection and reducing flows of otherecosystem services (64 65) The most conspicu-ous service that marine fauna make to society isthe contribution of their own bodies to globaldiets Marine animals primarily fishes make upa large proportion of global protein intake andthis contribution is especially strong for impov-erished coastal nations (66) According to theUN Food and Agriculture Organization (FAO)40 times more wild animal biomass is harvestedfrom the oceans than from land (67) Declines inthis source of free-range marine food represent amajor 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 cloudformation that appears to be stimulated by coralemissions of dimethylsulphoniopropionate (DMSP)(57 68 69) Another key service given forecastsof increasingly intense weather events and sea-level rise is coastal protection Coral oyster andother living reefs can dissipate up to 97 of thewave energy reaching them thus protecting builtstructures and human lives (70) In some casescorals are more than just perimeter buffers theyalso serve as the living platform upon which en-tire countries (eg the Maldives Kiribati theMarshall Islands) and entire cultures have beenfounded Atoll-living human populations in theseareas depend on the long-term health of theseanimate pedestals to literally hold their livestogether

Outlook and ways forward

Will climate change exacerbatemarine defaunation

The implications of climate change upon marinedefaunation are shaped by ocean physicsMarinespecies live in a vast globally connected fluid

SCIENCE sciencemagorg 16 JANUARY 2015 bull VOL 347 ISSUE 6219 1255641-3

Fig 3 Comparisons of range contractions for select marine and terrestrial faunaTerrestrial (green)and marine cases (blue) include evaluations of geographical range change for 43 North Americanmammals over the last ~200 years (NM) (114) 18 Indian mammals over the last 30 years (IM) (115) 201British birds from ~1970 to 1997 (BB) and 58 British butterflies from ~1976 to 1997 (BF) (116) 12 globallarge pelagic fishes from the 1960s to 2000s (PF) (14) and 327 trawl-surveyed North American marinefish and invertebrates from the 1970s to 2000s (TFI) (A) Percent of species whose ranges havecontractedwith binomial confidence intervals and (B) distribution of percent contraction for those speciesthat have contracted (violin plot) Sample sizes are shown above each data pointwhite 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 capacityand has exhibited a historically robust capabilityto buffer temperature change over daily annualand 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 theoceans may have left many subtidal marine an-imals poorly prepared relative to terrestrial coun-terparts for the temperature increases associatedwith global warming The same logic supportsrelated predictions that terrestrial fauna living inmore thermally stable environmentswill bemorevulnerable to warming than those found in areasof greater temperature variability (72)Ocean warming presents obvious challenges

to polar marine fauna trapped in thermal deadends (73) Tropical marine species are howeveralso highly sensitive to small increases in temper-ature For example coastal crabs on tropicalshores live closer to their upper thermal maximathan do similar temperate species (74) Likewisethe symbiosis of corals and dinoflagellates isfamously sensitive to rapid increases of only 1deg to2degC (75) Even though corals exhibit the capacityfor adaptation (47) coral bleaching events areexpected to be more common and consequentlymore stressful by the end of the century (76) Theeffects of rising ocean temperature extend wellbeyond coral reefs and are predicted to affectboth the adult and juvenile stages of a diverse setof marine species (77) to reshuffle marine com-munity composition (78) and to potentially alterthe overall structure and dynamics of entire ma-rine faunal communities (79)The wide range of other climate change-

associated alterations in seawater chemistryand physicsmdashincluding ocean acidification anoxiaocean circulation shifts changes in stratificationand changes in primary productivitymdashwill fun-damentally influence marine fauna Ocean acid-ification for example makes marine animalshell building more physiologically costly can

diminish animal sensory abilities and can altergrowth trajectories (80 81) Climate change im-pacts on phytoplankton can further accentuatedefaunation risk (82) At the same time thathumans are reducing the abundance of marineforage fish through direct harvest we also maybe indirectly reducing the planktonic food forforage fish and related consumers in manyregions

Mobility and managing defaunation

Many marine animals on average have signifi-cantly larger home ranges as adults [Fig 4 andfigs S3 and S4 (8)] and disperse greater dis-tances as juveniles than their terrestrial counter-parts (13) This wide-ranging behavior of manymarine species complicates the management ofocean wildlife as species often traverse multiplemanagement jurisdictions (83ndash85) On the otherhand the greater mobility of many marine ani-mal species may help them to better follow thevelocity of climate change and to colonize andrecolonize habitats so long as source populationrefuges 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 farbehind advancements made on land with anupper-bound estimate of only about 36 of theworldrsquos oceans now protected (8) (fig S5) Onesource of optimism for slowing marine defauna-tion particularly for mobile species is that themean size of marine protected areas has in-creased greatly in recent years (fig S5) Howevermostmarine protected areas remain smaller (me-dian 45 km2) than the home range size of manymarine animals (Fig 4) Though much is lost inthis type of crude comparison this observationhighlights what may be an important discon-nect between the scales at which wildlife usethe oceans and the scale at which we typicallymanage the oceans

This spatial mismatch is just one of manyreasons why protected areas cannot be the fullsolution for managing defaunation (83) Welearned this lesson arguably too late on landProtected areas can legitimately be viewed assome of our proudest conservation achievementson land (eg Yosemite Serengeti ChitwanNatio-nal Parks) and yet with four times more terres-trial area protected than marine protected areawe have still failed to satisfactorily rein in ter-restrial defaunation (1) (fig S5) The realizationthat more was needed to curb terrestrial defau-nation inspired a wave of effort to do conserva-tion out of the bounds of terrestrial protectedareas (eg conservation easements and corridorprojects) The delayed implementation of thesestrategies has however often relegated terres-trial conservation to operatingmore as a retroac-tive enterprise aimedat restoringdamagedhabitatsand triaging wildlife losses already underway Inthe oceans we are uniquely positioned to pre-emptively manage defaunation We can learnfrom the terrestrial defaunation experience thatprotected areas are valuable tools but that wemust proactively introduce measures to manageour impacts onmarine fauna in the vast majorityof the global oceans that is unprotectedStrategies tomeet these goals include incentive-

based fisheries management policies (89) spa-tially ambitious ecosystem-based managementplans (83) and emerging efforts to preemptivelyzone human activities that affect marine wildlife(90 91) There have been mixed responses amongmarine managers as to whether and how to em-brace these tools but more complete implementa-tion of these strategies will help chart a sustainablefuture for marine wildlife (43 90 91) A secondcomplementary set of goals is to incorporate cli-mate change intomarine protected area schemesto build networks that will provide protection forocean wildlife into the next century (92) Suchbuilt-in climate plans were unavailable and evenunthinkable when many major terrestrial parkswere laid out but data tools and opportunityexist to do this thoughtfully now in the oceans

Habitat degradation The coming threatto marine fauna

Many early extinctions of terrestrial fauna arebelieved to have been heavily influenced by hu-man hunting (2 93) whereas habitat loss ap-pears to be the primary driver of contemporarydefaunation on land (1 11 86 94) By contrastmarine defaunation today remains mainly driv-en by human harvest (95 96) If the trajectory ofterrestrial defaunation is any indicator we shouldanticipate that habitat alteration will ascendin importance as a future driver of marinedefaunationSigns 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 extensivelyhunted are now threatened by noise disruptionoil exploration vessel traffic and entanglementwith moored marine gear (fig S6) (97) Habitat-modifying fishing practices (eg bottom trawling)

1255641-4 16 JANUARY 2015 bull VOL 347 ISSUE 6219 sciencemagorg SCIENCE

Fig 4 Mobility of ter-restrial and marinefauna Because mobil-ity shapes defaunationrisk we compare thesize-standardizedhome range size of arepresentative selec-tion of marine (blue)and terrestrial (green)vertebrates Data arepresented for adultsover a full range ofanimal body sizesplotted on a logarith-mic scale Speciesinclude seabirdsmarine reptiles marinefishes marine mam-mals terrestrial birdsterrestrial reptiles andterrestrial mammals (see details in (8) table S2 and fig S3) Regression lines enclosed by shadedconfidence intervals are plotted for all marine and all terrestrial species The dotted red line demarcatesthe current median size of all marine protected areas (MPAs)

RESEARCH | REVIEW

have affected ~50 million km2 of seafloor (40)Trawlingmay represent just the beginning of ourcapacity to alter marine habitats Developmentof coastal cities where ~40 of the human pop-ulation lives (98) has an insatiable demand forcoastal land Countries like the United ArabEmirates and China have elected to meet thisdemandby ldquoseasteadingrdquomdashconstructing ambitiousnew artificial lands in the ocean (99) Technolog-ical advancement in seafloor mining dredgingoil and gas extraction tidalwave energy gener-ation and marine transport is fueling rapid ex-pansion of these marine industries (43 100)Even farming is increasing in the sea Projectionsnow suggest that in less than 20 years aquacul-ture will provide more fish for human consump-tion thanwild capture fisheries (101) Fish farminglike crop farming can consume or drastically alternatural habitatswhen carried out carelessly (102)Many of these emerging marine developmentactivities are reminiscent of the types of rapidenvironmental change observed on land duringthe industrial revolution that were associated

with pronounced increases in rates of terrestrialdefaunationMarine habitatsmay eventually jointhe ranks of terrestrial frontier areas such asthe American West the Brazilian Amazon andAlaska which were once believed to be imper-vious to development pollution and degradation

Land to sea defaunation connections

The ecologies of marine and terrestrial systemsare dynamically linked Impacts on terrestrialfauna can perturb the ecology of marine fauna(54) and vice versa (103) Furthermore the healthof marine animal populations is interactivelyconnected to the health of terrestrial wildlifepopulationsmdashand to the health of society Peoplein West Africa for example exploit wild terres-trial fauna more heavily in years when marinefauna are in short supply (104) It is not yet clearhow these linkages between marine and terres-trial defaunation will play out at the global levelWill decreasing yields from marine fisheries forexample require that more terrestrial wildlandsbe brought into human service as fields and

pastures tomeet shortfalls of ocean-derived foodsMarine ecosystem managers would do well tobetter incorporate considerations of land-to-seadefaunation connections in decision making

Not all bad news

It is easy to focus on the negative course thatdefaunation has taken in the oceans Humanshave however demonstrated a powerful capac-ity to reverse some of the most severe impactsthat we have had on ocean fauna and manymarinewildlife populations demonstrate immensepotential for resilience (47 105ndash107) The sea otterthe ecological czar of many coastal ecosystemswas thought to be extinct in the early 1900s butwas rediscovered in 1938 protected and hasresumed its key ecological role in large parts ofthe coastal North Pacific and Bering Sea (108)The reef ecosystems of Enewetak and BikiniAtolls present another potent example TheUnited States detonated 66 nuclear explosionsabove and below the water of these coral reefsin the 1940s and 1950s Less than 50 years laterthe coral and reef fish fauna on these reefsrecovered to the point where they were beingdescribed as remarkably healthy (109)There is great reason to worry however that

we are beginning to erode some of the systemicresilience of marine animal communities (110)Atomic attacks on local marine fauna are onething but an unimpeded transition toward anera of global chemical warfare on marine eco-systems (eg ocean acidification anoxia) mayretard or arrest the intrinsic capacity of marinefauna to bounce back from defaunation (75 111)

Conclusions

Onmany levels defaunation in the oceans has todate been less severe than defaunation on landDeveloping this contrast is useful because ourmore advanced terrestrial defaunation experi-ence can serve as a harbinger for the possiblefuture of marine defaunation (3) Humans havehad profoundly deleterious impacts on marineanimal populations but there is still time andthere exist mechanisms to avert the kinds ofdefaunation disasters observed on land Fewmarine extinctions have occurredmany subtidalmarine habitats are today less developed lesspolluted and more wild than their terrestrialcounterparts global body size distributions ofextant marine animal species have been mostlyunchanged in the oceans andmanymarine faunahave not yet experienced range contractions assevere as those observed on landWe are not necessarily doomed to helplessly

recapitulate the defaunation processes observedon land in the oceans intensifying marine hunt-ing until it becomes untenable and then embarkingon an era of large-scale marine habitat modifi-cation However if these actions move forwardin tandem we may finally trigger a wave of ma-rine extinctions of the same intensity as thatobserved on land Efforts to slow climate changerebuild affected animal populations and intelli-gently engage the coming wave of new marinedevelopment activities will all help to change the

SCIENCE sciencemagorg 16 JANUARY 2015 bull VOL 347 ISSUE 6219 1255641-5

Fig 5 Habitat change in the global oceans Trends in six indicators of marine habitat modificationsuggest that habitat changemay become an increasingly important threat tomarine wildlife (A) change inglobal percent cover of coral reef outside of marine protected areas [percent change at each time pointmeasured relative to percent coral cover in 1988 (44)] (B) global change in mangrove area (percentchange each yearmeasured relative tomangrove area in 1980) (117) (C) change in the cumulative numberof marine wind turbines installed worldwide (118) (D) change in the cumulative area of seabed undercontract for mineral extraction in international waters (119) (E) trends in the volume of global containerport traffic (120) and (F) change in the cumulative number of oxygen depleted marine ldquodead zonesrdquo Seedetails and data sources in (8)

RESEARCH | REVIEW

present course of marine defaunation We mustplay catch-up in the realm of marine protectedarea establishment tailoring them to be opera-tional in our changing oceans We must alsocarefully construct marine spatial managementplans for the vast regions in between these areasto help ensure that marine mining energy devel-opment and intensive aquaculture take impor-tant marine wildlife habitats into considerationnot vice versa All of this is a tall order but theoceans remain relatively full of the raw faunalingredients and still contain a sufficient degreeof resilient capacity so that the goal of reversingthe current crisis of marine defaunation remainswithin reach The next several decades will bethose in which we choose the fate of the future ofmarine wildlife

REFERENCES AND NOTES

1 R Dirzo et al Defaunation in the Anthropocene Science345 401ndash406 (2014) doi 101126science1251817pmid 25061202

2 A D Barnosky P L Koch R S Feranec S L WingA B Shabel Assessing the causes of late Pleistoceneextinctions on the continents Science 306 70ndash75 (2004)doi 101126science1101476 pmid 15459379

3 P L Koch A D Barnosky Late Quaternary extinctions Stateof the debate Annu Rev Ecol Evol Syst 37 215ndash250(2006) doi 101146annurevecolsys34011802132415

4 A D Barnosky et al Prelude to the Anthropocene Two newNorth American land mammal ages (NALMAs) AnthropolRev (2014) doi 1011772053019614547433

5 S OrsquoConnor R Ono C Clarkson Pelagic fishing at 42000 yearsbefore the present and the maritime skills of modern humansScience 334 1117ndash1121 (2011) doi 101126science1207703pmid 22116883

6 H K Lotze et al Depletion degradation and recoverypotential of estuaries and coastal seas Science 3121806ndash1809 (2006) doi 101126science1128035pmid 16794081

7 J B C Jackson et al Historical overfishing and the recentcollapse of coastal ecosystems Science 293 629ndash637(2001) doi 101126science1059199 pmid 11474098

8 Materials and methods are available as supplementarymaterials on Science Online

9 IUCN The IUCN Red List of Threatened Species Version20142 (2014) available at wwwiucnredlistorg

10 C Mora D P Tittensor S Adl A G B Simpson B WormHow many species are there on Earth and in the oceanPLOS Biol 9 e1001127 (2011) doi 101371journalpbio1001127 pmid 21886479

11 S L Pimm et al The biodiversity of species and their ratesof extinction distribution and protection Science 3441246752 (2014) doi 101126science1246752 pmid 24876501

12 E Alison Kay S R Palumbi Endemism and evolution inHawaiian marine invertebrates Trends Ecol Evol 2 183ndash186(1987) doi 1010160169-5347(87)90017-6 pmid 21227847

13 B P Kinlan S D Gaines Propagule dispersal in marine andterrestrial environments A community perspective Ecology84 2007ndash2020 (2003) doi 10189001-0622

14 B Worm D P Tittensor Range contraction in large pelagicpredators Proc Natl Acad Sci USA 108 11942ndash11947(2011) doi 101073pnas1102353108 pmid 21693644

15 E Dinerstein et al The Fate of wild tigers Bioscience 57508ndash514 (2007) doi 101641B570608

16 S L Fowler et al Eds Sharks Rays and Chimaeras TheStatus of the Chondrichthyan Fishes Status Survey (IUCNCambridge UK 2005)

17 J A Hutchings C Minto D Ricard J K Baum O P JensenTrends in the abundance of marine fishes Can J Fish AquatSci 67 1205ndash1210 (2010) doi 101139F10-081

18 WWF Living Planet Report (WWF International GlandSwitzerland 2012) httpwwfpandaorglpr

19 A M Springer et al Sequential megafaunal collapse in theNorth Pacific Ocean An ongoing legacy of industrial whalingProc Natl Acad Sci USA 100 12223ndash12228 (2003)doi 101073pnas1635156100 pmid 14526101

20 K H Redford The empty forest Bioscience 42 412ndash422(1992) doi 1023071311860

21 H S Young et al Declines in large wildlife increaselandscape-level prevalence of rodent-borne disease in AfricaProc Natl Acad Sci USA 111 7036ndash7041 (2014)doi 101073pnas1404958111 pmid 24778215

22 D J McCauley et al Positive and negative effects of athreatened parrotfish on reef ecosystems Conserv Biol28 1312ndash1321 (2014) doi 101111cobi12314pmid 25065396

23 J E Jimeacutenez The extirpation and current status of wildchinchillas Chinchilla lanigera and C brevicaudata Biol Conserv77 1ndash6 (1996) doi 1010160006-3207(95)00116-6

24 R R Reeves T D Smith Commercial whaling especially forgray whales Eschrichtius robustus and humpback whalesMegaptera novaeangliae at California and Baja Californiashore stations in the 19th century (1854ndash1899) Mar FishRev 72 1ndash25 (2010)

25 R Hilborn et al State of the worldrsquos fisheries Annu RevEnviron Resour 28 359ndash399 (2003) doi 101146annurevenergy28050302105509

26 F Courchamp et al Rarity value and species extinctionThe anthropogenic Allee effect PLOS Biol 4 e415 (2006)doi 101371journalpbio0040415 pmid 17132047

27 D Pauly V Christensen J Dalsgaard R Froese F Torres JrFishing down marine food webs Science 279 860ndash863(1998) doi 101126science2795352860 pmid 9452385

28 S A Sethi T A Branch R Watson Global fisherydevelopment patterns are driven by profit but not trophiclevel Proc Natl Acad Sci USA 107 12163ndash12167 (2010)doi 101073pnas1003236107 pmid 20566867

29 M L Pinsky O P Jensen D Ricard S R PalumbiUnexpected patterns of fisheries collapse in the worldrsquosoceans Proc Natl Acad Sci USA 108 8317ndash8322 (2011)doi 101073pnas1015313108 pmid 21536889

30 J B C Jackson Ecological extinction and evolution in thebrave new ocean Proc Natl Acad Sci USA 105 (suppl 1)11458ndash11465 (2008) doi 101073pnas0802812105pmid 18695220

31 S Jennings J L Blanchard Fish abundance with no fishingPredictions based on macroecological theory J Anim Ecol73 632ndash642 (2004) doi 101111j0021-8790200400839x

32 S K Lyons F A Smith J H Brown Of mice mastodonsand men Human-mediated extinctions on four continentsEvol Ecol Res 6 339ndash358 (2004)

33 A D Smith et al Impacts of fishing low-trophic level specieson marine ecosystems Science 333 1147ndash1150 (2011)doi 101126science1209395 pmid 21778363

34 R S Steneck J Vavrinec A V Leland Accelerating trophic-level dysfunction in kelp forest ecosystems of the westernNorth Atlantic Ecosystems 7 323ndash332 (2004) doi 101007s10021-004-0240-6

35 B Worm R A Myers Meta-analysis of codndashshrimpinteractions reveals top-down control in oceanic food websEcology 84 162ndash173 (2003) doi 1018900012-9658(2003)084[0162MAOCSI]20CO2

36 D O Duggins C A Simenstad J A Estes Magnification ofsecondary production by kelp detritus in coastal marineecosystems Science 245 170ndash173 (1989) doi 101126science2454914170 pmid 17787876

37 R A Myers J K Baum T D Shepherd S P PowersC H Peterson Cascading effects of the loss of apexpredatory sharks from a coastal ocean Science 3151846ndash1850 (2007) doi 101126science1138657pmid 17395829

38 L R Prugh et al The Rise of the Mesopredator Bioscience59 779ndash791 (2009) doi 101525bio20095999

39 S C Anderson J Mills Flemming R Watson H K LotzeRapid global expansion of invertebrate fisheries Trendsdrivers and ecosystem effects PLOS ONE 6 e14735 (2011)doi 101371journalpone0014735 pmid 21408090

40 B S Halpern et al A global map of human impact on marineecosystems Science 319 948ndash952 (2008) doi 101126science1149345 pmid 18276889

41 D J McCauley et al Conservation at the edges of the worldBiol Conserv 165 139ndash145 (2013) doi 101016jbiocon201305026

42 J E Cinner N A J Graham C Huchery M A MacneilGlobal effects of local human population density and distanceto markets on the condition of coral reef fisheries Conserv Biol27 453ndash458 (2013) doi 101111j1523-1739201201933xpmid 23025334

43 K J Mengerink et al A call for deep-ocean stewardshipScience 344 696ndash698 (2014) doi 101126science1251458pmid 24833377

44 E R Selig K S Casey J F Bruno Temperature-drivencoral decline The role of marine protected areas Glob ChangeBiol 18 1561ndash1570 (2012) doi 101111j1365-2486201202658x

45 J F Bruno E R Selig Regional decline of coral cover in theIndo-Pacific Timing extent and subregional comparisonsPLOS ONE 2 e711 (2007) doi 101371journalpone0000711pmid 17684557

46 C M Roberts et al Marine biodiversity hotspots andconservation priorities for tropical reefs Science 2951280ndash1284 (2002) doi 101126science1067728pmid 11847338

47 S R Palumbi D J Barshis N Traylor-Knowles R A BayMechanisms of reef coral resistance to future climatechange Science 344 895ndash898 (2014) doi 101126science1251336 pmid 24762535

48 J A Estes et al Trophic downgrading of planet EarthScience 333 301ndash306 (2011) doi 101126science1205106pmid 21764740

49 D J McCauley et al Acute effects of removing large fishfrom a near-pristine coral reef Mar Biol 157 2739ndash2750(2010) doi 101007s00227-010-1533-2 pmid 24391253

50 J A Estes Whales Whaling and Ocean Ecosystems (Univ ofCalifornia Press Berkeley CA 2006)

51 J Terborgh J A Estes Trophic Cascades Predators Preyand the Changing Dynamics of Nature (Island PressWashington DC 2013)

52 D J McCauley F Keesing T P Young B F AllanR M Pringle Indirect effects of large herbivores on snakes inan African savanna Ecology 87 2657ndash2663 (2006)doi 1018900012-9658(2006)87[2657IEOLHO]20CO2pmid 17089673

53 P M Cury et al Global seabird response to forage fishdepletionmdashone-third for the birds Science 334 1703ndash1706(2011) doi 101126science1212928 pmid 22194577

54 D J McCauley et al From wing to wing The persistence oflong ecological interaction chains in less-disturbedecosystems Sci Rep 2 409 (2012) doi 101038srep00409

55 D J McCauley et al Assessing the effects of large mobilepredators on ecosystem connectivity Ecol Appl 221711ndash1717 (2012) doi 10189011-16531 pmid 23092009

56 G L Britten et al Predator decline leads to decreasedstability in a coastal fish community Ecol Lett 17 1518ndash1525(2014) doi 101111ele12354

57 J Roman et al Whales as marine ecosystem engineersFront Ecol Environ 12 377ndash385 (2014) doi 101890130220

58 J M Pandolfi et al Ecology Are US coral reefs on theslippery slope to slime Science 307 1725ndash1726 (2005)doi 101126science1104258 pmid 15774744

59 S R Palumbi A R Palumbi The Extreme Life of the Sea(Princeton Univ Press Princeton NJ 2014)

60 S R Palumbi Humans as the worldrsquos greatest evolutionaryforce Science 293 1786ndash1790 (2001) doi 101126science29355361786 pmid 11546863

61 C Joslashrgensen et al Ecology Managing evolving fish stocksScience 318 1247ndash1248 (2007) doi 101126science1148089 pmid 18033868

62 M L Pinsky S R Palumbi Meta-analysis reveals lowergenetic diversity in overfished populations Mol Ecol 2329ndash39 (2014) doi 101111mec12509 pmid 24372754

63 M R Walsh S B Munch S Chiba D O ConoverMaladaptive changes in multiple traits caused by fishingImpediments to population recovery Ecol Lett 9 142ndash148(2006) doi 101111j1461-0248200500858x pmid 16958879

64 B Worm et al Impacts of biodiversity loss on oceanecosystem services Science 314 787ndash790 (2006)doi 101126science1132294 pmid 17082450

65 J S Brashares et al Wildlife decline and social conflictScience 345 376ndash378 (2014) doi 101126science1256734pmid 25061187

66 Fisheries and Aquaculture Department FAO ldquoThe State ofWorld Fisheries and Aquaculture 2012rdquo (FAO Rome 2012)

67 FAO FAOSTAT (2012) available at httpfaostat3faoorgfaostat-gatewaygotohomeE

68 C C Wilmers J A Estes M Edwards K L LaidreB Konar Do trophic cascades affect the storage andflux of atmospheric carbon An analysis of sea otters andkelp forests Front Ecol Environ 10 409ndash415 (2012)doi 101890110176

69 J-B Raina et al DMSP biosynthesis by an animal and itsrole in coral thermal stress response Nature 502 677ndash680(2013) doi 101038nature12677 pmid 24153189

1255641-6 16 JANUARY 2015 bull VOL 347 ISSUE 6219 sciencemagorg SCIENCE

RESEARCH | REVIEW

species that are succeeding in the face of intensemarine defaunation lobster proliferated as pred-atory groundfish declined (34) prawns increasedand replaced the dominance of finfish in land-ings (35) and urchin populations exploded in theabsence of their predators and competitors (36)Numerousmid-level predators also appear to ben-efit from the loss of top predators [eg small sharksand rays (37)]mdasha phenomenon analogous tomeso-predator release observed in terrestrial spheres(38) The status held by some of these defaunationwinners in the oceansmay however be ephemeralMany of the marine species that have initiallyflourished as a result of defaunation have them-selves become targets forharvest by prey-switchinghumans 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 ecosystemssuggest that coastal wildlife habitats have beenmore influenced than deep-water or pelagic ecosys-tems (40) The vulnerability of coastal areas pre-sumably results fromease of access to coastal zonesThis relationship between access and defaunationrisk manifests itself also at smaller spatial scaleswith populations ofmarinewildlife closest to tradenetworks and human settlements appearing oftento bemore heavily defaunated (41 42) The relativeinsulation that animal populations in regions likethe deep oceans presently experience howevermay be short-livedbecausedepletions of shallow-water marine resources and the developmentof new technologies have created both the ca-pacity and incentive to fish mine and drill oilin some of the deepest parts of the sea (28 43)Coral reefs in particular have consistently

been highlighted asmarine ecosystems of special

concern to defaunation Coral reefs have beenexposed to a wide range of impacts and distur-bances including sedimentation and pollutionthermal stress disease destructive fishing andcoastal development (44 45) Such stressors nega-tively influence both corals and the millions ofspecies that live within and depend upon reefs(46) Risk however is not uniform even across areefscape Shallow backreef pools for exampleroutinely overheat and consequently corals inthese parts of the reef aremore resistant to oceanwarming (47) Environmentally heterogeneousareas may in fact act as important natural fac-tories of adaptation that will buffer against sometypes of marine defaunation

Effects of marine defaunation

Extended consequences ofmarine defaunation

Marine defaunation has had far-reaching effectson ocean ecosystems Depletions of a wide rangeof ecologically important marine fauna such ascod sea otters great whales and sharks havetriggered cascading effects that propagate acrossmarine systems (37 48ndash51) Operating in the op-posite direction from trophic cascades are changesthat travel from the bottom to the top of foodchains as a result of the declining abundance oflowerndashtrophic level organisms (52) Depletions offauna such as anchovies sardines and krill causereductions in food for higher-trophic level animalssuch 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 onmarine

ecosystems also occur beyond the bounds of thesetop-down or bottom-up effects Defaunation canreduce cross-system connectivity (54 55) decreaseecosystem stability (56) and alter patterns of bio-geochemical cycling (57) The ill effects of food

webdisarticulation can be further amplifiedwhenthey occur in association with other marine dis-turbances For example mass releases of dis-carded plant fertilizers into marine ecosystemsfromwhich defaunation has eliminated importantconsumers can create ldquoproductivity explosionsrdquo byfueling overgrowth of microbes and algae thatfail to be routed into food webs (58 59)The selective force of human predation has

also been sufficiently strong and protracted soas to have altered the evolutionary trajectory ofnumerous species of harvested marine fauna(60) Harvest has driven many marine animalspecies to become smaller and thinner to growmore slowly to be less fecund and to reproduceat smaller sizes (61) There is also evidence thatharvest can reduce the genetic diversity of manymarine animal populations (62) The genetic ef-fects of defaunation represent a loss of adaptivepotential that may impair the resilient capacityof ocean wildlife (63)

Importance of marine defaunationto humans

Marine defaunation is already affecting humanwell-being in numerous ways by imperiling foodsustainability increasing social conflict impair-ing stormprotection and reducing flows of otherecosystem services (64 65) The most conspicu-ous service that marine fauna make to society isthe contribution of their own bodies to globaldiets Marine animals primarily fishes make upa large proportion of global protein intake andthis contribution is especially strong for impov-erished coastal nations (66) According to theUN Food and Agriculture Organization (FAO)40 times more wild animal biomass is harvestedfrom the oceans than from land (67) Declines inthis source of free-range marine food represent amajor 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 cloudformation that appears to be stimulated by coralemissions of dimethylsulphoniopropionate (DMSP)(57 68 69) Another key service given forecastsof increasingly intense weather events and sea-level rise is coastal protection Coral oyster andother living reefs can dissipate up to 97 of thewave energy reaching them thus protecting builtstructures and human lives (70) In some casescorals are more than just perimeter buffers theyalso serve as the living platform upon which en-tire countries (eg the Maldives Kiribati theMarshall Islands) and entire cultures have beenfounded Atoll-living human populations in theseareas depend on the long-term health of theseanimate pedestals to literally hold their livestogether

Outlook and ways forward

Will climate change exacerbatemarine defaunation

The implications of climate change upon marinedefaunation are shaped by ocean physicsMarinespecies live in a vast globally connected fluid

SCIENCE sciencemagorg 16 JANUARY 2015 bull VOL 347 ISSUE 6219 1255641-3

Fig 3 Comparisons of range contractions for select marine and terrestrial faunaTerrestrial (green)and marine cases (blue) include evaluations of geographical range change for 43 North Americanmammals over the last ~200 years (NM) (114) 18 Indian mammals over the last 30 years (IM) (115) 201British birds from ~1970 to 1997 (BB) and 58 British butterflies from ~1976 to 1997 (BF) (116) 12 globallarge pelagic fishes from the 1960s to 2000s (PF) (14) and 327 trawl-surveyed North American marinefish and invertebrates from the 1970s to 2000s (TFI) (A) Percent of species whose ranges havecontractedwith binomial confidence intervals and (B) distribution of percent contraction for those speciesthat have contracted (violin plot) Sample sizes are shown above each data pointwhite 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 capacityand has exhibited a historically robust capabilityto buffer temperature change over daily annualand 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 theoceans may have left many subtidal marine an-imals poorly prepared relative to terrestrial coun-terparts for the temperature increases associatedwith global warming The same logic supportsrelated predictions that terrestrial fauna living inmore thermally stable environmentswill bemorevulnerable to warming than those found in areasof greater temperature variability (72)Ocean warming presents obvious challenges

to polar marine fauna trapped in thermal deadends (73) Tropical marine species are howeveralso highly sensitive to small increases in temper-ature For example coastal crabs on tropicalshores live closer to their upper thermal maximathan do similar temperate species (74) Likewisethe symbiosis of corals and dinoflagellates isfamously sensitive to rapid increases of only 1deg to2degC (75) Even though corals exhibit the capacityfor adaptation (47) coral bleaching events areexpected to be more common and consequentlymore stressful by the end of the century (76) Theeffects of rising ocean temperature extend wellbeyond coral reefs and are predicted to affectboth the adult and juvenile stages of a diverse setof marine species (77) to reshuffle marine com-munity composition (78) and to potentially alterthe overall structure and dynamics of entire ma-rine faunal communities (79)The wide range of other climate change-

associated alterations in seawater chemistryand physicsmdashincluding ocean acidification anoxiaocean circulation shifts changes in stratificationand changes in primary productivitymdashwill fun-damentally influence marine fauna Ocean acid-ification for example makes marine animalshell building more physiologically costly can

diminish animal sensory abilities and can altergrowth trajectories (80 81) Climate change im-pacts on phytoplankton can further accentuatedefaunation risk (82) At the same time thathumans are reducing the abundance of marineforage fish through direct harvest we also maybe indirectly reducing the planktonic food forforage fish and related consumers in manyregions

Mobility and managing defaunation

Many marine animals on average have signifi-cantly larger home ranges as adults [Fig 4 andfigs S3 and S4 (8)] and disperse greater dis-tances as juveniles than their terrestrial counter-parts (13) This wide-ranging behavior of manymarine species complicates the management ofocean wildlife as species often traverse multiplemanagement jurisdictions (83ndash85) On the otherhand the greater mobility of many marine ani-mal species may help them to better follow thevelocity of climate change and to colonize andrecolonize habitats so long as source populationrefuges 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 farbehind advancements made on land with anupper-bound estimate of only about 36 of theworldrsquos oceans now protected (8) (fig S5) Onesource of optimism for slowing marine defauna-tion particularly for mobile species is that themean size of marine protected areas has in-creased greatly in recent years (fig S5) Howevermostmarine protected areas remain smaller (me-dian 45 km2) than the home range size of manymarine animals (Fig 4) Though much is lost inthis type of crude comparison this observationhighlights what may be an important discon-nect between the scales at which wildlife usethe oceans and the scale at which we typicallymanage the oceans

This spatial mismatch is just one of manyreasons why protected areas cannot be the fullsolution for managing defaunation (83) Welearned this lesson arguably too late on landProtected areas can legitimately be viewed assome of our proudest conservation achievementson land (eg Yosemite Serengeti ChitwanNatio-nal Parks) and yet with four times more terres-trial area protected than marine protected areawe have still failed to satisfactorily rein in ter-restrial defaunation (1) (fig S5) The realizationthat more was needed to curb terrestrial defau-nation inspired a wave of effort to do conserva-tion out of the bounds of terrestrial protectedareas (eg conservation easements and corridorprojects) The delayed implementation of thesestrategies has however often relegated terres-trial conservation to operatingmore as a retroac-tive enterprise aimedat restoringdamagedhabitatsand triaging wildlife losses already underway Inthe oceans we are uniquely positioned to pre-emptively manage defaunation We can learnfrom the terrestrial defaunation experience thatprotected areas are valuable tools but that wemust proactively introduce measures to manageour impacts onmarine fauna in the vast majorityof the global oceans that is unprotectedStrategies tomeet these goals include incentive-

based fisheries management policies (89) spa-tially ambitious ecosystem-based managementplans (83) and emerging efforts to preemptivelyzone human activities that affect marine wildlife(90 91) There have been mixed responses amongmarine managers as to whether and how to em-brace these tools but more complete implementa-tion of these strategies will help chart a sustainablefuture for marine wildlife (43 90 91) A secondcomplementary set of goals is to incorporate cli-mate change intomarine protected area schemesto build networks that will provide protection forocean wildlife into the next century (92) Suchbuilt-in climate plans were unavailable and evenunthinkable when many major terrestrial parkswere laid out but data tools and opportunityexist to do this thoughtfully now in the oceans

Habitat degradation The coming threatto marine fauna

Many early extinctions of terrestrial fauna arebelieved to have been heavily influenced by hu-man hunting (2 93) whereas habitat loss ap-pears to be the primary driver of contemporarydefaunation on land (1 11 86 94) By contrastmarine defaunation today remains mainly driv-en by human harvest (95 96) If the trajectory ofterrestrial defaunation is any indicator we shouldanticipate that habitat alteration will ascendin importance as a future driver of marinedefaunationSigns 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 extensivelyhunted are now threatened by noise disruptionoil exploration vessel traffic and entanglementwith moored marine gear (fig S6) (97) Habitat-modifying fishing practices (eg bottom trawling)

1255641-4 16 JANUARY 2015 bull VOL 347 ISSUE 6219 sciencemagorg SCIENCE

Fig 4 Mobility of ter-restrial and marinefauna Because mobil-ity shapes defaunationrisk we compare thesize-standardizedhome range size of arepresentative selec-tion of marine (blue)and terrestrial (green)vertebrates Data arepresented for adultsover a full range ofanimal body sizesplotted on a logarith-mic scale Speciesinclude seabirdsmarine reptiles marinefishes marine mam-mals terrestrial birdsterrestrial reptiles andterrestrial mammals (see details in (8) table S2 and fig S3) Regression lines enclosed by shadedconfidence intervals are plotted for all marine and all terrestrial species The dotted red line demarcatesthe current median size of all marine protected areas (MPAs)

RESEARCH | REVIEW

have affected ~50 million km2 of seafloor (40)Trawlingmay represent just the beginning of ourcapacity to alter marine habitats Developmentof coastal cities where ~40 of the human pop-ulation lives (98) has an insatiable demand forcoastal land Countries like the United ArabEmirates and China have elected to meet thisdemandby ldquoseasteadingrdquomdashconstructing ambitiousnew artificial lands in the ocean (99) Technolog-ical advancement in seafloor mining dredgingoil and gas extraction tidalwave energy gener-ation and marine transport is fueling rapid ex-pansion of these marine industries (43 100)Even farming is increasing in the sea Projectionsnow suggest that in less than 20 years aquacul-ture will provide more fish for human consump-tion thanwild capture fisheries (101) Fish farminglike crop farming can consume or drastically alternatural habitatswhen carried out carelessly (102)Many of these emerging marine developmentactivities are reminiscent of the types of rapidenvironmental change observed on land duringthe industrial revolution that were associated

with pronounced increases in rates of terrestrialdefaunationMarine habitatsmay eventually jointhe ranks of terrestrial frontier areas such asthe American West the Brazilian Amazon andAlaska which were once believed to be imper-vious to development pollution and degradation

Land to sea defaunation connections

The ecologies of marine and terrestrial systemsare dynamically linked Impacts on terrestrialfauna can perturb the ecology of marine fauna(54) and vice versa (103) Furthermore the healthof marine animal populations is interactivelyconnected to the health of terrestrial wildlifepopulationsmdashand to the health of society Peoplein West Africa for example exploit wild terres-trial fauna more heavily in years when marinefauna are in short supply (104) It is not yet clearhow these linkages between marine and terres-trial defaunation will play out at the global levelWill decreasing yields from marine fisheries forexample require that more terrestrial wildlandsbe brought into human service as fields and

pastures tomeet shortfalls of ocean-derived foodsMarine ecosystem managers would do well tobetter incorporate considerations of land-to-seadefaunation connections in decision making

Not all bad news

It is easy to focus on the negative course thatdefaunation has taken in the oceans Humanshave however demonstrated a powerful capac-ity to reverse some of the most severe impactsthat we have had on ocean fauna and manymarinewildlife populations demonstrate immensepotential for resilience (47 105ndash107) The sea otterthe ecological czar of many coastal ecosystemswas thought to be extinct in the early 1900s butwas rediscovered in 1938 protected and hasresumed its key ecological role in large parts ofthe coastal North Pacific and Bering Sea (108)The reef ecosystems of Enewetak and BikiniAtolls present another potent example TheUnited States detonated 66 nuclear explosionsabove and below the water of these coral reefsin the 1940s and 1950s Less than 50 years laterthe coral and reef fish fauna on these reefsrecovered to the point where they were beingdescribed as remarkably healthy (109)There is great reason to worry however that

we are beginning to erode some of the systemicresilience of marine animal communities (110)Atomic attacks on local marine fauna are onething but an unimpeded transition toward anera of global chemical warfare on marine eco-systems (eg ocean acidification anoxia) mayretard or arrest the intrinsic capacity of marinefauna to bounce back from defaunation (75 111)

Conclusions

Onmany levels defaunation in the oceans has todate been less severe than defaunation on landDeveloping this contrast is useful because ourmore advanced terrestrial defaunation experi-ence can serve as a harbinger for the possiblefuture of marine defaunation (3) Humans havehad profoundly deleterious impacts on marineanimal populations but there is still time andthere exist mechanisms to avert the kinds ofdefaunation disasters observed on land Fewmarine extinctions have occurredmany subtidalmarine habitats are today less developed lesspolluted and more wild than their terrestrialcounterparts global body size distributions ofextant marine animal species have been mostlyunchanged in the oceans andmanymarine faunahave not yet experienced range contractions assevere as those observed on landWe are not necessarily doomed to helplessly

recapitulate the defaunation processes observedon land in the oceans intensifying marine hunt-ing until it becomes untenable and then embarkingon an era of large-scale marine habitat modifi-cation However if these actions move forwardin tandem we may finally trigger a wave of ma-rine extinctions of the same intensity as thatobserved on land Efforts to slow climate changerebuild affected animal populations and intelli-gently engage the coming wave of new marinedevelopment activities will all help to change the

SCIENCE sciencemagorg 16 JANUARY 2015 bull VOL 347 ISSUE 6219 1255641-5

Fig 5 Habitat change in the global oceans Trends in six indicators of marine habitat modificationsuggest that habitat changemay become an increasingly important threat tomarine wildlife (A) change inglobal percent cover of coral reef outside of marine protected areas [percent change at each time pointmeasured relative to percent coral cover in 1988 (44)] (B) global change in mangrove area (percentchange each yearmeasured relative tomangrove area in 1980) (117) (C) change in the cumulative numberof marine wind turbines installed worldwide (118) (D) change in the cumulative area of seabed undercontract for mineral extraction in international waters (119) (E) trends in the volume of global containerport traffic (120) and (F) change in the cumulative number of oxygen depleted marine ldquodead zonesrdquo Seedetails and data sources in (8)

RESEARCH | REVIEW

present course of marine defaunation We mustplay catch-up in the realm of marine protectedarea establishment tailoring them to be opera-tional in our changing oceans We must alsocarefully construct marine spatial managementplans for the vast regions in between these areasto help ensure that marine mining energy devel-opment and intensive aquaculture take impor-tant marine wildlife habitats into considerationnot vice versa All of this is a tall order but theoceans remain relatively full of the raw faunalingredients and still contain a sufficient degreeof resilient capacity so that the goal of reversingthe current crisis of marine defaunation remainswithin reach The next several decades will bethose in which we choose the fate of the future ofmarine wildlife

REFERENCES AND NOTES

1 R Dirzo et al Defaunation in the Anthropocene Science345 401ndash406 (2014) doi 101126science1251817pmid 25061202

2 A D Barnosky P L Koch R S Feranec S L WingA B Shabel Assessing the causes of late Pleistoceneextinctions on the continents Science 306 70ndash75 (2004)doi 101126science1101476 pmid 15459379

3 P L Koch A D Barnosky Late Quaternary extinctions Stateof the debate Annu Rev Ecol Evol Syst 37 215ndash250(2006) doi 101146annurevecolsys34011802132415

4 A D Barnosky et al Prelude to the Anthropocene Two newNorth American land mammal ages (NALMAs) AnthropolRev (2014) doi 1011772053019614547433

5 S OrsquoConnor R Ono C Clarkson Pelagic fishing at 42000 yearsbefore the present and the maritime skills of modern humansScience 334 1117ndash1121 (2011) doi 101126science1207703pmid 22116883

6 H K Lotze et al Depletion degradation and recoverypotential of estuaries and coastal seas Science 3121806ndash1809 (2006) doi 101126science1128035pmid 16794081

7 J B C Jackson et al Historical overfishing and the recentcollapse of coastal ecosystems Science 293 629ndash637(2001) doi 101126science1059199 pmid 11474098

8 Materials and methods are available as supplementarymaterials on Science Online

9 IUCN The IUCN Red List of Threatened Species Version20142 (2014) available at wwwiucnredlistorg

10 C Mora D P Tittensor S Adl A G B Simpson B WormHow many species are there on Earth and in the oceanPLOS Biol 9 e1001127 (2011) doi 101371journalpbio1001127 pmid 21886479

11 S L Pimm et al The biodiversity of species and their ratesof extinction distribution and protection Science 3441246752 (2014) doi 101126science1246752 pmid 24876501

12 E Alison Kay S R Palumbi Endemism and evolution inHawaiian marine invertebrates Trends Ecol Evol 2 183ndash186(1987) doi 1010160169-5347(87)90017-6 pmid 21227847

13 B P Kinlan S D Gaines Propagule dispersal in marine andterrestrial environments A community perspective Ecology84 2007ndash2020 (2003) doi 10189001-0622

14 B Worm D P Tittensor Range contraction in large pelagicpredators Proc Natl Acad Sci USA 108 11942ndash11947(2011) doi 101073pnas1102353108 pmid 21693644

15 E Dinerstein et al The Fate of wild tigers Bioscience 57508ndash514 (2007) doi 101641B570608

16 S L Fowler et al Eds Sharks Rays and Chimaeras TheStatus of the Chondrichthyan Fishes Status Survey (IUCNCambridge UK 2005)

17 J A Hutchings C Minto D Ricard J K Baum O P JensenTrends in the abundance of marine fishes Can J Fish AquatSci 67 1205ndash1210 (2010) doi 101139F10-081

18 WWF Living Planet Report (WWF International GlandSwitzerland 2012) httpwwfpandaorglpr

19 A M Springer et al Sequential megafaunal collapse in theNorth Pacific Ocean An ongoing legacy of industrial whalingProc Natl Acad Sci USA 100 12223ndash12228 (2003)doi 101073pnas1635156100 pmid 14526101

20 K H Redford The empty forest Bioscience 42 412ndash422(1992) doi 1023071311860

21 H S Young et al Declines in large wildlife increaselandscape-level prevalence of rodent-borne disease in AfricaProc Natl Acad Sci USA 111 7036ndash7041 (2014)doi 101073pnas1404958111 pmid 24778215

22 D J McCauley et al Positive and negative effects of athreatened parrotfish on reef ecosystems Conserv Biol28 1312ndash1321 (2014) doi 101111cobi12314pmid 25065396

23 J E Jimeacutenez The extirpation and current status of wildchinchillas Chinchilla lanigera and C brevicaudata Biol Conserv77 1ndash6 (1996) doi 1010160006-3207(95)00116-6

24 R R Reeves T D Smith Commercial whaling especially forgray whales Eschrichtius robustus and humpback whalesMegaptera novaeangliae at California and Baja Californiashore stations in the 19th century (1854ndash1899) Mar FishRev 72 1ndash25 (2010)

25 R Hilborn et al State of the worldrsquos fisheries Annu RevEnviron Resour 28 359ndash399 (2003) doi 101146annurevenergy28050302105509

26 F Courchamp et al Rarity value and species extinctionThe anthropogenic Allee effect PLOS Biol 4 e415 (2006)doi 101371journalpbio0040415 pmid 17132047

27 D Pauly V Christensen J Dalsgaard R Froese F Torres JrFishing down marine food webs Science 279 860ndash863(1998) doi 101126science2795352860 pmid 9452385

28 S A Sethi T A Branch R Watson Global fisherydevelopment patterns are driven by profit but not trophiclevel Proc Natl Acad Sci USA 107 12163ndash12167 (2010)doi 101073pnas1003236107 pmid 20566867

29 M L Pinsky O P Jensen D Ricard S R PalumbiUnexpected patterns of fisheries collapse in the worldrsquosoceans Proc Natl Acad Sci USA 108 8317ndash8322 (2011)doi 101073pnas1015313108 pmid 21536889

30 J B C Jackson Ecological extinction and evolution in thebrave new ocean Proc Natl Acad Sci USA 105 (suppl 1)11458ndash11465 (2008) doi 101073pnas0802812105pmid 18695220

31 S Jennings J L Blanchard Fish abundance with no fishingPredictions based on macroecological theory J Anim Ecol73 632ndash642 (2004) doi 101111j0021-8790200400839x

32 S K Lyons F A Smith J H Brown Of mice mastodonsand men Human-mediated extinctions on four continentsEvol Ecol Res 6 339ndash358 (2004)

33 A D Smith et al Impacts of fishing low-trophic level specieson marine ecosystems Science 333 1147ndash1150 (2011)doi 101126science1209395 pmid 21778363

34 R S Steneck J Vavrinec A V Leland Accelerating trophic-level dysfunction in kelp forest ecosystems of the westernNorth Atlantic Ecosystems 7 323ndash332 (2004) doi 101007s10021-004-0240-6

35 B Worm R A Myers Meta-analysis of codndashshrimpinteractions reveals top-down control in oceanic food websEcology 84 162ndash173 (2003) doi 1018900012-9658(2003)084[0162MAOCSI]20CO2

36 D O Duggins C A Simenstad J A Estes Magnification ofsecondary production by kelp detritus in coastal marineecosystems Science 245 170ndash173 (1989) doi 101126science2454914170 pmid 17787876

37 R A Myers J K Baum T D Shepherd S P PowersC H Peterson Cascading effects of the loss of apexpredatory sharks from a coastal ocean Science 3151846ndash1850 (2007) doi 101126science1138657pmid 17395829

38 L R Prugh et al The Rise of the Mesopredator Bioscience59 779ndash791 (2009) doi 101525bio20095999

39 S C Anderson J Mills Flemming R Watson H K LotzeRapid global expansion of invertebrate fisheries Trendsdrivers and ecosystem effects PLOS ONE 6 e14735 (2011)doi 101371journalpone0014735 pmid 21408090

40 B S Halpern et al A global map of human impact on marineecosystems Science 319 948ndash952 (2008) doi 101126science1149345 pmid 18276889

41 D J McCauley et al Conservation at the edges of the worldBiol Conserv 165 139ndash145 (2013) doi 101016jbiocon201305026

42 J E Cinner N A J Graham C Huchery M A MacneilGlobal effects of local human population density and distanceto markets on the condition of coral reef fisheries Conserv Biol27 453ndash458 (2013) doi 101111j1523-1739201201933xpmid 23025334

43 K J Mengerink et al A call for deep-ocean stewardshipScience 344 696ndash698 (2014) doi 101126science1251458pmid 24833377

44 E R Selig K S Casey J F Bruno Temperature-drivencoral decline The role of marine protected areas Glob ChangeBiol 18 1561ndash1570 (2012) doi 101111j1365-2486201202658x

45 J F Bruno E R Selig Regional decline of coral cover in theIndo-Pacific Timing extent and subregional comparisonsPLOS ONE 2 e711 (2007) doi 101371journalpone0000711pmid 17684557

46 C M Roberts et al Marine biodiversity hotspots andconservation priorities for tropical reefs Science 2951280ndash1284 (2002) doi 101126science1067728pmid 11847338

47 S R Palumbi D J Barshis N Traylor-Knowles R A BayMechanisms of reef coral resistance to future climatechange Science 344 895ndash898 (2014) doi 101126science1251336 pmid 24762535

48 J A Estes et al Trophic downgrading of planet EarthScience 333 301ndash306 (2011) doi 101126science1205106pmid 21764740

49 D J McCauley et al Acute effects of removing large fishfrom a near-pristine coral reef Mar Biol 157 2739ndash2750(2010) doi 101007s00227-010-1533-2 pmid 24391253

50 J A Estes Whales Whaling and Ocean Ecosystems (Univ ofCalifornia Press Berkeley CA 2006)

51 J Terborgh J A Estes Trophic Cascades Predators Preyand the Changing Dynamics of Nature (Island PressWashington DC 2013)

52 D J McCauley F Keesing T P Young B F AllanR M Pringle Indirect effects of large herbivores on snakes inan African savanna Ecology 87 2657ndash2663 (2006)doi 1018900012-9658(2006)87[2657IEOLHO]20CO2pmid 17089673

53 P M Cury et al Global seabird response to forage fishdepletionmdashone-third for the birds Science 334 1703ndash1706(2011) doi 101126science1212928 pmid 22194577

54 D J McCauley et al From wing to wing The persistence oflong ecological interaction chains in less-disturbedecosystems Sci Rep 2 409 (2012) doi 101038srep00409

55 D J McCauley et al Assessing the effects of large mobilepredators on ecosystem connectivity Ecol Appl 221711ndash1717 (2012) doi 10189011-16531 pmid 23092009

56 G L Britten et al Predator decline leads to decreasedstability in a coastal fish community Ecol Lett 17 1518ndash1525(2014) doi 101111ele12354

57 J Roman et al Whales as marine ecosystem engineersFront Ecol Environ 12 377ndash385 (2014) doi 101890130220

58 J M Pandolfi et al Ecology Are US coral reefs on theslippery slope to slime Science 307 1725ndash1726 (2005)doi 101126science1104258 pmid 15774744

59 S R Palumbi A R Palumbi The Extreme Life of the Sea(Princeton Univ Press Princeton NJ 2014)

60 S R Palumbi Humans as the worldrsquos greatest evolutionaryforce Science 293 1786ndash1790 (2001) doi 101126science29355361786 pmid 11546863

61 C Joslashrgensen et al Ecology Managing evolving fish stocksScience 318 1247ndash1248 (2007) doi 101126science1148089 pmid 18033868

62 M L Pinsky S R Palumbi Meta-analysis reveals lowergenetic diversity in overfished populations Mol Ecol 2329ndash39 (2014) doi 101111mec12509 pmid 24372754

63 M R Walsh S B Munch S Chiba D O ConoverMaladaptive changes in multiple traits caused by fishingImpediments to population recovery Ecol Lett 9 142ndash148(2006) doi 101111j1461-0248200500858x pmid 16958879

64 B Worm et al Impacts of biodiversity loss on oceanecosystem services Science 314 787ndash790 (2006)doi 101126science1132294 pmid 17082450

65 J S Brashares et al Wildlife decline and social conflictScience 345 376ndash378 (2014) doi 101126science1256734pmid 25061187

66 Fisheries and Aquaculture Department FAO ldquoThe State ofWorld Fisheries and Aquaculture 2012rdquo (FAO Rome 2012)

67 FAO FAOSTAT (2012) available at httpfaostat3faoorgfaostat-gatewaygotohomeE

68 C C Wilmers J A Estes M Edwards K L LaidreB Konar Do trophic cascades affect the storage andflux of atmospheric carbon An analysis of sea otters andkelp forests Front Ecol Environ 10 409ndash415 (2012)doi 101890110176

69 J-B Raina et al DMSP biosynthesis by an animal and itsrole in coral thermal stress response Nature 502 677ndash680(2013) doi 101038nature12677 pmid 24153189

1255641-6 16 JANUARY 2015 bull VOL 347 ISSUE 6219 sciencemagorg SCIENCE

RESEARCH | REVIEW

medium that has immense heat-storage capacityand has exhibited a historically robust capabilityto buffer temperature change over daily annualand 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 theoceans may have left many subtidal marine an-imals poorly prepared relative to terrestrial coun-terparts for the temperature increases associatedwith global warming The same logic supportsrelated predictions that terrestrial fauna living inmore thermally stable environmentswill bemorevulnerable to warming than those found in areasof greater temperature variability (72)Ocean warming presents obvious challenges

to polar marine fauna trapped in thermal deadends (73) Tropical marine species are howeveralso highly sensitive to small increases in temper-ature For example coastal crabs on tropicalshores live closer to their upper thermal maximathan do similar temperate species (74) Likewisethe symbiosis of corals and dinoflagellates isfamously sensitive to rapid increases of only 1deg to2degC (75) Even though corals exhibit the capacityfor adaptation (47) coral bleaching events areexpected to be more common and consequentlymore stressful by the end of the century (76) Theeffects of rising ocean temperature extend wellbeyond coral reefs and are predicted to affectboth the adult and juvenile stages of a diverse setof marine species (77) to reshuffle marine com-munity composition (78) and to potentially alterthe overall structure and dynamics of entire ma-rine faunal communities (79)The wide range of other climate change-

associated alterations in seawater chemistryand physicsmdashincluding ocean acidification anoxiaocean circulation shifts changes in stratificationand changes in primary productivitymdashwill fun-damentally influence marine fauna Ocean acid-ification for example makes marine animalshell building more physiologically costly can

diminish animal sensory abilities and can altergrowth trajectories (80 81) Climate change im-pacts on phytoplankton can further accentuatedefaunation risk (82) At the same time thathumans are reducing the abundance of marineforage fish through direct harvest we also maybe indirectly reducing the planktonic food forforage fish and related consumers in manyregions

Mobility and managing defaunation

Many marine animals on average have signifi-cantly larger home ranges as adults [Fig 4 andfigs S3 and S4 (8)] and disperse greater dis-tances as juveniles than their terrestrial counter-parts (13) This wide-ranging behavior of manymarine species complicates the management ofocean wildlife as species often traverse multiplemanagement jurisdictions (83ndash85) On the otherhand the greater mobility of many marine ani-mal species may help them to better follow thevelocity of climate change and to colonize andrecolonize habitats so long as source populationrefuges 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 farbehind advancements made on land with anupper-bound estimate of only about 36 of theworldrsquos oceans now protected (8) (fig S5) Onesource of optimism for slowing marine defauna-tion particularly for mobile species is that themean size of marine protected areas has in-creased greatly in recent years (fig S5) Howevermostmarine protected areas remain smaller (me-dian 45 km2) than the home range size of manymarine animals (Fig 4) Though much is lost inthis type of crude comparison this observationhighlights what may be an important discon-nect between the scales at which wildlife usethe oceans and the scale at which we typicallymanage the oceans

This spatial mismatch is just one of manyreasons why protected areas cannot be the fullsolution for managing defaunation (83) Welearned this lesson arguably too late on landProtected areas can legitimately be viewed assome of our proudest conservation achievementson land (eg Yosemite Serengeti ChitwanNatio-nal Parks) and yet with four times more terres-trial area protected than marine protected areawe have still failed to satisfactorily rein in ter-restrial defaunation (1) (fig S5) The realizationthat more was needed to curb terrestrial defau-nation inspired a wave of effort to do conserva-tion out of the bounds of terrestrial protectedareas (eg conservation easements and corridorprojects) The delayed implementation of thesestrategies has however often relegated terres-trial conservation to operatingmore as a retroac-tive enterprise aimedat restoringdamagedhabitatsand triaging wildlife losses already underway Inthe oceans we are uniquely positioned to pre-emptively manage defaunation We can learnfrom the terrestrial defaunation experience thatprotected areas are valuable tools but that wemust proactively introduce measures to manageour impacts onmarine fauna in the vast majorityof the global oceans that is unprotectedStrategies tomeet these goals include incentive-

based fisheries management policies (89) spa-tially ambitious ecosystem-based managementplans (83) and emerging efforts to preemptivelyzone human activities that affect marine wildlife(90 91) There have been mixed responses amongmarine managers as to whether and how to em-brace these tools but more complete implementa-tion of these strategies will help chart a sustainablefuture for marine wildlife (43 90 91) A secondcomplementary set of goals is to incorporate cli-mate change intomarine protected area schemesto build networks that will provide protection forocean wildlife into the next century (92) Suchbuilt-in climate plans were unavailable and evenunthinkable when many major terrestrial parkswere laid out but data tools and opportunityexist to do this thoughtfully now in the oceans

Habitat degradation The coming threatto marine fauna

Many early extinctions of terrestrial fauna arebelieved to have been heavily influenced by hu-man hunting (2 93) whereas habitat loss ap-pears to be the primary driver of contemporarydefaunation on land (1 11 86 94) By contrastmarine defaunation today remains mainly driv-en by human harvest (95 96) If the trajectory ofterrestrial defaunation is any indicator we shouldanticipate that habitat alteration will ascendin importance as a future driver of marinedefaunationSigns 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 extensivelyhunted are now threatened by noise disruptionoil exploration vessel traffic and entanglementwith moored marine gear (fig S6) (97) Habitat-modifying fishing practices (eg bottom trawling)

1255641-4 16 JANUARY 2015 bull VOL 347 ISSUE 6219 sciencemagorg SCIENCE

Fig 4 Mobility of ter-restrial and marinefauna Because mobil-ity shapes defaunationrisk we compare thesize-standardizedhome range size of arepresentative selec-tion of marine (blue)and terrestrial (green)vertebrates Data arepresented for adultsover a full range ofanimal body sizesplotted on a logarith-mic scale Speciesinclude seabirdsmarine reptiles marinefishes marine mam-mals terrestrial birdsterrestrial reptiles andterrestrial mammals (see details in (8) table S2 and fig S3) Regression lines enclosed by shadedconfidence intervals are plotted for all marine and all terrestrial species The dotted red line demarcatesthe current median size of all marine protected areas (MPAs)

RESEARCH | REVIEW

have affected ~50 million km2 of seafloor (40)Trawlingmay represent just the beginning of ourcapacity to alter marine habitats Developmentof coastal cities where ~40 of the human pop-ulation lives (98) has an insatiable demand forcoastal land Countries like the United ArabEmirates and China have elected to meet thisdemandby ldquoseasteadingrdquomdashconstructing ambitiousnew artificial lands in the ocean (99) Technolog-ical advancement in seafloor mining dredgingoil and gas extraction tidalwave energy gener-ation and marine transport is fueling rapid ex-pansion of these marine industries (43 100)Even farming is increasing in the sea Projectionsnow suggest that in less than 20 years aquacul-ture will provide more fish for human consump-tion thanwild capture fisheries (101) Fish farminglike crop farming can consume or drastically alternatural habitatswhen carried out carelessly (102)Many of these emerging marine developmentactivities are reminiscent of the types of rapidenvironmental change observed on land duringthe industrial revolution that were associated

with pronounced increases in rates of terrestrialdefaunationMarine habitatsmay eventually jointhe ranks of terrestrial frontier areas such asthe American West the Brazilian Amazon andAlaska which were once believed to be imper-vious to development pollution and degradation

Land to sea defaunation connections

The ecologies of marine and terrestrial systemsare dynamically linked Impacts on terrestrialfauna can perturb the ecology of marine fauna(54) and vice versa (103) Furthermore the healthof marine animal populations is interactivelyconnected to the health of terrestrial wildlifepopulationsmdashand to the health of society Peoplein West Africa for example exploit wild terres-trial fauna more heavily in years when marinefauna are in short supply (104) It is not yet clearhow these linkages between marine and terres-trial defaunation will play out at the global levelWill decreasing yields from marine fisheries forexample require that more terrestrial wildlandsbe brought into human service as fields and

pastures tomeet shortfalls of ocean-derived foodsMarine ecosystem managers would do well tobetter incorporate considerations of land-to-seadefaunation connections in decision making

Not all bad news

It is easy to focus on the negative course thatdefaunation has taken in the oceans Humanshave however demonstrated a powerful capac-ity to reverse some of the most severe impactsthat we have had on ocean fauna and manymarinewildlife populations demonstrate immensepotential for resilience (47 105ndash107) The sea otterthe ecological czar of many coastal ecosystemswas thought to be extinct in the early 1900s butwas rediscovered in 1938 protected and hasresumed its key ecological role in large parts ofthe coastal North Pacific and Bering Sea (108)The reef ecosystems of Enewetak and BikiniAtolls present another potent example TheUnited States detonated 66 nuclear explosionsabove and below the water of these coral reefsin the 1940s and 1950s Less than 50 years laterthe coral and reef fish fauna on these reefsrecovered to the point where they were beingdescribed as remarkably healthy (109)There is great reason to worry however that

we are beginning to erode some of the systemicresilience of marine animal communities (110)Atomic attacks on local marine fauna are onething but an unimpeded transition toward anera of global chemical warfare on marine eco-systems (eg ocean acidification anoxia) mayretard or arrest the intrinsic capacity of marinefauna to bounce back from defaunation (75 111)

Conclusions

Onmany levels defaunation in the oceans has todate been less severe than defaunation on landDeveloping this contrast is useful because ourmore advanced terrestrial defaunation experi-ence can serve as a harbinger for the possiblefuture of marine defaunation (3) Humans havehad profoundly deleterious impacts on marineanimal populations but there is still time andthere exist mechanisms to avert the kinds ofdefaunation disasters observed on land Fewmarine extinctions have occurredmany subtidalmarine habitats are today less developed lesspolluted and more wild than their terrestrialcounterparts global body size distributions ofextant marine animal species have been mostlyunchanged in the oceans andmanymarine faunahave not yet experienced range contractions assevere as those observed on landWe are not necessarily doomed to helplessly

recapitulate the defaunation processes observedon land in the oceans intensifying marine hunt-ing until it becomes untenable and then embarkingon an era of large-scale marine habitat modifi-cation However if these actions move forwardin tandem we may finally trigger a wave of ma-rine extinctions of the same intensity as thatobserved on land Efforts to slow climate changerebuild affected animal populations and intelli-gently engage the coming wave of new marinedevelopment activities will all help to change the

SCIENCE sciencemagorg 16 JANUARY 2015 bull VOL 347 ISSUE 6219 1255641-5

Fig 5 Habitat change in the global oceans Trends in six indicators of marine habitat modificationsuggest that habitat changemay become an increasingly important threat tomarine wildlife (A) change inglobal percent cover of coral reef outside of marine protected areas [percent change at each time pointmeasured relative to percent coral cover in 1988 (44)] (B) global change in mangrove area (percentchange each yearmeasured relative tomangrove area in 1980) (117) (C) change in the cumulative numberof marine wind turbines installed worldwide (118) (D) change in the cumulative area of seabed undercontract for mineral extraction in international waters (119) (E) trends in the volume of global containerport traffic (120) and (F) change in the cumulative number of oxygen depleted marine ldquodead zonesrdquo Seedetails and data sources in (8)

RESEARCH | REVIEW

present course of marine defaunation We mustplay catch-up in the realm of marine protectedarea establishment tailoring them to be opera-tional in our changing oceans We must alsocarefully construct marine spatial managementplans for the vast regions in between these areasto help ensure that marine mining energy devel-opment and intensive aquaculture take impor-tant marine wildlife habitats into considerationnot vice versa All of this is a tall order but theoceans remain relatively full of the raw faunalingredients and still contain a sufficient degreeof resilient capacity so that the goal of reversingthe current crisis of marine defaunation remainswithin reach The next several decades will bethose in which we choose the fate of the future ofmarine wildlife

REFERENCES AND NOTES

1 R Dirzo et al Defaunation in the Anthropocene Science345 401ndash406 (2014) doi 101126science1251817pmid 25061202

2 A D Barnosky P L Koch R S Feranec S L WingA B Shabel Assessing the causes of late Pleistoceneextinctions on the continents Science 306 70ndash75 (2004)doi 101126science1101476 pmid 15459379

3 P L Koch A D Barnosky Late Quaternary extinctions Stateof the debate Annu Rev Ecol Evol Syst 37 215ndash250(2006) doi 101146annurevecolsys34011802132415

4 A D Barnosky et al Prelude to the Anthropocene Two newNorth American land mammal ages (NALMAs) AnthropolRev (2014) doi 1011772053019614547433

5 S OrsquoConnor R Ono C Clarkson Pelagic fishing at 42000 yearsbefore the present and the maritime skills of modern humansScience 334 1117ndash1121 (2011) doi 101126science1207703pmid 22116883

6 H K Lotze et al Depletion degradation and recoverypotential of estuaries and coastal seas Science 3121806ndash1809 (2006) doi 101126science1128035pmid 16794081

7 J B C Jackson et al Historical overfishing and the recentcollapse of coastal ecosystems Science 293 629ndash637(2001) doi 101126science1059199 pmid 11474098

8 Materials and methods are available as supplementarymaterials on Science Online

9 IUCN The IUCN Red List of Threatened Species Version20142 (2014) available at wwwiucnredlistorg

10 C Mora D P Tittensor S Adl A G B Simpson B WormHow many species are there on Earth and in the oceanPLOS Biol 9 e1001127 (2011) doi 101371journalpbio1001127 pmid 21886479

11 S L Pimm et al The biodiversity of species and their ratesof extinction distribution and protection Science 3441246752 (2014) doi 101126science1246752 pmid 24876501

12 E Alison Kay S R Palumbi Endemism and evolution inHawaiian marine invertebrates Trends Ecol Evol 2 183ndash186(1987) doi 1010160169-5347(87)90017-6 pmid 21227847

13 B P Kinlan S D Gaines Propagule dispersal in marine andterrestrial environments A community perspective Ecology84 2007ndash2020 (2003) doi 10189001-0622

14 B Worm D P Tittensor Range contraction in large pelagicpredators Proc Natl Acad Sci USA 108 11942ndash11947(2011) doi 101073pnas1102353108 pmid 21693644

15 E Dinerstein et al The Fate of wild tigers Bioscience 57508ndash514 (2007) doi 101641B570608

16 S L Fowler et al Eds Sharks Rays and Chimaeras TheStatus of the Chondrichthyan Fishes Status Survey (IUCNCambridge UK 2005)

17 J A Hutchings C Minto D Ricard J K Baum O P JensenTrends in the abundance of marine fishes Can J Fish AquatSci 67 1205ndash1210 (2010) doi 101139F10-081

18 WWF Living Planet Report (WWF International GlandSwitzerland 2012) httpwwfpandaorglpr

19 A M Springer et al Sequential megafaunal collapse in theNorth Pacific Ocean An ongoing legacy of industrial whalingProc Natl Acad Sci USA 100 12223ndash12228 (2003)doi 101073pnas1635156100 pmid 14526101

20 K H Redford The empty forest Bioscience 42 412ndash422(1992) doi 1023071311860

21 H S Young et al Declines in large wildlife increaselandscape-level prevalence of rodent-borne disease in AfricaProc Natl Acad Sci USA 111 7036ndash7041 (2014)doi 101073pnas1404958111 pmid 24778215

22 D J McCauley et al Positive and negative effects of athreatened parrotfish on reef ecosystems Conserv Biol28 1312ndash1321 (2014) doi 101111cobi12314pmid 25065396

23 J E Jimeacutenez The extirpation and current status of wildchinchillas Chinchilla lanigera and C brevicaudata Biol Conserv77 1ndash6 (1996) doi 1010160006-3207(95)00116-6

24 R R Reeves T D Smith Commercial whaling especially forgray whales Eschrichtius robustus and humpback whalesMegaptera novaeangliae at California and Baja Californiashore stations in the 19th century (1854ndash1899) Mar FishRev 72 1ndash25 (2010)

25 R Hilborn et al State of the worldrsquos fisheries Annu RevEnviron Resour 28 359ndash399 (2003) doi 101146annurevenergy28050302105509

26 F Courchamp et al Rarity value and species extinctionThe anthropogenic Allee effect PLOS Biol 4 e415 (2006)doi 101371journalpbio0040415 pmid 17132047

27 D Pauly V Christensen J Dalsgaard R Froese F Torres JrFishing down marine food webs Science 279 860ndash863(1998) doi 101126science2795352860 pmid 9452385

28 S A Sethi T A Branch R Watson Global fisherydevelopment patterns are driven by profit but not trophiclevel Proc Natl Acad Sci USA 107 12163ndash12167 (2010)doi 101073pnas1003236107 pmid 20566867

29 M L Pinsky O P Jensen D Ricard S R PalumbiUnexpected patterns of fisheries collapse in the worldrsquosoceans Proc Natl Acad Sci USA 108 8317ndash8322 (2011)doi 101073pnas1015313108 pmid 21536889

30 J B C Jackson Ecological extinction and evolution in thebrave new ocean Proc Natl Acad Sci USA 105 (suppl 1)11458ndash11465 (2008) doi 101073pnas0802812105pmid 18695220

31 S Jennings J L Blanchard Fish abundance with no fishingPredictions based on macroecological theory J Anim Ecol73 632ndash642 (2004) doi 101111j0021-8790200400839x

32 S K Lyons F A Smith J H Brown Of mice mastodonsand men Human-mediated extinctions on four continentsEvol Ecol Res 6 339ndash358 (2004)

33 A D Smith et al Impacts of fishing low-trophic level specieson marine ecosystems Science 333 1147ndash1150 (2011)doi 101126science1209395 pmid 21778363

34 R S Steneck J Vavrinec A V Leland Accelerating trophic-level dysfunction in kelp forest ecosystems of the westernNorth Atlantic Ecosystems 7 323ndash332 (2004) doi 101007s10021-004-0240-6

35 B Worm R A Myers Meta-analysis of codndashshrimpinteractions reveals top-down control in oceanic food websEcology 84 162ndash173 (2003) doi 1018900012-9658(2003)084[0162MAOCSI]20CO2

36 D O Duggins C A Simenstad J A Estes Magnification ofsecondary production by kelp detritus in coastal marineecosystems Science 245 170ndash173 (1989) doi 101126science2454914170 pmid 17787876

37 R A Myers J K Baum T D Shepherd S P PowersC H Peterson Cascading effects of the loss of apexpredatory sharks from a coastal ocean Science 3151846ndash1850 (2007) doi 101126science1138657pmid 17395829

38 L R Prugh et al The Rise of the Mesopredator Bioscience59 779ndash791 (2009) doi 101525bio20095999

39 S C Anderson J Mills Flemming R Watson H K LotzeRapid global expansion of invertebrate fisheries Trendsdrivers and ecosystem effects PLOS ONE 6 e14735 (2011)doi 101371journalpone0014735 pmid 21408090

40 B S Halpern et al A global map of human impact on marineecosystems Science 319 948ndash952 (2008) doi 101126science1149345 pmid 18276889

41 D J McCauley et al Conservation at the edges of the worldBiol Conserv 165 139ndash145 (2013) doi 101016jbiocon201305026

42 J E Cinner N A J Graham C Huchery M A MacneilGlobal effects of local human population density and distanceto markets on the condition of coral reef fisheries Conserv Biol27 453ndash458 (2013) doi 101111j1523-1739201201933xpmid 23025334

43 K J Mengerink et al A call for deep-ocean stewardshipScience 344 696ndash698 (2014) doi 101126science1251458pmid 24833377

44 E R Selig K S Casey J F Bruno Temperature-drivencoral decline The role of marine protected areas Glob ChangeBiol 18 1561ndash1570 (2012) doi 101111j1365-2486201202658x

45 J F Bruno E R Selig Regional decline of coral cover in theIndo-Pacific Timing extent and subregional comparisonsPLOS ONE 2 e711 (2007) doi 101371journalpone0000711pmid 17684557

46 C M Roberts et al Marine biodiversity hotspots andconservation priorities for tropical reefs Science 2951280ndash1284 (2002) doi 101126science1067728pmid 11847338

47 S R Palumbi D J Barshis N Traylor-Knowles R A BayMechanisms of reef coral resistance to future climatechange Science 344 895ndash898 (2014) doi 101126science1251336 pmid 24762535

48 J A Estes et al Trophic downgrading of planet EarthScience 333 301ndash306 (2011) doi 101126science1205106pmid 21764740

49 D J McCauley et al Acute effects of removing large fishfrom a near-pristine coral reef Mar Biol 157 2739ndash2750(2010) doi 101007s00227-010-1533-2 pmid 24391253

50 J A Estes Whales Whaling and Ocean Ecosystems (Univ ofCalifornia Press Berkeley CA 2006)

51 J Terborgh J A Estes Trophic Cascades Predators Preyand the Changing Dynamics of Nature (Island PressWashington DC 2013)

52 D J McCauley F Keesing T P Young B F AllanR M Pringle Indirect effects of large herbivores on snakes inan African savanna Ecology 87 2657ndash2663 (2006)doi 1018900012-9658(2006)87[2657IEOLHO]20CO2pmid 17089673

53 P M Cury et al Global seabird response to forage fishdepletionmdashone-third for the birds Science 334 1703ndash1706(2011) doi 101126science1212928 pmid 22194577

54 D J McCauley et al From wing to wing The persistence oflong ecological interaction chains in less-disturbedecosystems Sci Rep 2 409 (2012) doi 101038srep00409

55 D J McCauley et al Assessing the effects of large mobilepredators on ecosystem connectivity Ecol Appl 221711ndash1717 (2012) doi 10189011-16531 pmid 23092009

56 G L Britten et al Predator decline leads to decreasedstability in a coastal fish community Ecol Lett 17 1518ndash1525(2014) doi 101111ele12354

57 J Roman et al Whales as marine ecosystem engineersFront Ecol Environ 12 377ndash385 (2014) doi 101890130220

58 J M Pandolfi et al Ecology Are US coral reefs on theslippery slope to slime Science 307 1725ndash1726 (2005)doi 101126science1104258 pmid 15774744

59 S R Palumbi A R Palumbi The Extreme Life of the Sea(Princeton Univ Press Princeton NJ 2014)

60 S R Palumbi Humans as the worldrsquos greatest evolutionaryforce Science 293 1786ndash1790 (2001) doi 101126science29355361786 pmid 11546863

61 C Joslashrgensen et al Ecology Managing evolving fish stocksScience 318 1247ndash1248 (2007) doi 101126science1148089 pmid 18033868

62 M L Pinsky S R Palumbi Meta-analysis reveals lowergenetic diversity in overfished populations Mol Ecol 2329ndash39 (2014) doi 101111mec12509 pmid 24372754

63 M R Walsh S B Munch S Chiba D O ConoverMaladaptive changes in multiple traits caused by fishingImpediments to population recovery Ecol Lett 9 142ndash148(2006) doi 101111j1461-0248200500858x pmid 16958879

64 B Worm et al Impacts of biodiversity loss on oceanecosystem services Science 314 787ndash790 (2006)doi 101126science1132294 pmid 17082450

65 J S Brashares et al Wildlife decline and social conflictScience 345 376ndash378 (2014) doi 101126science1256734pmid 25061187

66 Fisheries and Aquaculture Department FAO ldquoThe State ofWorld Fisheries and Aquaculture 2012rdquo (FAO Rome 2012)

67 FAO FAOSTAT (2012) available at httpfaostat3faoorgfaostat-gatewaygotohomeE

68 C C Wilmers J A Estes M Edwards K L LaidreB Konar Do trophic cascades affect the storage andflux of atmospheric carbon An analysis of sea otters andkelp forests Front Ecol Environ 10 409ndash415 (2012)doi 101890110176

69 J-B Raina et al DMSP biosynthesis by an animal and itsrole in coral thermal stress response Nature 502 677ndash680(2013) doi 101038nature12677 pmid 24153189

1255641-6 16 JANUARY 2015 bull VOL 347 ISSUE 6219 sciencemagorg SCIENCE

RESEARCH | REVIEW

have affected ~50 million km2 of seafloor (40)Trawlingmay represent just the beginning of ourcapacity to alter marine habitats Developmentof coastal cities where ~40 of the human pop-ulation lives (98) has an insatiable demand forcoastal land Countries like the United ArabEmirates and China have elected to meet thisdemandby ldquoseasteadingrdquomdashconstructing ambitiousnew artificial lands in the ocean (99) Technolog-ical advancement in seafloor mining dredgingoil and gas extraction tidalwave energy gener-ation and marine transport is fueling rapid ex-pansion of these marine industries (43 100)Even farming is increasing in the sea Projectionsnow suggest that in less than 20 years aquacul-ture will provide more fish for human consump-tion thanwild capture fisheries (101) Fish farminglike crop farming can consume or drastically alternatural habitatswhen carried out carelessly (102)Many of these emerging marine developmentactivities are reminiscent of the types of rapidenvironmental change observed on land duringthe industrial revolution that were associated

with pronounced increases in rates of terrestrialdefaunationMarine habitatsmay eventually jointhe ranks of terrestrial frontier areas such asthe American West the Brazilian Amazon andAlaska which were once believed to be imper-vious to development pollution and degradation

Land to sea defaunation connections

The ecologies of marine and terrestrial systemsare dynamically linked Impacts on terrestrialfauna can perturb the ecology of marine fauna(54) and vice versa (103) Furthermore the healthof marine animal populations is interactivelyconnected to the health of terrestrial wildlifepopulationsmdashand to the health of society Peoplein West Africa for example exploit wild terres-trial fauna more heavily in years when marinefauna are in short supply (104) It is not yet clearhow these linkages between marine and terres-trial defaunation will play out at the global levelWill decreasing yields from marine fisheries forexample require that more terrestrial wildlandsbe brought into human service as fields and

pastures tomeet shortfalls of ocean-derived foodsMarine ecosystem managers would do well tobetter incorporate considerations of land-to-seadefaunation connections in decision making

Not all bad news

It is easy to focus on the negative course thatdefaunation has taken in the oceans Humanshave however demonstrated a powerful capac-ity to reverse some of the most severe impactsthat we have had on ocean fauna and manymarinewildlife populations demonstrate immensepotential for resilience (47 105ndash107) The sea otterthe ecological czar of many coastal ecosystemswas thought to be extinct in the early 1900s butwas rediscovered in 1938 protected and hasresumed its key ecological role in large parts ofthe coastal North Pacific and Bering Sea (108)The reef ecosystems of Enewetak and BikiniAtolls present another potent example TheUnited States detonated 66 nuclear explosionsabove and below the water of these coral reefsin the 1940s and 1950s Less than 50 years laterthe coral and reef fish fauna on these reefsrecovered to the point where they were beingdescribed as remarkably healthy (109)There is great reason to worry however that

we are beginning to erode some of the systemicresilience of marine animal communities (110)Atomic attacks on local marine fauna are onething but an unimpeded transition toward anera of global chemical warfare on marine eco-systems (eg ocean acidification anoxia) mayretard or arrest the intrinsic capacity of marinefauna to bounce back from defaunation (75 111)

Conclusions

Onmany levels defaunation in the oceans has todate been less severe than defaunation on landDeveloping this contrast is useful because ourmore advanced terrestrial defaunation experi-ence can serve as a harbinger for the possiblefuture of marine defaunation (3) Humans havehad profoundly deleterious impacts on marineanimal populations but there is still time andthere exist mechanisms to avert the kinds ofdefaunation disasters observed on land Fewmarine extinctions have occurredmany subtidalmarine habitats are today less developed lesspolluted and more wild than their terrestrialcounterparts global body size distributions ofextant marine animal species have been mostlyunchanged in the oceans andmanymarine faunahave not yet experienced range contractions assevere as those observed on landWe are not necessarily doomed to helplessly

recapitulate the defaunation processes observedon land in the oceans intensifying marine hunt-ing until it becomes untenable and then embarkingon an era of large-scale marine habitat modifi-cation However if these actions move forwardin tandem we may finally trigger a wave of ma-rine extinctions of the same intensity as thatobserved on land Efforts to slow climate changerebuild affected animal populations and intelli-gently engage the coming wave of new marinedevelopment activities will all help to change the

SCIENCE sciencemagorg 16 JANUARY 2015 bull VOL 347 ISSUE 6219 1255641-5

Fig 5 Habitat change in the global oceans Trends in six indicators of marine habitat modificationsuggest that habitat changemay become an increasingly important threat tomarine wildlife (A) change inglobal percent cover of coral reef outside of marine protected areas [percent change at each time pointmeasured relative to percent coral cover in 1988 (44)] (B) global change in mangrove area (percentchange each yearmeasured relative tomangrove area in 1980) (117) (C) change in the cumulative numberof marine wind turbines installed worldwide (118) (D) change in the cumulative area of seabed undercontract for mineral extraction in international waters (119) (E) trends in the volume of global containerport traffic (120) and (F) change in the cumulative number of oxygen depleted marine ldquodead zonesrdquo Seedetails and data sources in (8)

RESEARCH | REVIEW

present course of marine defaunation We mustplay catch-up in the realm of marine protectedarea establishment tailoring them to be opera-tional in our changing oceans We must alsocarefully construct marine spatial managementplans for the vast regions in between these areasto help ensure that marine mining energy devel-opment and intensive aquaculture take impor-tant marine wildlife habitats into considerationnot vice versa All of this is a tall order but theoceans remain relatively full of the raw faunalingredients and still contain a sufficient degreeof resilient capacity so that the goal of reversingthe current crisis of marine defaunation remainswithin reach The next several decades will bethose in which we choose the fate of the future ofmarine wildlife

REFERENCES AND NOTES

1 R Dirzo et al Defaunation in the Anthropocene Science345 401ndash406 (2014) doi 101126science1251817pmid 25061202

2 A D Barnosky P L Koch R S Feranec S L WingA B Shabel Assessing the causes of late Pleistoceneextinctions on the continents Science 306 70ndash75 (2004)doi 101126science1101476 pmid 15459379

3 P L Koch A D Barnosky Late Quaternary extinctions Stateof the debate Annu Rev Ecol Evol Syst 37 215ndash250(2006) doi 101146annurevecolsys34011802132415

4 A D Barnosky et al Prelude to the Anthropocene Two newNorth American land mammal ages (NALMAs) AnthropolRev (2014) doi 1011772053019614547433

5 S OrsquoConnor R Ono C Clarkson Pelagic fishing at 42000 yearsbefore the present and the maritime skills of modern humansScience 334 1117ndash1121 (2011) doi 101126science1207703pmid 22116883

6 H K Lotze et al Depletion degradation and recoverypotential of estuaries and coastal seas Science 3121806ndash1809 (2006) doi 101126science1128035pmid 16794081

7 J B C Jackson et al Historical overfishing and the recentcollapse of coastal ecosystems Science 293 629ndash637(2001) doi 101126science1059199 pmid 11474098

8 Materials and methods are available as supplementarymaterials on Science Online

9 IUCN The IUCN Red List of Threatened Species Version20142 (2014) available at wwwiucnredlistorg

10 C Mora D P Tittensor S Adl A G B Simpson B WormHow many species are there on Earth and in the oceanPLOS Biol 9 e1001127 (2011) doi 101371journalpbio1001127 pmid 21886479

11 S L Pimm et al The biodiversity of species and their ratesof extinction distribution and protection Science 3441246752 (2014) doi 101126science1246752 pmid 24876501

12 E Alison Kay S R Palumbi Endemism and evolution inHawaiian marine invertebrates Trends Ecol Evol 2 183ndash186(1987) doi 1010160169-5347(87)90017-6 pmid 21227847

13 B P Kinlan S D Gaines Propagule dispersal in marine andterrestrial environments A community perspective Ecology84 2007ndash2020 (2003) doi 10189001-0622

14 B Worm D P Tittensor Range contraction in large pelagicpredators Proc Natl Acad Sci USA 108 11942ndash11947(2011) doi 101073pnas1102353108 pmid 21693644

15 E Dinerstein et al The Fate of wild tigers Bioscience 57508ndash514 (2007) doi 101641B570608

16 S L Fowler et al Eds Sharks Rays and Chimaeras TheStatus of the Chondrichthyan Fishes Status Survey (IUCNCambridge UK 2005)

17 J A Hutchings C Minto D Ricard J K Baum O P JensenTrends in the abundance of marine fishes Can J Fish AquatSci 67 1205ndash1210 (2010) doi 101139F10-081

18 WWF Living Planet Report (WWF International GlandSwitzerland 2012) httpwwfpandaorglpr

19 A M Springer et al Sequential megafaunal collapse in theNorth Pacific Ocean An ongoing legacy of industrial whalingProc Natl Acad Sci USA 100 12223ndash12228 (2003)doi 101073pnas1635156100 pmid 14526101

20 K H Redford The empty forest Bioscience 42 412ndash422(1992) doi 1023071311860

21 H S Young et al Declines in large wildlife increaselandscape-level prevalence of rodent-borne disease in AfricaProc Natl Acad Sci USA 111 7036ndash7041 (2014)doi 101073pnas1404958111 pmid 24778215

22 D J McCauley et al Positive and negative effects of athreatened parrotfish on reef ecosystems Conserv Biol28 1312ndash1321 (2014) doi 101111cobi12314pmid 25065396

23 J E Jimeacutenez The extirpation and current status of wildchinchillas Chinchilla lanigera and C brevicaudata Biol Conserv77 1ndash6 (1996) doi 1010160006-3207(95)00116-6

24 R R Reeves T D Smith Commercial whaling especially forgray whales Eschrichtius robustus and humpback whalesMegaptera novaeangliae at California and Baja Californiashore stations in the 19th century (1854ndash1899) Mar FishRev 72 1ndash25 (2010)

25 R Hilborn et al State of the worldrsquos fisheries Annu RevEnviron Resour 28 359ndash399 (2003) doi 101146annurevenergy28050302105509

26 F Courchamp et al Rarity value and species extinctionThe anthropogenic Allee effect PLOS Biol 4 e415 (2006)doi 101371journalpbio0040415 pmid 17132047

27 D Pauly V Christensen J Dalsgaard R Froese F Torres JrFishing down marine food webs Science 279 860ndash863(1998) doi 101126science2795352860 pmid 9452385

28 S A Sethi T A Branch R Watson Global fisherydevelopment patterns are driven by profit but not trophiclevel Proc Natl Acad Sci USA 107 12163ndash12167 (2010)doi 101073pnas1003236107 pmid 20566867

29 M L Pinsky O P Jensen D Ricard S R PalumbiUnexpected patterns of fisheries collapse in the worldrsquosoceans Proc Natl Acad Sci USA 108 8317ndash8322 (2011)doi 101073pnas1015313108 pmid 21536889

30 J B C Jackson Ecological extinction and evolution in thebrave new ocean Proc Natl Acad Sci USA 105 (suppl 1)11458ndash11465 (2008) doi 101073pnas0802812105pmid 18695220

31 S Jennings J L Blanchard Fish abundance with no fishingPredictions based on macroecological theory J Anim Ecol73 632ndash642 (2004) doi 101111j0021-8790200400839x

32 S K Lyons F A Smith J H Brown Of mice mastodonsand men Human-mediated extinctions on four continentsEvol Ecol Res 6 339ndash358 (2004)

33 A D Smith et al Impacts of fishing low-trophic level specieson marine ecosystems Science 333 1147ndash1150 (2011)doi 101126science1209395 pmid 21778363

34 R S Steneck J Vavrinec A V Leland Accelerating trophic-level dysfunction in kelp forest ecosystems of the westernNorth Atlantic Ecosystems 7 323ndash332 (2004) doi 101007s10021-004-0240-6

35 B Worm R A Myers Meta-analysis of codndashshrimpinteractions reveals top-down control in oceanic food websEcology 84 162ndash173 (2003) doi 1018900012-9658(2003)084[0162MAOCSI]20CO2

36 D O Duggins C A Simenstad J A Estes Magnification ofsecondary production by kelp detritus in coastal marineecosystems Science 245 170ndash173 (1989) doi 101126science2454914170 pmid 17787876

37 R A Myers J K Baum T D Shepherd S P PowersC H Peterson Cascading effects of the loss of apexpredatory sharks from a coastal ocean Science 3151846ndash1850 (2007) doi 101126science1138657pmid 17395829

38 L R Prugh et al The Rise of the Mesopredator Bioscience59 779ndash791 (2009) doi 101525bio20095999

39 S C Anderson J Mills Flemming R Watson H K LotzeRapid global expansion of invertebrate fisheries Trendsdrivers and ecosystem effects PLOS ONE 6 e14735 (2011)doi 101371journalpone0014735 pmid 21408090

40 B S Halpern et al A global map of human impact on marineecosystems Science 319 948ndash952 (2008) doi 101126science1149345 pmid 18276889

41 D J McCauley et al Conservation at the edges of the worldBiol Conserv 165 139ndash145 (2013) doi 101016jbiocon201305026

42 J E Cinner N A J Graham C Huchery M A MacneilGlobal effects of local human population density and distanceto markets on the condition of coral reef fisheries Conserv Biol27 453ndash458 (2013) doi 101111j1523-1739201201933xpmid 23025334

43 K J Mengerink et al A call for deep-ocean stewardshipScience 344 696ndash698 (2014) doi 101126science1251458pmid 24833377

44 E R Selig K S Casey J F Bruno Temperature-drivencoral decline The role of marine protected areas Glob ChangeBiol 18 1561ndash1570 (2012) doi 101111j1365-2486201202658x

45 J F Bruno E R Selig Regional decline of coral cover in theIndo-Pacific Timing extent and subregional comparisonsPLOS ONE 2 e711 (2007) doi 101371journalpone0000711pmid 17684557

46 C M Roberts et al Marine biodiversity hotspots andconservation priorities for tropical reefs Science 2951280ndash1284 (2002) doi 101126science1067728pmid 11847338

47 S R Palumbi D J Barshis N Traylor-Knowles R A BayMechanisms of reef coral resistance to future climatechange Science 344 895ndash898 (2014) doi 101126science1251336 pmid 24762535

48 J A Estes et al Trophic downgrading of planet EarthScience 333 301ndash306 (2011) doi 101126science1205106pmid 21764740

49 D J McCauley et al Acute effects of removing large fishfrom a near-pristine coral reef Mar Biol 157 2739ndash2750(2010) doi 101007s00227-010-1533-2 pmid 24391253

50 J A Estes Whales Whaling and Ocean Ecosystems (Univ ofCalifornia Press Berkeley CA 2006)

51 J Terborgh J A Estes Trophic Cascades Predators Preyand the Changing Dynamics of Nature (Island PressWashington DC 2013)

52 D J McCauley F Keesing T P Young B F AllanR M Pringle Indirect effects of large herbivores on snakes inan African savanna Ecology 87 2657ndash2663 (2006)doi 1018900012-9658(2006)87[2657IEOLHO]20CO2pmid 17089673

53 P M Cury et al Global seabird response to forage fishdepletionmdashone-third for the birds Science 334 1703ndash1706(2011) doi 101126science1212928 pmid 22194577

54 D J McCauley et al From wing to wing The persistence oflong ecological interaction chains in less-disturbedecosystems Sci Rep 2 409 (2012) doi 101038srep00409

55 D J McCauley et al Assessing the effects of large mobilepredators on ecosystem connectivity Ecol Appl 221711ndash1717 (2012) doi 10189011-16531 pmid 23092009

56 G L Britten et al Predator decline leads to decreasedstability in a coastal fish community Ecol Lett 17 1518ndash1525(2014) doi 101111ele12354

57 J Roman et al Whales as marine ecosystem engineersFront Ecol Environ 12 377ndash385 (2014) doi 101890130220

58 J M Pandolfi et al Ecology Are US coral reefs on theslippery slope to slime Science 307 1725ndash1726 (2005)doi 101126science1104258 pmid 15774744

59 S R Palumbi A R Palumbi The Extreme Life of the Sea(Princeton Univ Press Princeton NJ 2014)

60 S R Palumbi Humans as the worldrsquos greatest evolutionaryforce Science 293 1786ndash1790 (2001) doi 101126science29355361786 pmid 11546863

61 C Joslashrgensen et al Ecology Managing evolving fish stocksScience 318 1247ndash1248 (2007) doi 101126science1148089 pmid 18033868

62 M L Pinsky S R Palumbi Meta-analysis reveals lowergenetic diversity in overfished populations Mol Ecol 2329ndash39 (2014) doi 101111mec12509 pmid 24372754

63 M R Walsh S B Munch S Chiba D O ConoverMaladaptive changes in multiple traits caused by fishingImpediments to population recovery Ecol Lett 9 142ndash148(2006) doi 101111j1461-0248200500858x pmid 16958879

64 B Worm et al Impacts of biodiversity loss on oceanecosystem services Science 314 787ndash790 (2006)doi 101126science1132294 pmid 17082450

65 J S Brashares et al Wildlife decline and social conflictScience 345 376ndash378 (2014) doi 101126science1256734pmid 25061187

66 Fisheries and Aquaculture Department FAO ldquoThe State ofWorld Fisheries and Aquaculture 2012rdquo (FAO Rome 2012)

67 FAO FAOSTAT (2012) available at httpfaostat3faoorgfaostat-gatewaygotohomeE

68 C C Wilmers J A Estes M Edwards K L LaidreB Konar Do trophic cascades affect the storage andflux of atmospheric carbon An analysis of sea otters andkelp forests Front Ecol Environ 10 409ndash415 (2012)doi 101890110176

69 J-B Raina et al DMSP biosynthesis by an animal and itsrole in coral thermal stress response Nature 502 677ndash680(2013) doi 101038nature12677 pmid 24153189

1255641-6 16 JANUARY 2015 bull VOL 347 ISSUE 6219 sciencemagorg SCIENCE

RESEARCH | REVIEW

present course of marine defaunation We mustplay catch-up in the realm of marine protectedarea establishment tailoring them to be opera-tional in our changing oceans We must alsocarefully construct marine spatial managementplans for the vast regions in between these areasto help ensure that marine mining energy devel-opment and intensive aquaculture take impor-tant marine wildlife habitats into considerationnot vice versa All of this is a tall order but theoceans remain relatively full of the raw faunalingredients and still contain a sufficient degreeof resilient capacity so that the goal of reversingthe current crisis of marine defaunation remainswithin reach The next several decades will bethose in which we choose the fate of the future ofmarine wildlife

REFERENCES AND NOTES

1 R Dirzo et al Defaunation in the Anthropocene Science345 401ndash406 (2014) doi 101126science1251817pmid 25061202

2 A D Barnosky P L Koch R S Feranec S L WingA B Shabel Assessing the causes of late Pleistoceneextinctions on the continents Science 306 70ndash75 (2004)doi 101126science1101476 pmid 15459379

3 P L Koch A D Barnosky Late Quaternary extinctions Stateof the debate Annu Rev Ecol Evol Syst 37 215ndash250(2006) doi 101146annurevecolsys34011802132415

4 A D Barnosky et al Prelude to the Anthropocene Two newNorth American land mammal ages (NALMAs) AnthropolRev (2014) doi 1011772053019614547433

5 S OrsquoConnor R Ono C Clarkson Pelagic fishing at 42000 yearsbefore the present and the maritime skills of modern humansScience 334 1117ndash1121 (2011) doi 101126science1207703pmid 22116883

6 H K Lotze et al Depletion degradation and recoverypotential of estuaries and coastal seas Science 3121806ndash1809 (2006) doi 101126science1128035pmid 16794081

7 J B C Jackson et al Historical overfishing and the recentcollapse of coastal ecosystems Science 293 629ndash637(2001) doi 101126science1059199 pmid 11474098

8 Materials and methods are available as supplementarymaterials on Science Online

9 IUCN The IUCN Red List of Threatened Species Version20142 (2014) available at wwwiucnredlistorg

10 C Mora D P Tittensor S Adl A G B Simpson B WormHow many species are there on Earth and in the oceanPLOS Biol 9 e1001127 (2011) doi 101371journalpbio1001127 pmid 21886479

11 S L Pimm et al The biodiversity of species and their ratesof extinction distribution and protection Science 3441246752 (2014) doi 101126science1246752 pmid 24876501

12 E Alison Kay S R Palumbi Endemism and evolution inHawaiian marine invertebrates Trends Ecol Evol 2 183ndash186(1987) doi 1010160169-5347(87)90017-6 pmid 21227847

13 B P Kinlan S D Gaines Propagule dispersal in marine andterrestrial environments A community perspective Ecology84 2007ndash2020 (2003) doi 10189001-0622

14 B Worm D P Tittensor Range contraction in large pelagicpredators Proc Natl Acad Sci USA 108 11942ndash11947(2011) doi 101073pnas1102353108 pmid 21693644

15 E Dinerstein et al The Fate of wild tigers Bioscience 57508ndash514 (2007) doi 101641B570608

16 S L Fowler et al Eds Sharks Rays and Chimaeras TheStatus of the Chondrichthyan Fishes Status Survey (IUCNCambridge UK 2005)

17 J A Hutchings C Minto D Ricard J K Baum O P JensenTrends in the abundance of marine fishes Can J Fish AquatSci 67 1205ndash1210 (2010) doi 101139F10-081

18 WWF Living Planet Report (WWF International GlandSwitzerland 2012) httpwwfpandaorglpr

19 A M Springer et al Sequential megafaunal collapse in theNorth Pacific Ocean An ongoing legacy of industrial whalingProc Natl Acad Sci USA 100 12223ndash12228 (2003)doi 101073pnas1635156100 pmid 14526101

20 K H Redford The empty forest Bioscience 42 412ndash422(1992) doi 1023071311860

21 H S Young et al Declines in large wildlife increaselandscape-level prevalence of rodent-borne disease in AfricaProc Natl Acad Sci USA 111 7036ndash7041 (2014)doi 101073pnas1404958111 pmid 24778215

22 D J McCauley et al Positive and negative effects of athreatened parrotfish on reef ecosystems Conserv Biol28 1312ndash1321 (2014) doi 101111cobi12314pmid 25065396

23 J E Jimeacutenez The extirpation and current status of wildchinchillas Chinchilla lanigera and C brevicaudata Biol Conserv77 1ndash6 (1996) doi 1010160006-3207(95)00116-6

24 R R Reeves T D Smith Commercial whaling especially forgray whales Eschrichtius robustus and humpback whalesMegaptera novaeangliae at California and Baja Californiashore stations in the 19th century (1854ndash1899) Mar FishRev 72 1ndash25 (2010)

25 R Hilborn et al State of the worldrsquos fisheries Annu RevEnviron Resour 28 359ndash399 (2003) doi 101146annurevenergy28050302105509

26 F Courchamp et al Rarity value and species extinctionThe anthropogenic Allee effect PLOS Biol 4 e415 (2006)doi 101371journalpbio0040415 pmid 17132047

27 D Pauly V Christensen J Dalsgaard R Froese F Torres JrFishing down marine food webs Science 279 860ndash863(1998) doi 101126science2795352860 pmid 9452385

28 S A Sethi T A Branch R Watson Global fisherydevelopment patterns are driven by profit but not trophiclevel Proc Natl Acad Sci USA 107 12163ndash12167 (2010)doi 101073pnas1003236107 pmid 20566867

29 M L Pinsky O P Jensen D Ricard S R PalumbiUnexpected patterns of fisheries collapse in the worldrsquosoceans Proc Natl Acad Sci USA 108 8317ndash8322 (2011)doi 101073pnas1015313108 pmid 21536889

30 J B C Jackson Ecological extinction and evolution in thebrave new ocean Proc Natl Acad Sci USA 105 (suppl 1)11458ndash11465 (2008) doi 101073pnas0802812105pmid 18695220

31 S Jennings J L Blanchard Fish abundance with no fishingPredictions based on macroecological theory J Anim Ecol73 632ndash642 (2004) doi 101111j0021-8790200400839x

32 S K Lyons F A Smith J H Brown Of mice mastodonsand men Human-mediated extinctions on four continentsEvol Ecol Res 6 339ndash358 (2004)

33 A D Smith et al Impacts of fishing low-trophic level specieson marine ecosystems Science 333 1147ndash1150 (2011)doi 101126science1209395 pmid 21778363

34 R S Steneck J Vavrinec A V Leland Accelerating trophic-level dysfunction in kelp forest ecosystems of the westernNorth Atlantic Ecosystems 7 323ndash332 (2004) doi 101007s10021-004-0240-6

35 B Worm R A Myers Meta-analysis of codndashshrimpinteractions reveals top-down control in oceanic food websEcology 84 162ndash173 (2003) doi 1018900012-9658(2003)084[0162MAOCSI]20CO2

36 D O Duggins C A Simenstad J A Estes Magnification ofsecondary production by kelp detritus in coastal marineecosystems Science 245 170ndash173 (1989) doi 101126science2454914170 pmid 17787876

37 R A Myers J K Baum T D Shepherd S P PowersC H Peterson Cascading effects of the loss of apexpredatory sharks from a coastal ocean Science 3151846ndash1850 (2007) doi 101126science1138657pmid 17395829

38 L R Prugh et al The Rise of the Mesopredator Bioscience59 779ndash791 (2009) doi 101525bio20095999

39 S C Anderson J Mills Flemming R Watson H K LotzeRapid global expansion of invertebrate fisheries Trendsdrivers and ecosystem effects PLOS ONE 6 e14735 (2011)doi 101371journalpone0014735 pmid 21408090

40 B S Halpern et al A global map of human impact on marineecosystems Science 319 948ndash952 (2008) doi 101126science1149345 pmid 18276889

41 D J McCauley et al Conservation at the edges of the worldBiol Conserv 165 139ndash145 (2013) doi 101016jbiocon201305026

42 J E Cinner N A J Graham C Huchery M A MacneilGlobal effects of local human population density and distanceto markets on the condition of coral reef fisheries Conserv Biol27 453ndash458 (2013) doi 101111j1523-1739201201933xpmid 23025334

43 K J Mengerink et al A call for deep-ocean stewardshipScience 344 696ndash698 (2014) doi 101126science1251458pmid 24833377

44 E R Selig K S Casey J F Bruno Temperature-drivencoral decline The role of marine protected areas Glob ChangeBiol 18 1561ndash1570 (2012) doi 101111j1365-2486201202658x

45 J F Bruno E R Selig Regional decline of coral cover in theIndo-Pacific Timing extent and subregional comparisonsPLOS ONE 2 e711 (2007) doi 101371journalpone0000711pmid 17684557

46 C M Roberts et al Marine biodiversity hotspots andconservation priorities for tropical reefs Science 2951280ndash1284 (2002) doi 101126science1067728pmid 11847338

47 S R Palumbi D J Barshis N Traylor-Knowles R A BayMechanisms of reef coral resistance to future climatechange Science 344 895ndash898 (2014) doi 101126science1251336 pmid 24762535

48 J A Estes et al Trophic downgrading of planet EarthScience 333 301ndash306 (2011) doi 101126science1205106pmid 21764740

49 D J McCauley et al Acute effects of removing large fishfrom a near-pristine coral reef Mar Biol 157 2739ndash2750(2010) doi 101007s00227-010-1533-2 pmid 24391253

50 J A Estes Whales Whaling and Ocean Ecosystems (Univ ofCalifornia Press Berkeley CA 2006)

51 J Terborgh J A Estes Trophic Cascades Predators Preyand the Changing Dynamics of Nature (Island PressWashington DC 2013)

52 D J McCauley F Keesing T P Young B F AllanR M Pringle Indirect effects of large herbivores on snakes inan African savanna Ecology 87 2657ndash2663 (2006)doi 1018900012-9658(2006)87[2657IEOLHO]20CO2pmid 17089673

53 P M Cury et al Global seabird response to forage fishdepletionmdashone-third for the birds Science 334 1703ndash1706(2011) doi 101126science1212928 pmid 22194577

54 D J McCauley et al From wing to wing The persistence oflong ecological interaction chains in less-disturbedecosystems Sci Rep 2 409 (2012) doi 101038srep00409

55 D J McCauley et al Assessing the effects of large mobilepredators on ecosystem connectivity Ecol Appl 221711ndash1717 (2012) doi 10189011-16531 pmid 23092009

56 G L Britten et al Predator decline leads to decreasedstability in a coastal fish community Ecol Lett 17 1518ndash1525(2014) doi 101111ele12354

57 J Roman et al Whales as marine ecosystem engineersFront Ecol Environ 12 377ndash385 (2014) doi 101890130220

58 J M Pandolfi et al Ecology Are US coral reefs on theslippery slope to slime Science 307 1725ndash1726 (2005)doi 101126science1104258 pmid 15774744

59 S R Palumbi A R Palumbi The Extreme Life of the Sea(Princeton Univ Press Princeton NJ 2014)

60 S R Palumbi Humans as the worldrsquos greatest evolutionaryforce Science 293 1786ndash1790 (2001) doi 101126science29355361786 pmid 11546863

61 C Joslashrgensen et al Ecology Managing evolving fish stocksScience 318 1247ndash1248 (2007) doi 101126science1148089 pmid 18033868

62 M L Pinsky S R Palumbi Meta-analysis reveals lowergenetic diversity in overfished populations Mol Ecol 2329ndash39 (2014) doi 101111mec12509 pmid 24372754

63 M R Walsh S B Munch S Chiba D O ConoverMaladaptive changes in multiple traits caused by fishingImpediments to population recovery Ecol Lett 9 142ndash148(2006) doi 101111j1461-0248200500858x pmid 16958879

64 B Worm et al Impacts of biodiversity loss on oceanecosystem services Science 314 787ndash790 (2006)doi 101126science1132294 pmid 17082450

65 J S Brashares et al Wildlife decline and social conflictScience 345 376ndash378 (2014) doi 101126science1256734pmid 25061187

66 Fisheries and Aquaculture Department FAO ldquoThe State ofWorld Fisheries and Aquaculture 2012rdquo (FAO Rome 2012)

67 FAO FAOSTAT (2012) available at httpfaostat3faoorgfaostat-gatewaygotohomeE

68 C C Wilmers J A Estes M Edwards K L LaidreB Konar Do trophic cascades affect the storage andflux of atmospheric carbon An analysis of sea otters andkelp forests Front Ecol Environ 10 409ndash415 (2012)doi 101890110176

69 J-B Raina et al DMSP biosynthesis by an animal and itsrole in coral thermal stress response Nature 502 677ndash680(2013) doi 101038nature12677 pmid 24153189

1255641-6 16 JANUARY 2015 bull VOL 347 ISSUE 6219 sciencemagorg SCIENCE

RESEARCH | REVIEW

70 F Ferrario et al The effectiveness of coral reefs for coastalhazard risk reduction and adaptation Nat Commun 5 3794(2014) doi 101038ncomms4794

71 M T Burrows et al The pace of shifting climate inmarine and terrestrial ecosystems Science 334652ndash655 (2011) doi 101126science1210288pmid 22053045

72 J J Tewksbury R B Huey C A Deutsch EcologyPutting the heat on tropical animals Science 3201296ndash1297 (2008) doi 101126science1159328pmid 18535231

73 W W Cheung et al Projecting global marine biodiversityimpacts under climate change scenarios Fish Fish 10235ndash251 (2009) doi 101111j1467-2979200800315x

74 J H Stillman Acclimation capacity underlies susceptibility toclimate change Science 301 65ndash65 (2003) doi 101126science1083073 pmid 12843385

75 O Hoegh-Guldberg et al Coral reefs under rapid climatechange and ocean acidification Science 318 1737ndash1742(2007) doi 101126science1152509 pmid 18079392

76 C A Logan J P Dunne C M Eakin S D DonnerIncorporating adaptive responses into future projections ofcoral bleaching Glob Change Biol 20 125ndash139 (2014)doi 101111gcb12390

77 M I OrsquoConnor et al Temperature control of larvaldispersal and the implications for marine ecologyevolution and conservation Proc Natl Acad Sci USA104 1266ndash1271 (2007) doi 101073pnas0603422104pmid 17213327

78 M L Pinsky B Worm M J Fogarty J L SarmientoS A Levin Marine taxa track local climate velocities Science341 1239ndash1242 (2013) doi 101126science1239352pmid 24031017

79 W W L Cheung et al Shrinking of fishes exacerbatesimpacts of global ocean changes on marine ecosystems NatClim Change 3 254ndash258 (2013) doi 101038nclimate1691

80 T A Branch B M DeJoseph L J Ray C A WagnerImpacts of ocean acidification on marine seafood TrendsEcol Evol 28 178ndash186 (2013) doi 101016jtree201210001 pmid 23122878

81 G E Hofmann et al The effect of ocean acidification oncalcifying organisms in marine ecosystems An organism-to-ecosystem perspective Annu Rev Ecol Evol Syst 41127ndash147 (2010) doi 101146annurevecolsys110308120227

82 D G Boyce M Dowd M R Lewis B Worm Estimatingglobal chlorophyll changes over the past century ProgOceanogr 122 163ndash173 (2014) doi 101016jpocean201401004

83 T Agardy G N di Sciara P Christie Mind the gapAddressing the shortcomings of marine protected areasthrough large scale marine spatial planning Mar Policy 35226ndash232 (2011) doi 101016jmarpol201010006

84 L B Crowder et al Sustainability Resolving mismatches inUS ocean governance Science 313 617ndash618 (2006)doi 101126science1129706 pmid 16888124

85 D J McCauley et al Reliance of mobile species on sensitivehabitats A case study of manta rays (Manta alfredi) andlagoons Mar Biol 161 1987ndash1998 (2014) doi 101007s00227-014-2478-7

86 M H Carr et al Comparing marine and terrestrialecosystems Implications for the design of coastal marinereserves Ecol Appl 13 (supp1) 90ndash107 (2003)doi 1018901051-0761(2003)013[0090CMATEI]20CO2

87 M T Burrows et al Geographical limits to species-rangeshifts are suggested by climate velocity Nature 507492ndash495 (2014) doi 101038nature12976 pmid 24509712

88 G J Edgar et al Global conservation outcomes dependon marine protected areas with five key features Nature506 216ndash220 (2014) doi 101038nature13022pmid 24499817

89 C Costello S D Gaines J Lynham Can catch sharesprevent fisheries collapse Science 321 1678ndash1681 (2008)doi 101126science1159478 pmid 18801999

90 C White B S Halpern C V Kappel Ecosystem servicetradeoff analysis reveals the value of marine spatial planningfor multiple ocean uses Proc Natl Acad Sci USA 1094696ndash4701 (2012) doi 101073pnas1114215109pmid 22392996

91 W Qiu P J S Jones The emerging policy landscape formarine spatial planning in Europe Mar Policy 39 182ndash190(2013) doi 101016jmarpol201210010

92 E McLeod R Salm A Green J Almany Designing marineprotected area networks to address the impacts ofclimate change Front Ecol Environ 7 362ndash370 (2009)doi 101890070211

93 S T Turvey Holocene Extinctions (Oxford Univ PressNew York 2009)

94 J Schipper et al The status of the worldrsquos land andmarine mammals Diversity threat and knowledge Science322 225ndash230 (2008) doi 101126science1165115pmid 18845749

95 N K Dulvy J K Pinnegar J D Reynolds in HoloceneExtinctions S T Turvey Ed (Oxford University Press NewYork 2009) pp 129ndash150

96 C V Kappel Losing pieces of the puzzle Threats to marineestuarine and diadromous species Front Ecol Environ 3275ndash282 (2005) doi 1018901540-9295(2005)003[0275LPOTPT]20CO2

97 S D Kraus et al Ecology North Atlantic right whales incrisis Science 309 561ndash562 (2005) doi 101126science1111200 pmid 16040692

98 M L Martiacutenez et al The coasts of our world Ecologicaleconomic and social importance Ecol Econ 63 254ndash272(2007) doi 101016jecolecon200610022

99 P F Sale et al The growing need for sustainable ecologicalmanagement of marine communities of the Persian GulfAmbio 40 4ndash17 (2011) doi 101007s13280-010-0092-6pmid 21404819

100 A B Gill Offshore renewable energy Ecological implicationsof generating electricity in the coastal zone J Appl Ecol 42605ndash615 (2005) doi 101111j1365-2664200501060x

101 The World Bank ldquoFish to 2030 Prospects for fisheries andaquaculturerdquo (83177 The World Bank 2013) pp 1ndash102

102 D H Klinger R Naylor Searching for Solutions inAquaculture Charting a Sustainable Course Annu RevEnviron Resour 37 247ndash276 (2012) doi 101146annurev-environ-021111-161531

103 M D Rose G A Polis The distribution and abundance ofcoyotes The effects of allochthonous food subsidies from thesea Ecology 79 998ndash1007 (1998) doi 1018900012-9658(1998)079[0998TDAAOC]20CO2

104 J S Brashares et al Bushmeat hunting wildlife declinesand fish supply in West Africa Science 306 1180ndash1183(2004) doi 101126science1102425 pmid 15539602

105 S R Palumbi C Sotka The Death and Life of Monterey BayA Story of Revival (Island Press Washington DC 2010)

106 H K Lotze M Coll A M Magera C Ward-Paige L AiroldiRecovery of marine animal populations and ecosystemsTrends Ecol Evol 26 595ndash605 (2011) doi 101016jtree201107008

107 B Worm et al Rebuilding global fisheries Science 325 578ndash585(2009) doi 101126science1173146 pmid 19644114

108 K W Kenyon The sea otter in the Eastern Pacific OceanNorth Am Fauna 68 1ndash352 (1969) doi 103996nafa680001

109 J S Davis Scales of Eden Conservation and pristinedevastation on Bikini Atoll Environ Plan Soc Space 25213ndash235 (2007) doi 101068d1405

110 B deYoung et al Regime shifts in marine ecosystemsDetection prediction and management Trends Ecol Evol 23402ndash409 (2008) doi 101016jtree200803008pmid 18501990

111 T P Hughes et al Phase shifts herbivory and the resilienceof coral reefs to climate change Curr Biol 17 360ndash365(2007) doi 101016jcub200612049 pmid 17291763

112 T Saxby IAN Image and Video Library IAN UMCES availableat ianumceseduimagelibrary

113 IUCN The IUCN Red List of Threatened Species Version20132 (2013) available at wwwiucnredlistorg

114 A S Laliberte W J Ripple Range contractions of NorthAmerican carnivores and ungulates Bioscience 54 123ndash138(2004) doi 1016410006-3568(2004)054[0123RCONAC]20CO2

115 R Pillay A J T Johnsingh R Raghunath M D MadhusudanPatterns of spatiotemporal change in large mammaldistribution and abundance in the southern WesternGhats India Biol Conserv 144 1567ndash1576 (2011)doi 101016jbiocon201101026

116 J A Thomas et al Comparative losses of British butterfliesbirds and plants and the global extinction crisis Science303 1879ndash1881 (2004) doi 101126science1095046pmid 15031508

117 FAO ldquoThe worldrsquos mangroves 1980-2005 FAO ForestryPaper 153rdquo (FAO Rome 2007)

118 The European Wind Energy Association Offshore Statisticsavailable at wwweweaorgstatisticsoffshore

119 International Seabed Authority Contractors Int SeabedAuth available at wwwisaorgjmdeep-seabed-minerals-contractorsoverview

120 The World Bank Container port traffic (TEU 20 footequivalent units) available at httpdataworldbankorgindicatorISSHPGOODTU

ACKNOWLEDGMENTS

We thank A Barnosky N Dulvy M Galetti C Golden T RogierE Selig T White the World Database on Protected AreasB Worm and H Young Figure images were contributed byT Llobet A Musser and IANUMCES (112) Funding was providedby the National Science Foundation and the Gordon andBetty Moore Foundation

SUPPLEMENTARY MATERIALS

wwwsciencemagorgcontent34762191255641supplDC1Materials and MethodsFigs S1 to S7Tables S1 and S2References (121ndash298)

101126science1255641

SCIENCE sciencemagorg 16 JANUARY 2015 bull VOL 347 ISSUE 6219 1255641-7

RESEARCH | REVIEW

DOI 101126science1255641 (2015)347 Science

et alDouglas J McCauleyMarine defaunation Animal loss in the global ocean

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CopyrightAmerican Association for the Advancement of Science 1200 New York Avenue NW Washington DC 20005 (print ISSN 0036-8075 online ISSN 1095-9203) is published weekly except the last week in December by theScience

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