REVIEW SUMMARY

CLIMATE CHANGE

The broad footprint of climate changefrom genes to biomes to peopleBrett R Scheffers Luc De Meester Tom C L Bridge Ary A HoffmannJohn M Pandolfi Richard T Corlett Stuart H M Butchart Paul Pearce-KellyKit M Kovacs David Dudgeon Michela Pacifici Carlo Rondinini Wendy B FodenTara G Martin Camilo Mora David Bickford James E M Watson

BACKGROUNDClimate change impacts havenow been documented across every ecosystemon Earth despite an average warming of only~1degC so far Here we describe the full rangeand scale of climate change effects on globalbiodiversity that have been observed in nat-ural systems To do this we identify a set ofcore ecological processes (32 in terrestrial and31 each in marine and freshwater ecosystems)that underpin ecosystem functioning and sup-port services to people Of the 94 processes

considered 82 show evidence of impact fromclimate change in the peer-reviewed literatureExamples of observed impacts from meta-analyses and case studies go beyond well-established shifts in species ranges and changesto phenology and population dynamics to in-clude disruptions that scale from the gene tothe ecosystem

ADVANCES Species are undergoing evolu-tionary adaptation to temperature extremes

and climate change has substantial impactson species physiology that include changes intolerances to high temperatures shifts in sexratios in species with temperature-dependentsex determination and increased metaboliccosts of living in a warmer world These phys-iological adjustments have observable impactson morphology with many species in bothaquatic and terrestrial systems shrinking inbody size because large surface-to-volume ratiosare generally favored under warmer conditionsOther morphological changes include reduc-tions in melanism to improve thermoregula-tion and altered wing and bill length in birds

Broader-scale responsesto climate change includechanges in the phenologyabundance and distribu-tion of species Temperateplants are budding andflowering earlier in spring

and later in autumn Comparable adjustmentshave been observed in marine and freshwaterfish spawning events and in the timing of sea-sonal migrations of animals worldwide Changesin the abundance and age structure of popula-tions have also been observed with widespreadevidence of range expansion in warm-adaptedspecies and range contraction in cold-adaptedspecies As a by-product of species redistributionsnovel community interactions have emergedTropical and boreal species are increasinglyincorporated into temperate and polar commu-nities respectively and when possible lowlandspecies are increasingly assimilating into moun-tain communities Multiplicative impacts fromgene to community levels scale up to produceecological regime shifts in which one ecosys-tem state shifts to an alternative state

OUTLOOK The many observed impacts ofclimate change at different levels of biologicalorganization point toward an increasinglyunpredictable future for humans Reduced ge-netic diversity in crops inconsistent crop yieldsdecreased productivity in fisheries from re-duced body size and decreased fruit yieldsfrom fewer winter chill events threaten foodsecurity Changes in the distribution of dis-ease vectors alongside the emergence of novelpathogens and pests are a direct threat to hu-man health as well as to crops timber andlivestock resources Humanity depends on in-tact functioning ecosystems for a range ofgoods and services Enhanced understandingof the observed impacts of climate change oncore ecological processes is an essential firststep to adapting to them and mitigating theirinfluence on biodiversity and ecosystem ser-vice provision

RESEARCH

SCIENCE sciencemagorg 11 NOVEMBER 2016 bull VOL 354 ISSUE 6313 719

The list of author affiliations is available in the full article onlineCorresponding author Email brettscheffersufleduCite this article as B R Scheffers et al Science 354 aaf7671(2016) DOI 101126scienceaaf7671

Climate change impacts on ecological processes in marine freshwater and terrestrialecosystems Impacts can be measured on multiple processes at different levels of biologicalorganization within ecosystems In total 82 of 94 ecological processes show evidence ofbeing affected by climate change Within levels of organization the percentage of processesimpacted varies from 60 for genetics to 100 for species distribution

ON OUR WEBSITE

Read the full articleat httpdxdoiorg101126scienceaaf7671

on

Nov

embe

r 10

201

6ht

tp

scie

nce

scie

ncem

ago

rg

Dow

nloa

ded

from

REVIEW

CLIMATE CHANGE

The broad footprint of climate changefrom genes to biomes to peopleBrett R Scheffers1 Luc De Meester2 Tom C L Bridge34 Ary A Hoffmann5

John M Pandolfi6 Richard T Corlett7 Stuart H M Butchart89 Paul Pearce-Kelly10

Kit M Kovacs11 David Dudgeon12 Michela Pacifici13 Carlo Rondinini13

Wendy B Foden14 Tara G Martin15 Camilo Mora16

David Bickford17dagger James E M Watson1819

Most ecological processes now show responses to anthropogenic climate change In terrestrialfreshwater andmarineecosystems species are changinggenetically physiologicallymorphologicallyand phenologically and are shifting their distributionswhich affects food webs and results in newinteractions Disruptions scale from the gene to the ecosystem and have documented consequencesfor people including unpredictable fisheries and crop yields loss of genetic diversity in wild cropvarieties and increasing impacts of pests and diseases In addition to themore easily observedchanges such as shifts in flowering phenology we argue that many hidden dynamics such asgenetic changes are also taking place Understanding shifts in ecological processes can guidehuman adaptation strategies In addition to reducing greenhouse gases climate action andpolicy must therefore focus equally on strategies that safeguard biodiversity and ecosystems

Atmospheric concentrations of greenhousegases from burning fossil fuels and de-forestation are approaching levels that havenot been detected in the past 20 millionyears (1) This has altered the chemical

composition of the Earthrsquos atmosphere oceansand fresh waters (2) As a result temperatures

in the upper ocean and on land are now ~1degChigher than in preindustrial times and temper-ature wind and precipitation regimes havebecome more variable and extreme (3 4) Thesechanges are having clear impacts on planetarybiophysical processes including desalinizationand acidification of the worldrsquos oceans (5) andmelting of permafrost ice sheets and glaciers(6 7) Lakes and rivers have increased in temper-ature altering seasonal patterns of mixing andflows (8)Changing climate regimes have been an im-

portant driver of natural selection in the past(9) and as in the past species are respondingto the current human-induced climate event invarious ways Previous reviews have covered manyof the more obvious changes in species rangesphenologies and population dynamics (10ndash15)but have usually focused on one ecological sys-tem at a time Here we discuss the full rangeand scale of climate change effects on biotaincluding some of the less obvious disruptionsobserved in natural systems We present exam-ples of case studies of observed impacts acrossterrestrial and aquatic biomes and find evidencethat climate change is now affecting most biolog-ical and ecological processes on Earthmdashspanninggenetics organismal physiology and life-historypopulation distributions and dynamics com-munity structure and ecosystem functioning(Fig 1 and table S1) People depend on intactfunctioning ecosystems for a range of goodsand services including those associated withclimate adaptation (16) Understanding the ob-served impacts of current climate change oncore ecological processes is therefore an essen-tial first step in humans planning and adaptingto changing ecosystem conditions

Although inherently different marine fresh-water and terrestrial realms share a commonhierarchy of levels of biological organizationranging from genes to organisms populationsspecies communities and ecosystems Broadlyadapting from Bellard et al (17) we screenedthe literature (supplementary materials) to eval-uate evidence that climate change is affectingecological components across different levels ofbiological organization each of which comprisesa core set of ecological processes (Fig 1 fig S1and table S1) We identify a set of core ecolog-ical processes on Earth (32 in terrestrial and 31each in marine and freshwater) which to-gether facilitate ecosystem functioning thatsupports services to people (17) These processesinclude changes in genetic diversity (genetics)metabolic rates (physiology) body size (morphol-ogy) timing of migration (phenology) recruitment(population dynamics) range size (distribution)loss of synchronization (interspecific relation-ships) and biomass (productivity) (17) Becauseour main goal is to assess what processes areaffected by climate change we define ldquoimpactrdquoon each process as an observed change in thatprocess linked to climate change We do notdifferentiate between ldquopositiverdquo (adaptive buf-fering or mitigating) and ldquonegativerdquo (stress ordamage) responses because responses may bepositive at one level of biological organization(such as genetic adaptation to climate change)but negative at another (such as reduced ge-netic variation and capacity to deal with otherstressors) We then consider the relevance ofthe affected ecological processes in human sys-tems and illustrate observed impacts to ecosys-tem services such as food and resource security(fisheries agriculture forestry and livestock pro-duction) human health and hazard reduction

Ecological impacts of climate change

OrganismsGenetics

There is now growing evidence that species areundergoing evolutionary adaptation to human-induced climate change For example betweenthe 1960s and 2000s the water flea (Daphniamagna) evolved to cope with higher thermalextremes in the UK (18) and cornflower (Centaureacyanus) life history traits have recently evolvedin response to warmer springs across northernFrance (19) Other examples include the evolu-tion of earlier migration timing in anadromouspink salmon (Oncorhynchus gorbuscha) withdecreased frequency of incidence of a geneticmarker that encodes for late migration (20)Time-series data that control for physiologicalacclimatization also show strong evidence forgenetic responses to climate change For exampleBradshaw and Holzapfel showed that genotypicvalues for the critical day length that induces dia-pause in the pitcher plant mosquito (Wyeomyiasmithii) change with latitude and that the lati-tudinal relationship has changed over the periodfrom 1972 to 1996 (21) Onset of diapause nowoccurs later which is consistent with a longer

RESEARCH

SCIENCE sciencemagorg 11 NOVEMBER 2016 bull VOL 354 ISSUE 6313 aaf7671-1

1Department of Wildlife Ecology and Conservation Universityof Florida Gainesville FL 32611-0430 USA 2Laboratory ofAquatic Ecology Evolution and Conservation KU Leuven ChDe Beriotstraat 32 3000 Leuven Belgium 3AustralianResearch Council Centre of Excellence for Coral Reef StudiesJames Cook University Townsville QLD 4811 Australia4Queensland Museum Townsville Queensland 4810 Australia5Bio21 Institute School of Biosciences University of MelbourneVictoria 3010 Australia 6School of Biological Sciences and theAustralian Research Council Centre of Excellence for Coral ReefStudies The University of Queensland Brisbane Queensland4072 Australia 7Center for Integrative ConservationXishuangbanna Tropical Botanical Gardens Chinese Academy ofSciences Yunnan 666303 China 8BirdLife International DavidAttenborough Building Pembroke Street Cambridge CB2 3QZUK 9Department of Zoology University of Cambridge DowningStreet Cambridge CB2 3EJ UK 10Zoological Society of LondonRegentrsquos Park London NW1 4RY UK 11Norwegian PolarInstitute FRAM Centre 9296 Tromsoslash Norway 12School ofBiological Sciences University of Hong Kong Hong Kong SARChina 13Global Mammal Assessment Program Department ofBiology and Biotechnologies Sapienza Universitagrave di Roma VialedellrsquoUniversitagrave 32 I-00185 Rome Italy 14Department of Botanyand Zoology University of Stellenbosch PBag X1 Matieland7602 Stellenbosch South Africa 15Department of Forest andConservation Sciences University of British ColumbiaVancouver British Columbia Canada 16Department ofGeography University of Hawaii Honolulu Hawaii USA17Department of Biological Sciences National University ofSingapore 14 Science Drive 4 117543 Singapore 18School ofGeography Planning and Environmental Management TheUniversity of Queensland Brisbane Queensland 4072 Australia19Global Conservation Program Wildlife Conservation Society2300 Southern Boulevard Bronx NY 10460 USACorresponding author Email brettscheffersufledudaggerPresent address Rimba 4 Jalan 19D 43650 Bandar Baru BangiSelangor Malaysia

on

Nov

embe

r 10

201

6ht

tp

scie

nce

scie

ncem

ago

rg

Dow

nloa

ded

from

aaf7671-2 11 NOVEMBER 2016 bull VOL 354 ISSUE 6313 sciencemagorg SCIENCE

Fig 1 Climate change impacts on Earthrsquos marine terrestrial and fresh-water systems The presence of observed impacts on the differentlevels of biological organization and its inner components across theEarthrsquos marine terrestrial and freshwater ecosystems The denomina-tor represents the total number of processes that we considered foreach group and the numerator is the number of these processes withevidence of impact (a complete list of processes is provided in fig S1and table S1) In total 82 of all (n = 94) ecological processes thatwere considered have observed evidence of impact by climate change

Each process has at least one supporting case study The asterisk in-dicates whether the affected process was assessed in a meta-analysisin addition to case studies Thus double-asterisk indicates that twoprocesses were assessed in at least one meta-analysis Confidence thatthe observed impact can be attributed to climate change was assignedfor each level of organization and ranges from very low low mediumhigh to very high this assessment is based on tables 18-7 18-8 and 18-11in (13) The darkest circle indicates confidence level with the most litera-ture support IM

AGECREDITS

TACEYJO

NESM

ICHELE

WOODIFA

S

RESEARCH | REVIEW

on

Nov

embe

r 10

201

6ht

tp

scie

nce

scie

ncem

ago

rg

Dow

nloa

ded

from

growing season under warmer conditions Oce-anic phytoplankton have adapted to a temper-ature change of +073degC associated with 15 yearsof climate warming in the Gulf of CariacoVenezuela by adjusting their thermal niche by+045degC (22) Although such evidence fromsmall organisms with short generation timesis accumulating we found little documentedevidence of evolutionary change from specieswith longer generation times such as birdsmammals and trees (14 23) although adapta-tion appears to be possible in some long-livedreef corals (24)Changes in species ranges have altered or

created new ldquohybridization zonesrdquo across theplanet For example in North America hybridzones between black-capped (Poecile atricapillus)and Carolina chickadees (P carolinensis) are shift-ing in response to warmer winter temperatures(25) and because the southern flying squirrel(Glaucomys volans) has expanded its range north-ward in eastern North America it is now hybrid-izing with the northern flying squirrel (G sabrinus)(26) In North American rivers and streamshybridization between invasive rainbow trout(Oncorhynchus mykiss) and native cutthroat trout(O clarkia) has increased in frequency as theformer expand into warming waters (27) Such hy-bridization events have also been observed insomemarine fishes such as the coastal West Coastdusky cob (Argyrosomus coronus) and are ex-pected to increase as species shift their rangespoleward in response to rapidly warming oceanconditions (28)

Physiology

Many species display temperature-driven traitplasticity in physiological processes such asthermal optima (29) Whereas some responsessuch as acclimation to high temperatures max-imize fitness others can reflect failure to copewith temperature stress and other climate-mediated changes These responses can occurwithin a generation or between generationsthrough maternal or epigenetic effects (30)There is some observational evidence that

warming has affected temperature-dependentsex determination (TSD) of species in marine andterrestrial systems Snake pipefish (Entelurusaequoreus) in the northeastern Atlantic havealtered their operational sex ratios and reproduc-tive rates as a consequence of warmer sea surfacetemperatures (31) Most evidence for impactson TSD in marine systems however is derivedfrom experimental studies which provide strongsupport for TSD changes in sea turtles and variousfish species (32 33) In terrestrial and freshwatersystems TSD has been implicated in masculin-ization and feminization respectively of lizardand turtle populations (34 35)In marine systems physiological responses to

both climate warming and changing ocean con-ditions are widespread (36 37) Matching fieldand laboratory data for the eelpout (Zoarcesviviparus) show increased metabolic costs asso-ciated with warming in the North and Baltic Seas(38) In aquatic systems warming increases oxy-

gen demand but decreases oxygen content of thewater resulting in substantial metabolic costs(39) Although climate change per se does notcause acidification of the oceans both arise di-rectly from higher atmospheric carbon dioxideand experimental evidence has raised concernsregarding negative effects of ocean acidificationon calcification growth development and sur-vival of calcifying organisms (12) For exampleacidification has led to extensive shell dissolu-tion in populations of the pteropod Limacinahelicina in northwest North America and in theSouthern Ocean off Antarctica (40 41)

Morphology

Individuals in some species are becoming smallerwith increasing warming because large surface-to-volume ratios are generally favored underwarmer conditions (42)mdasha phenomenon that islinked to standard metabolic principles (43) In theAppalachian Mountains six species of Plethodonwoodland salamander have undergone on aver-age an 8 reduction in body size over the past50 years (44) Similarly three species of passer-ine birds from the northeast United States showan average 4 decrease in wing length correlatedwith recent warming (45) and the long-distancemigrant bird the red knot (Calidris canutus) is nowproducing smaller offspring with smaller billswhich reduces survival in juveniles because ofaltered foraging success on underground bivalves(46) In general decreasing body size with warm-ing is expected but evidence from cold high-altitude habitats suggests that increased primaryproductivity and longer growing seasons fromwarming have led to increased body size in somemammal species such as American marten (Martesamericana) and yellow-bellied marmot (Marmotaflaviventris) (47 48) In South Australia leaf widthin soapberry (Dodonaea viscosa) has decreasedcompared with the ancestral condition docu-mented under cooler temperatures 127 years ago(49) Other climate change impacts on morphol-ogy include color changes in butterflies dragon-flies and birds (50ndash53) and pronounced changesin skull shape in the alpine chipmunk (Tamiasalpinus) (54)

PopulationPhenology

For most species migrations and life-historyprocesses (such as budding and flowering inplants hatching and fledging in birds and hi-bernation in mammals) are closely tied to seasonaland interannual variation in climate and thereis now overwhelming evidence that both havebeen affected by climate change (10 37 55 56)Across marine freshwater and terrestrial eco-systems spring phenologies have advanced by23 to 51 days per decade (10 57) A combinationof climate warming and higher atmospheric CO2

concentrations has extended the growing periodof many plant populations (58) In a large globalanalysis which included 21 phenological metricssuch as leaf-off and leaf-on dates and growing-season length plant phenologies were found tohave shifted by more than 2 standard deviations

across 54 of Earthrsquos land area during the pastthree decades (59)In marine and freshwater systems advances

in the timing of annual phytoplankton bloomsmdashthe basis for many aquatic food websmdashhaveoccurred more rapidly than temporal shifts interrestrial plants (37 60) Such changes in plank-ton phenology have been attributed to increasesin water temperatures reduction in the durationof ice cover and the alteration of the seasonalduration of thermal stability or stratification ofthe water columnShifts in spawning times have been documented

for 43 fish species in the northeast Pacific Oceanfrom 1951 to 2008 with earlier spawning asso-ciated with increased sea surface temperatureand later spawning associated with delays inseasonal upwelling of nutrients toward the oceansurface (61) Similar impacts on breeding havebeen observed in terrestrial and marine birdspecies (62)Changes in the timing of migration events have

been extensively documented including advancesin spring arrival dates of long-distance migratorybird species in Europe North America and Aus-tralia (63ndash65) Similarly long-term data on manyamphibians and mammals have shown advance-ments in spring and delays in autumn migration(66ndash68) and altered peak calling periods of maleamphibians (67ndash69) In the largest meta-analysisto date of phenological drivers and trends amongspecies in the southern hemisphere 82 of ter-restrial data sets and 42 of marine data setsdemonstrated an advance in phenology asso-ciated with rising temperature (70)

Abundance and population dynamics

Acute temperature stress can have severe neg-ative effects on population dynamics such asabundance recruitment age structure and sexratios Meta-analyses across thousands of spe-cies report that ~80 of communities acrossterrestrial freshwater and marine ecosystemsexhibited a response in abundance that was inaccordance with climate change predictions(10 70) In a meta-analysis of marine species52 of warm-adapted species increased in abun-dance whereas 52 of cold-adapted speciesdecreased (71) Temperature spikes may causemass mortality of key ecosystem engineers inboth temperate and tropical oceans Excessiveheat kills canopy-forming macroalgae in tem-perate marine systems (72) and causes bleach-ing and mass mortality of corals in the tropics(73) Reductions in sea ice extent have causeddeclines in abundances of ice-affiliated species inthe Arctic [for example ivory gulls (Pagophilaeburnea) ringed seals (Pusa hispida) and polarbears (Ursus maritimus) (74)] whereas in somecases such as on Beaufort Island in the southernRoss Sea the loss of ice from receding glaciersresulted in increased abundances of Adeacutelie pen-guins (Pygoscelis adeliae) (75) In the United Statesthe bull trout (Salvelinus confluentus) has lostgt10 of its spawning grounds in central Idahoover the past 13 years because of increased watertemperatures (76) while the brown trout (Salmo

SCIENCE sciencemagorg 11 NOVEMBER 2016 bull VOL 354 ISSUE 6313 aaf7671-3

RESEARCH | REVIEW

on

Nov

embe

r 10

201

6ht

tp

scie

nce

scie

ncem

ago

rg

Dow

nloa

ded

from

trutta) has lost habitat in the Swiss Alps (77) Inwestern Canada reduced survival of adult migrat-ing Fraser River sockeye salmon (Oncorhynchusnerka) has been observed with increased watertemperatures (78) and in eastern Canadian lakesgolden-brown algae dramatically increased in abun-dance as water temperature increased 15degC dur-ing the latter part of the 20th century (79) Someof the best evidence for climate-change impactson the abundance of terrestrial species comesfrom analyses of bird population trends derivedfrom systematic monitoring schemes in Europewith warm-adapted species having increasedin abundance on average since the 1980s andcold-adapted species having declined (80)Climate change can increase the abundance of

temperature-sensitive disease vectors with subse-quent effects on disease outbreaks In the AfricanSerengeti there is some evidence that a com-bination of extreme weather high abundancesof ticks carrying Babesia-piroplasm and sup-pressed immunity to canine distemper virus ledto widespread mortality of lions (Panthera leo)(81) In marine systems field evidence showsthat corals are increasingly susceptible to whiteband disease at higher temperatures leading todeclines in two of the most important reef-buildingacroporid (branching) corals in the western At-lantic (82)

SpeciesDistribution

One of the most rapid responses observed formarine freshwater and terrestrial species is ashift in their distributions to track optimal hab-itat conditions (71 83 84) Across land and aquaticecosystems species have expanded their lead-ing (cold limit) edge by 197 km per decade withmarine species expanding by 72 km per decadecompared with 6 km per decade in terrestrialspecies (37) The distributions of many marinetaxa have shifted at higher velocities than thoseof terrestrial taxa (37) because areas with rapidchanges in climate extend across broader re-gions of the ocean than on land and connectiv-ity in marine environments tends to be high (85)To illustrate this point corals around Japan haveshifted their range by up to 14 km per year overthe past 80 years (86) and in waters off the south-east coast of Australia intertidal invertebratespecies have shifted their geographic distribu-tions polewards at an average rate of 29 kmper decade (87) Where connectivity allows fordispersal some freshwater fishes are capableof shifting at rates comparable with those ofmarine and terrestrial taxa (88) but mean shiftsby river fishes in some regions have been in-sufficient to compensate for measured temper-ature rises (89)There has been a consistent overall trend for

tropical warm-adapted species to expand theirranges into environments previously dominatedby temperate cold-tolerant species (ldquotropicaliza-tionrdquo) (90) A similar phenomenon has beendocumented in the Arctic where boreal fish com-munities have responded to warming in theBarents Sea by shifting northward resulting in a

high turnover in Arctic fish communities (ldquobore-alizationrdquo) (91) Similarly on land increased mini-mum temperatures have driven rapid changesin the range size (as well as distribution) of Swe-dish birds with northern species retracting andsouthern species expanding northward (92)In addition to latitudinal changes many ob-

served shifts in species distributions have occuredacross elevation gradients In the mountains ofNew Guinea birds have shifted their distribu-tions upslope by 95 to 152 m from 1965 to 2013(93) A similar upslope shift was observed in re-cent decades in mountainous stream-dwellingfish in France (89) North American plants (94)and Bornean insects (95) An analogous responsehas been the shift to deeper colder waters amongsome marine fishes (91)In some cases species have shown no response

or even downhill shifts in their distributions(96) or increased frequency of range disjunctionrather than poleward or upward range shifts(97) Savage and Vellend (98) found upward rangeshifts in North American plant species and anoverall trend toward biotic homogenization from1970 to 2010 but their study also documents con-siderable time lags between warming and plantresponses (99 100) Delayed community responsesto increasing temperature may be in part due tothe buffering effects of microhabitats (101 102)and possibly moisture which is a critical butless often studied driver in the redistribution ofspecies (103) For example Crimmins et al ob-served downhill movements for North Americanplants under climate change over an 80-year pe-riod which they attribute to changes in waterbalance rather than temperature (104)

CommunityInterspecific relationships

As a by-product of the redistribution of speciesin response to changing climate existing inter-actions among species are being disrupted andnew interactions are emerging (105 106) Thesenovel biotic interactions can exacerbate the impactsof abiotic climate change (107 108) Woody plantsare invading arctic and alpine herb-dominatedcommunities in response to rapid warming inrecent decades leading to secondary shifts indistribution of other plants and animals (92)In the Sierra Nevada Mountains of CaliforniaTingley and Beissinger found high levels ofavian community turnover during the past100 years at the lowest and highest elevations(109) and in Greece Sgardeli et al found sim-ilar patterns of temperature-driven turnover inbutterfly communities (110) There are surpris-ingly few studies of observed impacts of cli-mate change on competitive interactions (108)In one example from Sweden Wittwer et alfound that among four bird species occupyingthe same ecological guild resident birds wereable to adapt to warmer temperatures and out-compete the sole long-distance migrant Ficedulahypoleuca (111)New interactions among species can also lead

to trophic disruptions such as overgrazing Inwestern Australia for example overgrazing of

subtropical reefs by the poleward spread oftropical browsing fish has suppressed recoveryof seaweeds after temperature-induced mortal-ity (112) These types of trophic disruptions areescalating with range shifts by tropical herbiv-orous fishes increasing herbivory rates in sub-tropical and temperate coastal ecosystems whereseaweeds are the dominant habitat-formingtaxa (90)Phenological mismatches have been observed

between butterflies and their annual host plantswith the plants dying before the insect larvaewere ready to enter diapause (113) Similarly ananalysis of 27 years of predator-prey data fromthe UK showed asynchronous shifts between thetawny owl (Strix aluco) and its principle preythe field vole (Microtus agrestis) which led to re-duced owl fledging success (114) In Lake Wash-ington United States spring diatom bloomsadvanced by over 20 days since 1962 resultingin predator-prey mismatches with their maingrazer the water flea (Daphnia pulicaria) andpopulation declines in the latter (60) In Cana-dian Arctic lakes asynchronous shifts in diatomblooms resulted in generalist water fleas beingreplaced by more specialist species (115) Athigher trophic levels warming has affected thefry and the juvenile life-history stages of lakechar (Salvelinus umbla) via direct impacts ontheir zooplankton and vendace (Coregonus alba)food sources (116)

Productivity

Changes in productivity are one of the mostcritical impacts of climate change across aquaticand terrestrial ecosystems (117 118) In marinesystems climate-mediated changes in chlorophyll-aconcentrations as a proxy of phytoplankton bio-mass have been highly variable (119) Dependingon location these include both dramatic in-creases and decreases in abundance as well aschanges in phenology and distribution of phyto-plankton over the past several decades In aglobal study of phytoplankton since 1899 an~1 decline in global median phytoplanktonper year was strongly correlated with increasesin sea surface temperature (120) whereas in theAntarctic Peninsula phytoplankton increasedby 66 in southern subregions and decreasedby 12 in northern subregions over a 30-yearperiod These conflicting observations in theAntarctic are in part linked to changes in seasurface temperature but also changes in ice covercloudiness and windiness which effect water-column mixing (121)In deep tropical freshwater lakes dominated

by internal nutrient loading through regularmixing warmer surface waters confer greaterthermal stability with reduced mixing and re-turn of nutrients to the photic zone substan-tially decreasing primary productivity (122)phytoplankton growth (123) and fish abun-dance (122) In contrast eutrophication effectsare exacerbated by higher temperatures in shal-low lakes resulting in increased productivityand phytoplankton and toxic cyanobacteriablooms (124)

aaf7671-4 11 NOVEMBER 2016 bull VOL 354 ISSUE 6313 sciencemagorg SCIENCE

RESEARCH | REVIEW

on

Nov

embe

r 10

201

6ht

tp

scie

nce

scie

ncem

ago

rg

Dow

nloa

ded

from

Globally terrestrial plant growth has increasedwith increasing temperatures and CO2 levelsThis may in part explain the on average 6 in-crease in net primary productivity (NPP) from1982 to 1999 (125) although these changes inNPP may also be related to natural variation inEl NintildeondashLa Nintildea cycles (126) However responsesare highly variable and some terrestrial systemsare not experiencing increased productivity owingto either extreme temperatures or lack of waterSevere short-term droughts in climatically sta-ble rainforest environments are unusual but inrecent years have increased in frequency Theseevents have led to changes in forest canopy struc-ture in Amazonia (127) and decreases in above-ground woody and leaf biomass in the Congobasin (128) Across large expanses of the Amazonthere has been an overall reduction in above-

ground biomass owing to increased climate var-iability over the past three decades (129)

Impacts across ecosystems

All three biotic realms (terrestrial freshwater andmarine) are being affected by climate change andthe evidence summarized here reveals that theseimpacts span the biological hierarchy from genesto communities Of the 94 processes consideredwe found that 82 have evidence of impact byclimate change and this has occurred with just1degC of average warming globally (Fig 1) Impactsrange from genetic and physiological changesto responses in population abundance and dis-tribution (Fig 2)The fact that evidence is missing for some

processes is more likely to reflect data deficien-cies than the absence of any response to climate

change We only considered field-based casestudies that report changes in the processesthrough time For many components such asgenetics (23) and physiology (29) there is strongevidence from experiments on a wide range ofspecies that individuals and populations canand likely will respond to climate change Thuseven though we found compelling evidenceof widespread responses across the biologicalhierarchy we still consider our discussion of im-pacted processes to be conservative To illustratethis point Box 1 shows the range of observed re-sponses in the water flea Daphnia which spansthe entire hierarchy of biological organization

Ecosystem state shifts

As ecological systems continue to accumulatestress through compromised ecological processes

SCIENCE sciencemagorg 11 NOVEMBER 2016 bull VOL 354 ISSUE 6313 aaf7671-5

Fig 2 Climate impacts on ecological processes Examples of ecological components and processes affected by climate changes across marinefreshwater and terrestrial ecosystems (fig S1 and table S1)

IMAGECREDITS

TACEYJO

NESM

ICHELE

WOODIFA

SRESEARCH | REVIEW

on

Nov

embe

r 10

201

6ht

tp

scie

nce

scie

ncem

ago

rg

Dow

nloa

ded

from

either directly from climate change or interac-tively with other forced disturbances (discus-sion is provided in the supplementary materials)diminished resilience may lead to ecological re-gime shiftsmdashin which one ecosystem state shiftsto an alternative and potentially undesirable sta-ble state For example some reefs are transi-tioning from coral- to algal-dominated states asa consequence of mass coral mortality (130)

whereas kelp forests are turning into rocky bar-rens in temperate seas (90 131 132) In lakesclimate change has increased the risk of regimeshifts from clear-water to turbid states and in-creased the occurrence of cyanobacteria blooms(124) If sufficient community-based processesare affected at regional scales wholesale biomeshifts can occur such as has been observed inAlaska where tundra is transitioning to borealconditions (133) These are clear signs of large-scale ecosystem change and disruption in whichdisequilibrium rapidly pushes the system into anew state (134)

Using ecology to better understandclimate change impacts on humanwell-beingThreats to production

The impacts of climate change on marine fish-eries have major consequences for human so-cieties because these currently provide ~17of the global protein for people (135) There ishowever no current consensus on the costs andbenefits of the ongoing global redistributionof fisheries because trends are highly variableIn the Arctic commercially important fish suchas Atlantic cod (Gadus morhua) and walleye pol-lock (Theragra chalcogramma) have increased inbiomass primarily because of increases in plank-ton production from reduced sea ice (136 137)whereas changes in fish biomass in the SouthernOcean are less clear (138) In Switzerland whichhas experienced twice the average global temper-ature increase trout catches have been halvedover two decades because of rising temperaturesin Alpine streams (77)Changes in total marine productivity are not

just attributed to abundance shifts but also mor-phological shifts Indeed some fish species ap-pear to be shrinking but attributing this solely toocean warming is difficult because size-dependentresponses can be triggered by commercial fishingas well as long-term climate change (139) How-ever long-term trend analyses show convincinglythat eight commercial fish species in the NorthSea underwent simultaneous reductions in bodysize over a 40-year period because of ocean warm-ing resulting in 23 lower yields (140) Reducedbody size in fish is also being recorded in lakesand rivers throughout Europe and has beenlinked to increased temperature and climate-induced shifts in nutrient inputs (141 142)Impacts on plant genetics and physiology are

influencing human agricultural systems Forexample yields in rice maize and coffee havedeclined in response to the combined effectsof rising temperatures and increasing precipita-tion variability over past decades (143ndash145)Genetics is being used to counteract decreasingyields in some key crops such as wheat [for whichglobally yields have declined by 6 since theearly 1980s (146)] through crossing domesticatedcrops with wild relatives to maintain the evolu-tionary potential of varieties (147) Yet some im-portant wild strains are also showing signs ofimpact from climate change Nevo et al docu-mented high levels of genetic changes in the

progenitors of cultivated wheat and barley inIsrael over the past 28 years (148) These wildcereals exhibited landscape-level changes inflowering time and a loss of genetic diversity inresponse to increasing temperaturesLosing genetic resources in nature may un-

dermine future development of novel crop var-ieties (149) and compromise key strategies thathumans use to adapt to climate change Onesuch strategy is to use assisted gene flow themanaged movement of individuals or gametesbetween populations to mitigate local maladap-tation in the short and long term (150) Wheregenetic introgressionmdashthe movement of geneticmaterial from one species into the genome ofanothermdashcan occur from unexploited natural pop-ulations to managed or exploited populationsthat are poorly adapted to warmer or drier con-ditions adaptive changes may be facilitated (147)as in white spruce (Picea glauca) a tree commonlyharvested for timber (151) Human-assisted evolu-tion may also be a key strategy in maintaining reef-dependent fisheries by accelerating and enhancingthe stress tolerance of corals (152)Phenological changes due to milder winters

are influencing crop and fruit production (153)Climate change has reduced winter chill eventsin temperate agricultural areas (154) whichcan desynchronize male and female flowers andtrigger delayed pollination delayed foliationand reduced fruit yield and quality To counterthis tree crop industries have developed adap-tation measures such as low-chill cultivars withdormancy-breaking chemicals For example theldquoUFBestrdquo peach requires four times fewer chilldays than cultivars frommore temperate climates(155) Advances in the timing of budding flower-ing and fruiting of plant species has inducedearlier harvesting periods in some countries[such as Japan (156)]Pollination is a key process linked to yields for

a large number of crops The short-lived highlymobile insect species that provide pollination ser-vices to numerous crops have responded rapidlyto changing climates by shifting their rangesthroughout North America and Europe (157) Ad-ditionally over the past 120 years many plant-pollinator networks have been lost with overalldecline in pollination services which is attributedto a combination of habitat loss pollution andclimate warming (158) Yet observed changes inthe phenology abundance and distribution of com-mon pollinators have not been directly linked todeclines in yields of animal-pollinated cropsThis is likely due to limited data that directlylink pollination services to crop yield over timeand may in part reflect resilience provided bythe diversity of insect species that pollinatemany crops (159 160) More specialized pollina-tion systems are expected to be more vulnerableto climate change Humans have adapted to thedeclines in native pollinators by transportingdomesticated pollinators to crop locations

Pest and disease threats

Climate-induced ecosystem-level changes suchas forest die-offs have an obvious impact on

aaf7671-6 11 NOVEMBER 2016 bull VOL 354 ISSUE 6313 sciencemagorg SCIENCE

Box 1 A complete hierarchy of climatechange impact in one model system thewater flea Daphnia Combining time-seriesdata with experimental approaches can lendinsights to the breadth of climate change im-pacts For water fleas of the genus Daphniafor instance there is evidence for responsesto temperature at all levels of biological or-ganization Daphnia are important grazersin lakes and ponds (180) They adapt to tem-perature increase through genetic changesin thermal tolerance (18) body size and lifehistory traits (181 182) In the laboratoryDaphnia exhibit phenotypic plasticity in phys-iology to changing temperatures [for exam-ple hemoglobin quality and quantity (183)or metabolic activity (184)] behavior [suchas swimming activity (184)] life history traits(185) and body size (182) Daphnia adjusttheir phenology (186) and abundance (187)in response to increases in temperature whichresults in mismatches with phytoplanktondynamics (60) Warmer drier weather overtwo decades can lead to expanded distri-butions and increased colonization capacity(188) Temperature influences interactionsof Daphnia with predators (189) and para-sites (190) and adaptation to increased tem-perature influences competitive strength(185) In the absence of fish high abundancesof Daphnia in +4degC heated mesocosms ex-ert strong top-down control on phytoplank-ton (191)

PHOTOJ

OACHIM

MERGEAY

RESEARCH | REVIEW

on

Nov

embe

r 10

201

6ht

tp

scie

nce

scie

ncem

ago

rg

Dow

nloa

ded

from

people with a reduction in timber supplies andcarbon sequestration and changes in water qualityand watershed volume (161ndash163) Several nativeinsect species from North America with no priorrecords of severe infestation have recently emergedas severe pathogens of forest resources because ofchanges in population dynamics These includethe Aspen leaf miner (Phyllocnistis populiella)the leafblotch miner (Micrurapteryx salicifoliella)and the Janetrsquos looper (Nepytia janetae) whichhave decimated millions of hectares of aspenwillows and spruce-fir forests since the early1990s (164) Known pests such as mountain andsouthern pine beetles (Dendroctonus frontalis andD ponderosae respectively) and spruce beetles(D rufipennis) have recently expanded their dis-tribution and infestation intensity on commer-cially important pine and spruce trees (161 164)These outbreaks may increase in the future be-cause hundreds of plant pest and pathogen spe-cies have shifted their distributions 2 to 35 kmyearminus1 poleward since the 1960s (165)An emerging threat to human health under

climate change is vector-borne disease (166)Vectors that have shifted their ranges and abun-dance can be found in marine freshwater andterrestrial systems For example in marine sys-tems unprecedented warming in the Baltic Sealed to emergence of Vibrio infections in North-ern Europe (167 168) a geographic localitythat had limited prior occurrence of this water-borne bacterial pathogen Mosquitoes (eg Aedesjaponicus A aegypti A albopictus) are extendingtheir distribution into areas that are much warmerthan their original habitats As a result of eco-

logical adaptation mosquitos have become morecompetent vectors for spreading diseases suchas chikungunya dengue and possibly the emerg-ing Zika virus (169) Last in terrestrial systemsLevi et al found that the nymph stage of theLyme diseasendashcarrying blacklegged tick (Ixodesscapularis) exhibited an overall advancement innymph and larvae phenology since 1994 shiftingthe timing of greatest risk for pathogen transferto humans to earlier in the year (170)

Losing intact ecosystemsand their function

Changes in ecological processes might com-promise the functionality of ecosystems This isan important consideration because healthy sys-tems (both terrestrial and marine) sequester sub-stantial amounts of carbon (171) regulate localclimate regimes (172) and reduce risks associatedwith climate-related hazards such as floods sea-level rise and cyclones (173) In island and coastalcommunities coral reefs can reduce wave energyby an average of 97 (174) and coastal ecosystemssuch asmangroves and tidal marshes buffer storms(175) while on land intact native forests are im-portant in reducing the frequency and severity offloods (176) In many cases maintaining function-ing systems offers more sustainable cost-effectiveand ecologically sound alternatives than conven-tional engineering solutions (16)

Science and action in a warmer world

The United Nations Framework Convention onClimate Change (UNFCCC) and the recent COP21agreement in Paris presently offer the best

opportunity for decisive action to reduce thecurrent trajectory of climate change This latteragreement set global warming targets of 15 to2degC above preindustrial levels in order to avoidldquodangerous climate changerdquo yet the current 1degCaverage increase has already had broad andworrying impacts on natural systems with ac-cumulating consequences for people (Table 1)Minimizing the impacts of climate change oncore ecological processes must now be a keypolicy priority for all nations given the adop-tion of the UN Sustainable Development Goalsaiming to increase human well-being This willrequire continued funding of basic science focusedon understanding how ecological processes areinteracting with climate change and of programsaimed at supporting ecosystem-based adaptationsthat enhance natural defences against climate haz-ards for people and nature and ensure ongoingprovision of natural goods and services (177)We must also recognize the role that intact

natural ecosystems particularly large areasplay in overcoming the challenges that climatechange presents not only as important reposi-tories for carbon but also because of their abilityto buffer and regulate local climate regimes andhelp human populations adapt to climate change(16 173) These systems are also critical for main-taining global biodiversity because the con-nectivity provided by large contiguous areasspanning environmental gradientsmdashsuch as alti-tude depth or salinitymdashwill maximize the poten-tial for gene flow and genetic adaptation whilealso allowing species to track shifting climatespatially (178)

SCIENCE sciencemagorg 11 NOVEMBER 2016 bull VOL 354 ISSUE 6313 aaf7671-7

Table 1 Climate change consequences for humans Affected ecological processes have direct consequences in food systems and human health

Organism Population Species Community

Genetics physiology

morphologyPhenology dynamics Distribution

Interspecific relationships

productivity

Resource security Rapid genetic adaptation to

climate change in timber

species

Increased herbivory on crops

and timber by pests

Overall distribution shifts in

marine and freshwater

fisheries

Decline in plant-pollinator

networks and pollination

services

Decreased crop yields in hot

climates and increases in

cool climates

Decreased genetic diversity

and altered flowering

time in wild cereals and

novel crop varieties

Reduced range size or changes

in pollinator abundance

Novel pests and invasive

species

Increased weed-crop

competition and parasite-

livestock interactions

Reduced fruit yields from

fewer winter chill events

Decreased yield in fisheries

from reduced body size

Reduced productivity in

commercial fisheries

Human health Decline in reef calcifiers

threatens coastal

communities loss of

protection from storm

surges and loss of

foodprotein sources

Increased costs and risk to

subsistence communities

from loss of sea ice and

permafrost

Expanding andor new

distributions of disease

vectors

Increased human-wildlife

conflicts

Rapid adaptation of disease

vectors to new climatic

conditions

Redistribution of arable land Novel disease vectors

RESEARCH | REVIEW

on

Nov

embe

r 10

201

6ht

tp

scie

nce

scie

ncem

ago

rg

Dow

nloa

ded

from

The overriding priority of the UNFCCC is to setin motion a sustained global reduction in green-house gas emissions This must be achievedalongside an improvement in our understandingof key ecological processes that form the foun-dation of biological and human systems and intandem with efforts to conserve the natural hab-itats in which such ecological processes operateIt is now up to national governments to make

good on the promises they made in Paris throughregular tightening of emission targets and alsoto recognize the importance of healthy ecosys-tems in times of unprecedented change (179)Time is running out for a globally synchronizedresponse to climate change that integrates ade-quate protection of biodiversity and ecosystemservices

REFERENCES AND NOTES

1 D J Beerling D L Royer Convergent Cenozoic CO2 historyNat Geosci 4 418ndash420 (2011) doi 101038ngeo1186

2 P Ciais et al in Climate Change 2013 The Physical ScienceBasis Contribution of Working Group I to the FifthAssessment Report of the Intergovernmental Panel on ClimateChange T F Stocker et al Eds (Cambridge Univ Press2014) pp 465ndash570

3 N L Bindoff et al in Climate Change 2013 The PhysicalScience Basis Contribution of Working Group I to the FifthAssessment Report of the Intergovernmental Panel on ClimateChange T F Stocker et al Eds (Cambridge Univ Press2013) pp 867ndash952

4 S J Smith J Edmonds C Hartin A Mundra K CalvinNear-term acceleration in the rate of temperature changeNat Clim Chang 5 333ndash336 (2015) doi 101038nclimate2552

5 R Curry C Mauritzen Dilution of the northern North AtlanticOcean in recent decades Science 308 1772ndash1774 (2005)doi 101126science1109477 pmid 15961666

6 W N Meier et al Arctic sea ice in transformationA review of recent observed changes and impacts on biologyand human activity Rev Geophys 52 185ndash217 (2014)doi 1010022013RG000431

7 B Marzeion J G Cogley K Richter D Parkes Attributionof global glacier mass loss to anthropogenic and naturalcauses Science 345 919ndash921 (2014) doi 101126science1254702 pmid 25123485

8 M W Swinton L W Eichler J L Farrell C W BoylenEvidence for water temperature increase in Lake George NYImpact on growing season duration and degree daysLake Reservior Manage 31 241ndash253 (2015) doi 1010801040238120151067660

9 B Sandel et al The influence of Late Quaternary climate-change velocity on species endemism Science 334 660ndash664(2011) doi 101126science1210173 pmid 21979937

10 C Parmesan G Yohe A globally coherent fingerprintof climate change impacts across natural systemsNature 421 37ndash42 (2003) doi 101038nature01286pmid 12511946

11 C Parmesan Ecological and evolutionary responses torecent climate change Annu Rev Ecol Evol Syst 37637ndash669 (2006) doi 101146annurevecolsys37091305110100

12 K J Kroeker et al Impacts of ocean acidification onmarine organisms Quantifying sensitivities and interactionwith warming Glob Change Biol 19 1884ndash1896 (2013)doi 101111gcb12179 pmid 23505245

13 W Cramer et al in Climate Climate Change 2014 ImpactsAdaptation and Vulnerability C B Field et al Eds(Cambridge Univ Press 2014) pp 979ndash1038

14 J Merilauml A P Hendry Climate change adaptation andphenotypic plasticity The problem and the evidenceEvol Appl 7 1ndash14 (2014) doi 101111eva12137pmid 24454544

15 J-P Gattuso et al Contrasting futures for ocean and societyfrom different anthropogenic CO2 emissions scenariosScience 349 aac4722 (2015) pmid 26138982

16 T G Martin J E M Watson Intact ecosystems providebest defence against climate change Nat Clim Chang 6122ndash124 (2016) doi 101038nclimate2918

17 C Bellard C Bertelsmeier P Leadley W ThuillerF Courchamp Impacts of climate change on the futureof biodiversity Ecol Lett 15 365ndash377 (2012)pmid 22257223

18 N Geerts et al Rapid evolution of thermal tolerance in thewater flea Daphnia Nat Clim Chang 5 1ndash5 (2015)

19 M Thomann E Imbert R C Engstrand P-O CheptouContemporary evolution of plant reproductive strategiesunder global change is revealed by stored seeds J Evol Biol28 766ndash778 (2015) doi 101111jeb12603 pmid 25682981

20 R P Kovach A J Gharrett D A Tallmon Genetic changefor earlier migration timing in a pink salmon populationProc Biol Sci 279 3870ndash3878 (2012) doi 101098rspb20121158 pmid 22787027

21 W E Bradshaw C M Holzapfel Genetic shift inphotoperiodic response correlated with global warmingProc Natl Acad Sci USA 98 14509ndash14511 (2001)doi 101073pnas241391498 pmid 11698659

22 A J Irwin Z V Finkel F E Muumlller-KargerL Troccoli Ghinaglia Phytoplankton adapt to changing oceanenvironments Proc Natl Acad Sci USA 112 5762ndash5766(2015) doi 101073pnas1414752112 pmid 25902497

23 A A Hoffmann C M Sgrograve Climate change and evolutionaryadaptation Nature 470 479ndash485 (2011) doi 101038nature09670 pmid 21350480

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

25 S A Taylor et al Climate-mediated movement of an avianhybrid zone Curr Biol 24 671ndash676 (2014) doi 101016jcub201401069 pmid 24613306

26 C J Garroway et al Climate change induced hybridizationin flying squirrels Glob Change Biol 16 113ndash121 (2010)doi 101111j1365-2486200901948x

27 C C Muhlfeld et al Invasive hybridization in a threatenedspecies is accelerated by climate change Nat Clim Chang4 620ndash624 (2014) doi 101038nclimate2252

28 W M Potts et al Ocean warming a rapid distributionalshift and the hybridization of a coastal fish species GlobChange Biol 20 2765ndash2777 (2014) doi 101111gcb12612pmid 24753154

29 S L Chown et al Adapting to climate change A perspectivefrom evolutionary physiology Clim Res 43 3ndash15 (2010)doi 103354cr00879

30 J M Donelson P L Munday Transgenerational plasticitymitigates the impact of global warming to offspring sexratios Glob Change Biol 21 2954ndash2962 (2015) doi 101111gcb12912 pmid 25820432

31 R R Kirby D G Johns J A Lindley Fathers in hot waterRising sea temperatures and a Northeastern Atlantic pipefishbaby boom Biol Lett 2 597ndash600 (2006) doi 101098rsbl20060530 pmid 17148298

32 L A Hawkes A C Broderick M H Godfrey B J GodleyInvestigating the potential impacts of climate change on amarine turtle population Glob Change Biol 13 923ndash932(2007) doi 101111j1365-2486200701320x

33 N Ospina-Aacutelvarez F Piferrer Temperature-dependent sexdetermination in fish revisited Prevalence a single sex ratioresponse pattern and possible effects of climate changePLOS ONE 3 e2837 (2008) doi 101371journalpone0002837 pmid 18665231

34 L E Schwanz F J Janzen Climate change and temperature-dependent sex determination Can individual plasticity innesting phenology prevent extreme sex ratios PhysiolBiochem Zool 81 826ndash834 (2008) doi 101086590220pmid 18831689

35 R S Telemeco M J Elphick R Shine Nesting lizards(Bassiana duperreyi) compensate partly but not completelyfor climate change Ecology 90 17ndash22 (2009) doi 10189008-14521 pmid 19294908

36 P Krishnan et al Elevated sea surface temperatureduring May 2010 induces mass bleaching of corals in theAndaman Curr Sci 100 111ndash117 (2011)

37 E S Poloczanska et al Global imprint of climate change onmarine life Nat Clim Chang 3 919ndash925 (2013)

38 H O Poumlrtner R Knust Climate change affects marinefishes through the oxygen limitation of thermal toleranceScience 315 95ndash97 (2007) doi 101126science1135471pmid 17204649

39 C Deutsch A Ferrel B Seibel H-O Poumlrtner R B HueyClimate change tightens a metabolic constraint on marinehabitats Science 348 1132ndash1135 (2015) doi 101126scienceaaa1605 pmid 26045435

40 N Bednaršek et al Limacina helicina shell dissolution as anindicator of declining habitat suitability owing to oceanacidification in the California Current Ecosystem Proc RSoc B Biol Sci 281 20140123 (2014)

41 N Bednaršek et al Extensive dissolution of live pteropodsin the Southern Ocean Nat Geosci 5 881ndash885 (2012)doi 101038ngeo1635

42 J Sheridan D Bickford Shrinking body size as an ecologicalresponse to climate change Nat Clim Chang 1 401ndash406(2011) doi 101038nclimate1259

43 J H Brown J F Gillooly A P Allen V M Savage G B WestToward a metabolic theory of ecology Ecology 85 1771ndash1789(2004) doi 10189003-9000

44 N M Caruso M W Sears D C Adams K R Lips Widespreadrapid reductions in body size of adult salamanders inresponse to climate change Glob Change Biol 20 1751ndash1759(2014) doi 101111gcb12550 pmid 24664864

45 D E McCoy Connecticut birds and climate changeBergmannrsquos rule in the fourth dimension NortheastNatural 19 323ndash334 (2012) doi 1016560450190213

46 J A van Gils et al Body shrinkage due to Arctic warmingreduces red knot fitness in tropical wintering rangeScience 352 819ndash821 (2016) doi 101126scienceaad6351pmid 27174985

47 A Ozgul et al Coupled dynamics of body mass andpopulation growth in response to environmental changeNature 466 482ndash485 (2010) doi 101038nature09210pmid 20651690

48 Y Yom-Tov S Yom-Tov G Jarrell Recent increase in bodysize of the American marten Martes americana in Alaska BiolJ Linn Soc Lond 93 701ndash707 (2008) doi 101111j1095-8312200700950x

49 G R Guerin H Wen A J Lowe Leaf morphology shiftlinked to climate change Biol Lett 8 882ndash886 (2012)doi 101098rsbl20120458 pmid 22764114

50 A Roulin Melanin-based colour polymorphism respondingto climate change Glob Change Biol 20 3344ndash3350(2014) doi 101111gcb12594 pmid 24700793

51 D Zeuss R Brandl M Braumlndle C Rahbek S BrunzelGlobal warming favours light-coloured insects in EuropeNat Commun 5 3874 (2014) doi 101038ncomms4874pmid 24866819

52 J G Kingsolver L B Buckley Climate variability slowsevolutionary responses of Colias butterflies to recent climatechange Proc Biol Sci 282 20142470 (2015) doi 101098rspb20142470 pmid 25631995

53 P Karell K Ahola T Karstinen J Valkama J E BrommerClimate change drives microevolution in a wild birdNat Commun 2 208 (2011) doi 101038ncomms1213pmid 21343926

54 R E Walsh et al Morphological and dietary responses ofchipmunks to a century of climate change Glob Chang Biol(2016) doi 101111gcb13216

55 M E Visser C Both Shifts in phenology due to globalclimate change the need for a yardstick Proc R SocB Biol Sci 272 2561ndash2569 (2005)

56 C Reacutezouki et al Socially mediated effects of climate changedecrease survival of hibernating Alpine marmots J AnimEcol 85 761ndash773 (2016) doi 1011111365-265612507pmid 26920650

57 T L Root et al Fingerprints of global warming on wildanimals and plants Nature 421 57ndash60 (2003) doi 101038nature01333 pmid 12511952

58 M Reyes-Fox et al Elevated CO2 further lengthens growingseason under warming conditions Nature 510 259ndash262(2014) doi 101038nature13207 pmid 24759322

59 R Buitenwerf L Rose S I Higgins Three decades ofmulti-dimensional change in global leaf phenology Nat ClimChang 5 364ndash368 (2015) doi 101038nclimate2533

60 M Winder D E Schindler Climate change uncouplestrophic interactions in an aquatic ecosystem Ecology 852100ndash2106 (2004) doi 10189004-0151

61 R G Asch Climate change and decadal shifts in thephenology of larval fishes in the California Currentecosystem Proc Natl Acad Sci USA 112 E4065ndashE4074(2015) doi 101073pnas1421946112 pmid 26159416

62 P O Dunn A P Moslashller Changes in breeding phenologyand population size of birds J Anim Ecol 83 729ndash739(2014) doi 1011111365-265612162 pmid 24117440

63 P Gienapp R Leimu J Merila Responses to climatechange in avian migration timendashMicroevolution versusphenotypic plasticity Clim Res 35 25ndash35 (2007)doi 103354cr00712

aaf7671-8 11 NOVEMBER 2016 bull VOL 354 ISSUE 6313 sciencemagorg SCIENCE

RESEARCH | REVIEW

on

Nov

embe

r 10

201

6ht

tp

scie

nce

scie

ncem

ago

rg

Dow

nloa

ded

from

64 A H Hurlbert Z Liang Spatiotemporal variation in avianmigration phenology Citizen science reveals effects ofclimate change PLOS ONE 7 e31662 (2012) doi 101371journalpone0031662 pmid 22384050

65 S E Travers et al Climate change and shifting arrival date ofmigratory birds over a century in the northern Great PlainsWilson J Ornithol 127 43ndash51 (2015) doi 10167614-0331

66 C Ramp J Delarue P J Palsboslashll R Sears P S HammondAdapting to a warmer oceanmdashSeasonal shift of baleen whalemovements over three decades PLOS ONE 10 e0121374(2015) doi 101371journalpone0121374 pmid 25785462

67 B D Todd D E Scott J H K Pechmann J W GibbonsClimate change correlates with rapid delays and advancementsin reproductive timing in an amphibian community Proc RSoc B Biol Sci 278 2191ndash2197 (2011)

68 A A Walpole J Bowman D C Tozer D S BadzinskiCommunity-level response to climate change Shifts inanuran calling phenology Herpetol Conserv Biol 7 249ndash257(2012)

69 A B Phillimore J D Hadfield O R Jones R J SmithersDifferences in spawning date between populations ofcommon frog reveal local adaptation Proc Natl AcadSci USA 107 8292ndash8297 (2010) doi 101073pnas0913792107 pmid 20404185

70 L E Chambers et al Phenological changes in the southernhemisphere PLOS ONE 8 e75514 (2013) doi 101371journalpone0075514 pmid 24098389

71 E S Poloczanska et al Responses of marine organisms toclimate change across oceans Front Mar Sci 3 1ndash21(2016) doi 103389fmars201600062

72 T Wernberg et al Seaweed communities in retreat fromocean warming Curr Biol 21 1828ndash1832 (2011)doi 101111j1365-2486201202656x

73 A C Baker P W Glynn B Riegl Climate change and coralreef bleaching An ecological assessment of long-termimpacts recovery trends and future outlook Estuar CoastShelf Sci 80 435ndash471 (2008) doi 101016jecss200809003

74 K L Laidre et al Arctic marine mammal population statussea ice habitat loss and conservation recommendations forthe 21st century Conserv Biol 29 724ndash737 (2015)doi 101111cobi12474 pmid 25783745

75 M A LaRue et al Climate change winners Receding icefields facilitate colony expansion and altered dynamics in anAdeacutelie penguin metapopulation PLOS ONE 8 e60568 (2013)doi 101371journalpone0060568 pmid 23573267

76 D J Isaak et al Effects of climate change and wildfire onstream temperatures and salmonid thermal habitat in amountain river network Ecol Appl 20 1350ndash1371 (2010)doi 10189009-08221 pmid 20666254

77 C Cianfrani H F Satizaacutebal C Randin A spatial modellingframework for assessing climate change impacts onfreshwater ecosystems Response of brown trout (Salmotrutta L) biomass to warming water temperature Ecol Modell313 1ndash12 (2015) doi 101016jecolmodel201506023

78 E G Martins et al Effects of river temperature andclimate warming on stock‐specific survival of adultmigrating Fraser River sockeye salmon (Oncorhynchusnerka) Glob Change Biol 17 99ndash114 (2011)doi 101111j1365-2486201002241x

79 B Ginn M Rate B Cumming J Smol Ecologicaldistribution of scaled-chrysophyte assemblages from thesediments of 54 lakes in Nova Scotia and southernNew Brunswick Canada J Paleolimnol 43 293ndash308 (2010)doi 101007s10933-009-9332-9

80 R D Gregory et al An indicator of the impact of climaticchange on European bird populations PLOS ONE 4e4678 (2009) doi 101371journalpone0004678pmid 19259270

81 L Munson et al Climate extremes promote fatal co-infectionsduring canine distemper epidemics in African lions PLOSONE 3 e2545 (2008) doi 101371journalpone0002545pmid 18575601

82 C J Randall R van Woesik Contemporary white-banddisease in Caribbean corals driven by climate change NatClim Chang 5 375ndash379 (2015) doi 101038nclimate2530

83 C Tayleur et al Swedish birds are tracking temperaturebut not rainfall Evidence from a decade of abundancechanges Glob Ecol Biogeogr 24 859ndash872 (2015)doi 101111geb12308

84 A Lehikoinen R Virkkala North by north-west Climatechange and directions of density shifts in birdsGlob Change Biol 22 1121ndash1129 (2016) doi 101111gcb13150 pmid 26691578

85 M T Burrows et al The pace of shifting climate in marineand terrestrial ecosystems Science 334 652ndash655 (2011)doi 101126science1210288 pmid 22053045

86 H Yamano K Sugihara K Nomura Rapid poleward rangeexpansion of tropical reef corals in response to rising seasurface temperatures Geophys Res Lett 38 1ndash6 (2011)doi 1010292010GL046474

87 N R Pitt E S Poloczanska A J Hobday Climate-drivenrange changes in Tasmanian intertidal fauna Mar FreshwRes 61 963ndash970 (2010) doi 101071MF09225

88 K M Alofs D Jackson N P Lester Ontario freshwaterfishes demonstrate differing range-boundary shifts ina warming climate Divers Distrib 20 123ndash136 (2014)doi 101111ddi12130

89 L Comte G Grenouillet Do stream fish track climatechange Assessing distribution shifts in recent decadesEcography 36 1236ndash1246 (2013) doi 101111j1600-0587201300282x

90 A Vergeacutes et al The tropicalization of temperate marineecosystems climate-mediated changes in herbivory andcommunity phase shifts Proc R Soc B Biol Sci 28120140846 (2014)

91 M Fossheim et al Recent warming leads to a rapidborealization of fish communities in the Arctic Nat ClimChang 5 673ndash677 (2015) doi 101038nclimate2647

92 B Elmhagen J Kindberg P Hellstroumlm A AngerbjoumlrnA boreal invasion in response to climate change Rangeshifts and community effects in the borderland betweenforest and tundra Ambio 44 (suppl 1) S39ndashS50 (2015)doi 101007s13280-014-0606-8 pmid 25576279

93 B G Freeman A M Class Freeman Rapid upslope shifts inNew Guinean birds illustrate strong distributional responsesof tropical montane species to global warming Proc NatlAcad Sci USA 111 4490ndash4494 (2014) doi 101073pnas1318190111 pmid 24550460

94 A Wolf N B Zimmerman W R L Anderegg P E BusbyJ Christensen Altitudinal shifts of the native and introducedflora of California in the context of 20th-century warmingGlob Ecol Biogeogr 25 418ndash429 (2016) doi 101111geb12423

95 I-C Chen et al Elevation increases in moth assemblagesover 42 years on a tropical mountain Proc Natl AcadSci USA 106 1479ndash1483 (2009) doi 101073pnas0809320106 pmid 19164573

96 I-C Chen J K Hill R Ohlemuumlller D B Roy C D ThomasRapid range shifts of species associated with high levelsof climate warming Science 333 1024ndash1026 (2011)doi 101126science1206432 pmid 21852500

97 E Kuhn J Lenoir C Piedallu J-C Geacutegout Early signs ofrange disjunction of sub‐mountainous plant species anunexplored consequence of future and contemporary climatechanges Glob Chang Biol 22 2094ndash2105 (2016)

98 J Savage M Vellend Elevational shifts biotic homogenizationand time lags in vegetation change during 40 years ofclimate warming Ecography 38 546ndash555 (2015)doi 101111ecog01131

99 G Forero-Medina J Terborgh S J Socolar S L PimmElevational ranges of birds on a tropical montane gradientlag behind warming temperatures PLOS ONE 6 e28535(2011) doi 101371journalpone0028535 pmid 22163309

100 F A La Sorte W Jetz Tracking of climatic nicheboundaries under recent climate change J Anim Ecol 81914ndash925 (2012) doi 101111j1365-2656201201958xpmid 22372840

101 P De Frenne et al Microclimate moderates plant responsesto macroclimate warming Proc Natl Acad Sci USA110 18561ndash18565 (2013) doi 101073pnas1311190110pmid 24167287

102 B R Scheffers D P Edwards A Diesmos S E WilliamsT A Evans Microhabitats reduce animalrsquos exposure toclimate extremes Glob Change Biol 20 495ndash503 (2014)doi 101111gcb12439 pmid 24132984

103 C M McCain R K Colwell Assessing the threat to montanebiodiversity from discordant shifts in temperature andprecipitation in a changing climate Ecol Lett 14 1236ndash1245(2011) doi 101111j1461-0248201101695xpmid 21981631

104 S M Crimmins S Z Dobrowski J A GreenbergJ T Abatzoglou A R Mynsberge Changes in climaticwater balance drive downhill shifts in plant speciesrsquo optimumelevations Science 331 324ndash327 (2011) doi 101126science1199040 pmid 21252344

105 J E Jankowski S K Robinson D J Levey Squeezedat the top Interspecific aggression may constrain elevational

ranges in tropical birds Ecology 91 1877ndash1884 (2010)doi 10189009-20631 pmid 20715605

106 J G Molinos et al Climate velocity and the future globalredistribution of marine biodiversity Nat Clim Chang101038nclimate2769 (2015) doi 101038nclimate2769

107 E Cahill et al How does climate change cause extinctionProc R Soc B Biol Sci (2012) doi 101098rspb20121890

108 N Ockendon et al Mechanisms underpinning climaticimpacts on natural populations Altered species interactionsare more important than direct effects Glob Change Biol 202221ndash2229 (2014) doi 101111gcb12559 pmid 24677405

109 M W Tingley S R Beissinger Cryptic loss of montane avianrichness and high community turnover over 100 yearsEcology 94 598ndash609 (2013) doi 10189012-09281pmid 23687886

110 V Sgardeli K Zografou J M Halley Climate Changeversus Ecological Drift Assessing 13 years of turnover in abutterfly community Basic Appl Ecol 17 283ndash290 (2016)doi 101016jbaae201512008

111 T Wittwer R B OrsquoHara P Caplat T Hickler H G SmithLong‐term population dynamics of a migrant birdsuggests interaction of climate change and competitionwith resident species Oikos 124 1151ndash1159 (2015)doi 101111oik01559

112 S Bennett T Wernberg E S Harvey J Santana-GarconB J Saunders Tropical herbivores provide resilience to aclimate-mediated phase shift on temperate reefs Ecol Lett18 714ndash723 (2015) doi 101111ele12450 pmid 25994785

113 C Parmesan et al Beyond climate change attribution inconservation and ecological research Ecol Lett 16 (suppl 1)58ndash71 (2013) doi 101111ele12098 pmid 23679010

114 A Millon et al Dampening prey cycle overrides the impactof climate change on predator population dynamicsA long-term demographic study on tawny owls Glob ChangeBiol 20 1770ndash1781 (2014) doi 101111gcb12546pmid 24634279

115 J R Thienpont et al Recent climate warming favours morespecialized cladoceran taxa in western Canadian Arctic lakesJ Biogeogr 42 1553ndash1565 (2015) doi 101111jbi12519

116 T Jonsson M Setzer A freshwater predator hit twice by theeffects of warming across trophic levels Nat Commun 65992 (2015) doi 101038ncomms6992 pmid 25586020

117 M Steinacher et al Projected 21st century decrease inmarine productivity A multi-model analysis Biogeosciences7 979ndash1005 (2010) doi 105194bg-7-979-2010

118 F Hofhansl J Kobler S Drage E Poumllz W Wanek Sensitivityof tropical lowland net primary production to climateanomalies EGU Gen Assem Conf Abstr 16 10585(2014)

119 G C Hays A J Richardson C Robinson Climatechange and marine plankton Trends Ecol Evol 20337ndash344 (2005) doi 101016jtree200503004pmid 16701390

120 D G Boyce M R Lewis B Worm Global phytoplanktondecline over the past century Nature 466 591ndash596 (2010)doi 101038nature09268 pmid 20671703

121 M Montes-Hugo et al Recent changes in phytoplanktoncommunities associated with rapid regional climatechange along the western Antarctic Peninsula Science323 1470ndash1473 (2009) doi 101126science1164533pmid 19286554

122 C M OrsquoReilly S R Alin P D Plisnier A S CohenB A McKee Climate change decreases aquatic ecosystemproductivity of Lake Tanganyika Africa Nature 424766ndash768 (2003) doi 101038nature01833pmid 12917682

123 H Sarmento A M Amado J-P Descy Climate change intropical fresh waters (comment on the paper Planktondynamics under different climatic conditions in space andtime by de Senerpont Domis et al 2013) Freshw Biol 582208ndash2210 (2013) doi 101111fwb12140

124 B Moss et al Allied attack Climate change and eutrophicationInland Waters 1 101ndash105 (2011) doi 105268IW-12359

125 R R Nemani et al Climate-driven increases in globalterrestrial net primary production from 1982 to 1999 Science300 1560ndash1563 (2003) doi 101126science1082750pmid 12791990

126 A Bastos S W Running C Gouveia R M Trigo The globalNPP dependence on ENSO La Nintildea and the extraordinaryyear of 2011 J Geophys Res Biogeosci 118 1247ndash1255(2013) doi 101002jgrg20100

127 S Saatchi et al Persistent effects of a severe drought onAmazonian forest canopy Proc Natl Acad Sci USA

SCIENCE sciencemagorg 11 NOVEMBER 2016 bull VOL 354 ISSUE 6313 aaf7671-9

RESEARCH | REVIEW

on

Nov

embe

r 10

201

6ht

tp

scie

nce

scie

ncem

ago

rg

Dow

nloa

ded

from

110 565ndash570 (2013) doi 101073pnas1204651110pmid 23267086

128 L Zhou et al Widespread decline of Congo rainforestgreenness in the past decade Nature 509 86ndash90 (2014)doi 101038nature13265 pmid 24759324

129 R J W Brienen et al Long-term decline of the Amazoncarbon sink Nature 519 344ndash348 (2015) doi 101038nature14283 pmid 25788097

130 N A J Graham S Jennings M A MacNeil D MouillotS K Wilson Predicting climate-driven regime shifts versusrebound potential in coral reefs Nature 518 94ndash97 (2015)doi 101038nature14140 pmid 25607371

131 S D Ling C R Johnson S D Frusher K R RidgwayOverfishing reduces resilience of kelp beds to climate-drivencatastrophic phase shift Proc Natl Acad Sci USA 10622341ndash22345 (2009) doi 101073pnas0907529106pmid 20018706

132 T Wernberg et al Climate-driven regime shift of a temperatemarine ecosystem Science 353 169ndash172 (2016)doi 101126scienceaad8745 pmid 27387951

133 P S A Beck et al Changes in forest productivity acrossAlaska consistent with biome shift Ecol Lett 14 373ndash379(2011) doi 101111j1461-0248201101598xpmid 21332901

134 J Gao B Barzel A-L Barabaacutesi Universal resiliencepatterns in complex networks Nature 530 307ndash312 (2016)doi 101038nature16948 pmid 26887493

135 FAO The State of World Fisheries and Aquaculture(Rome 2014)

136 P Wassmann C M Duarte S Agusti M K SejrFootprints of climate change in the Arctic marineecosystem Glob Change Biol 17 1235ndash1249 (2011)doi 101111j1365-2486201002311x

137 A B Hollowed B Planque H Loeng Potential movementof fish and shellfish stocks from the sub-Arctic to theArctic Ocean Fish Oceanogr 22 355ndash370 (2013)doi 101111fog12027

138 M M McBride et al Krill climate and contrasting futurescenarios for Arctic and Antarctic fisheries ICES JMar Sci J du Cons 71 1932ndash1933 (2014)doi 101093icesjmsfsu002

139 M J Genner et al Body size‐dependent responses of amarine fish assemblage to climate change and fishing over acentury‐long scale Glob Change Biol 16 517ndash527 (2010)doi 101111j1365-2486200902027x

140 A R Baudron C L Needle A D Rijnsdorp C T MarshallWarming temperatures and smaller body sizes Synchronouschanges in growth of North Sea fishes Glob Change Biol20 1023ndash1031 (2014) doi 101111gcb12514pmid 24375891

141 M Daufresne K Lengfellner U Sommer Global warmingbenefits the small in aquatic ecosystems Proc NatlAcad Sci USA 106 12788ndash12793 (2009) doi 101073pnas0902080106 pmid 19620720

142 E Jeppesen et al Impacts of climate warming on the long-term dynamics of key fish species in 24 European lakesHydrobiologia 694 1ndash39 (2012) doi 101007s10750-012-1182-1

143 S Peng et al Rice yields decline with higher night temperaturefrom global warming Proc Natl Acad Sci USA 1019971ndash9975 (2004) doi 101073pnas0403720101pmid 15226500

144 J R Porter et al in Climate Change 2014 ImpactsAdaptation and Vulnerability Part A Global and SectoralAspects Contribution of Working Group II to the FifthAssessment Report of the Intergovernmental Panel of ClimateChange C B Field et al Eds (Cambridge Univ Press 2014)pp 485ndash533

145 C W Craparo P J Van Asten P Laumlderach L T P JassogneS W Grab Coffea arabica yields decline in Tanzania due toclimate change Global implications Agric For Meteorol 2071ndash10 (2015) doi 101016jagrformet201503005

146 D B Lobell W Schlenker J Costa-Roberts Climatetrends and global crop production since 1980 Science333 616ndash620 (2011) doi 101126science1204531pmid 21551030

147 J A Hamilton J M Miller Adaptive introgression as aresource for management and genetic conservationin a changing climate Conserv Biol 30 33ndash41 (2016)doi 101111cobi12574 pmid 26096581

148 E Nevo et al Evolution of wild cereals during 28 yearsof global warming in Israel Proc Natl Acad Sci USA109 3412ndash3415 (2012) doi 101073pnas1121411109pmid 22334646

149 P Stratonovitch M A Semenov Heat tolerance aroundflowering in wheat identified as a key trait for increasedyield potential in Europe under climate change J Exp Bot66 3599ndash3609 (2015) doi 101093jxberv070pmid 25750425

150 S N Aitken M C Whitlock Assisted gene flow to facilitatelocal adaptation to climate change Annu Rev Ecol EvolSyst 44 367ndash388 (2013) doi 101146annurev-ecolsys-110512-135747

151 M J H van Oppen J K Oliver H M Putnam R D GatesBuilding coral reef resilience through assisted evolutionProc Natl Acad Sci USA 112 2307ndash2313 (2015)doi 101073pnas1422301112 pmid 25646461

152 B Zheng K Chenu S C Chapman Velocity of temperatureand flowering time in wheatmdashAssisting breeders to keeppace with climate change Glob Change Biol 22 921ndash933(2016) doi 101111gcb13118 pmid 26432666

153 E Luedeling J Gebauer A Buerkert Climate change effectson winter chill for tree crops with chilling requirementson the Arabian Peninsula Clim Change 96 219ndash237 (2009)doi 101007s10584-009-9581-7

154 J X Chaparro W B Shermain Peach tree named ldquoUFBestrdquo(2014) wwwgooglecompatentsUSPP25129

155 T Sugiura H Sumida S Yokoyama H Ono Overview ofrecent effects of global warming on agricultural productionin Japan Jpn Agric Res Q 46 7ndash13 (2012)doi 106090jarq467

156 J T Kerr et al Climate change impacts on bumblebeesconverge across continents Science 349 177ndash180 (2015)pmid 26160945

157 L A Burkle J C Marlin T M Knight Plant-pollinatorinteractions over 120 years Loss of species co-occurrenceand function Science 339 1611ndash1615 (2013) doi 101126science1232728 pmid 23449999

158 I Bartomeus et al Historical changes in northeastern US beepollinators related to shared ecological traits Proc NatlAcad Sci USA 110 4656ndash4660 (2013) doi 101073pnas1218503110 pmid 23487768

159 R Rader J Reilly I Bartomeus R Winfree Native beesbuffer the negative impact of climate warming on honeybee pollination of watermelon crops Glob Change Biol19 3103ndash3110 (2013) doi 101111gcb12264pmid 23704044

160 W A Kurz et al Mountain pine beetle and forest carbonfeedback to climate change Nature 452 987ndash990 (2008)doi 101038nature06777 pmid 18432244

161 W R L Anderegg J M Kane L D L AndereggConsequences of widespread tree mortality triggered bydrought and temperature stress Nat Clim Chang 3 30ndash36(2013) doi 101038nclimate1635

162 L A Bearup R M Maxwell D W Clow J E MccrayHydrological effects of forest transpiration loss in barkbeetle-impacted watersheds Nat Clim Chang 4 481ndash486(2014) doi 101038nclimate2198

163 A S Weed M P Ayres J A Hicke Consequences ofclimate change for biotic disturbances in NorthAmerican forests Ecol Monogr 83 441ndash470 (2013)doi 10189013-01601

164 D P Bebber M T Ramotowski S J Gurr Crop pestsand pathogens move polewards in a warming worldNat Clim Chang 3 985ndash988 (2013) doi 101038nclimate1990

165 S Altizer R S Ostfeld P T J Johnson S Kutz C D HarvellClimate change and infectious diseases From evidenceto a predictive framework Science 341 514ndash519 (2013)pmid 23908230

166 S Paz N Bisharat E Paz O Kidar D Cohen Climatechange and the emergence of Vibrio vulnificus disease inIsrael Environ Res 103 390ndash396 (2007) doi 101016jenvres200607002 pmid 16949069

167 C Baker-Austin et al Emerging Vibrio risk at high latitudes inresponse to ocean warming Nat Clim Chang 3 73ndash77(2012) doi 101038nclimate1628

168 A Egizi N H Fefferman D M Fonseca Evidence thatimplicit assumptions of lsquono evolutionrsquo of disease vectorsin changing environments can be violated on a rapidtimescale Philos Trans R Soc Lond B Biol Sci370 20140136 (2015) doi 101098rstb20140136pmid 25688024

169 T Levi F Keesing K Oggenfuss R S Ostfeld Acceleratedphenology of blacklegged ticks under climate warmingPhilos Trans R Soc London B Biol Sci 370 20130556(2015) pmid 25688016

170 E Mcleod et al A blueprint for blue carbon Toward animproved understanding of the role of vegetated coastalhabitats in sequestering CO2 Front Ecol Environ 9 552ndash560(2011) doi 101890110004

171 R A Pielke Sr et al Land useland cover changes andclimate Modeling analysis and observational evidenceWiley Interdiscip Rev Clim Chang 2 828ndash850 (2011)doi 101002wcc144

172 K McKinnon V Hickey Convenient solutions to aninconvenient truth Ecosystem-based approaches to climatechange Int Bank Reconstr Dev World Bank 2 (2009)

173 F Ferrario et al The effectiveness of coral reefs for coastalhazard risk reduction and adaptation Nat Commun5 3794 (2014) doi 101038ncomms4794pmid 24825660

174 S Temmerman et al Ecosystem-based coastal defencein the face of global change Nature 504 79ndash83 (2013)doi 101038nature12859 pmid 24305151

175 C J A Bradshaw N S Sodhi K S Peh B W Brook Globalevidence that deforestation amplifies flood risk and severityin the developing world Glob Change Biol 13 2379ndash2395(2007) doi 101111j1365-2486200701446x

176 S L Maxwell O Venter K R Jones J E M WatsonIntegrating human responses to climate change intoconservation vulnerability assessments and adaptationplanning Ann N Y Acad Sci 1355 98ndash116 (2015)doi 101111nyas12952 pmid 26555860

177 C M Sgrograve A J Lowe A A Hoffmann Building evolutionaryresilience for conserving biodiversity under climate changeEvol Appl 4 326ndash337 (2011) doi 101111j1752-4571201000157x pmid 25567976

178 D G Hole et al Projected impacts of climate change on acontinent-wide protected area network Ecol Lett 12420ndash431 (2009) doi 101111j1461-0248200901297xpmid 19379136

179 B E Miner L De Meester M E Pfrender W LampertN G Hairston Jr Linking genes to communities andecosystems Daphnia as an ecogenomic model Proc BiolSci 279 1873ndash1882 (2012) doi 101098rspb20112404pmid 22298849

180 W Van Doorslaer R Stoks C Duvivier A BednarskaL De Meester Population dynamics determine geneticadaptation to temperature in Daphnia Evolution 631867ndash1878 (2009) doi 101111j1558-5646200900679xpmid 19473405

181 W Van Doorslaer et al Experimental thermal microevolutionin community-embedded Daphnia populations Clim Res 4381ndash89 (2010) doi 103354cr00894

182 B Zeis D Becker P Gerke M Koch R J PaulHypoxia-inducible haemoglobins of Daphnia pulex andtheir role in the response to acute and chronictemperature increase Biochim Biophys Acta 18341704ndash1710 (2013) doi 101016jbbapap201301036pmid 23388388

183 R J Paul et al Thermal acclimation in the microcrustaceanDaphnia A survey of behavioural physiological andbiochemical mechanisms J Therm Biol 29 655ndash662(2004) doi 101016jjtherbio200408035

184 W van Doorslaer et al Local adaptation to highertemperatures reduces immigration success of genotypesfrom a warmer region in the water flea Daphnia Glob ChangeBiol 15 3046ndash3055 (2009) doi 101111j1365-2486200901980x

185 D Straile R Adrian D E Schindler Uniform temperaturedependency in the phenology of a keystone herbivore in lakesof the Northern Hemisphere PLOS ONE 7 e45497(2012) doi 101371journalpone0045497 pmid 23071520

186 T Blenckner et al Large‐scale climatic signatures inlakes across Europe A meta‐analysis Glob Change Biol13 1314ndash1326 (2007) doi 101111j1365-2486200701364x

187 F Altermatt V I Pajunen D Ebert Climate changeaffects colonization dynamics in a metacommunity ofthree Daphnia species Glob Change Biol 14 1209ndash1220(2008) doi 101111j1365-2486200801588x

188 M De Block K Pauwels M Van Den Broeck L De MeesterR Stoks Local genetic adaptation generates latitude-specificeffects of warming on predator-prey interactions GlobChange Biol 19 689ndash696 (2013) doi 101111gcb12089pmid 23504827

189 S R Hall A J Tessier M A Duffy M Huebner C E CaacuteceresWarmer does not have to mean sicker Temperature andpredators can jointly drive timing of epidemics Ecology 87

aaf7671-10 11 NOVEMBER 2016 bull VOL 354 ISSUE 6313 sciencemagorg SCIENCE

RESEARCH | REVIEW

on

Nov

embe

r 10

201

6ht

tp

scie

nce

scie

ncem

ago

rg

Dow

nloa

ded

from

1684ndash1695 (2006) doi 1018900012-9658(2006)87[1684WDNHTM]20CO2 pmid 16922319

190 H Feuchtmayr et al Differential effects of warmingand nutrient loading on the timing and size of the springzooplankton peak An experimental approach withhypertrophic freshwater mesocosms J Plankton Res 321715ndash1725 (2010) doi 101093planktfbq087

191 S J Franks A E Weis A change in climate causesrapid evolution of multiple life-history traits and theirinteractions in an annual plant J Evol Biol 211321ndash1334 (2008) doi 101111j1420-9101200801566xpmid 18557796

ACKNOWLEDGMENTS

We thank the Intergovernmental Panel on Climate ChangeIntergovernmental Platform on Biodiversity and Ecosystem Servicesand the thousands of researchers that have studied biodiversityand ecosystem services and the impacts of climate change onEarthmdashmany of whom we were not able to cite because of lengthrestrictions of the journal S Greenspan J Greenspan and E Perryprovided helpful discussion and feedback on this manuscript S Jonesand M Wood were instrumental in figure creation LDM acknowledgesKU Leuven Research Fund PF201007 and Future Earth core projectBioGENESIS We thank the International Union for Conservation ofNature Climate Change Specialist Group for collaborative discussions

on climate change themes and impacts on conservation ofspecies and ecosystems and three anonymous reviewers forconstructive suggestions that improved our manuscript

SUPPLEMENTARY MATERIALS

wwwsciencemagorgcontent3546313aaf7671supplDC1Supplementary TextFig S1Table S1References (192ndash310)

101126scienceaaf7671

SCIENCE sciencemagorg 11 NOVEMBER 2016 bull VOL 354 ISSUE 6313 aaf7671-11

RESEARCH | REVIEW

on

Nov

embe

r 10

201

6ht

tp

scie

nce

scie

ncem

ago

rg

Dow

nloa

ded

from

(6313) [doi 101126scienceaaf7671]354Science (November 10 2016) Martin Camilo Mora David Bickford and James E M WatsonMichela Pacifici Carlo Rondinini Wendy B Foden Tara G Butchart Paul Pearce-Kelly Kit M Kovacs David DudgeonHoffmann John M Pandolfi Richard T Corlett Stuart H M Brett R Scheffers Luc De Meester Tom C L Bridge Ary ApeopleThe broad footprint of climate change from genes to biomes to

Editors Summary

this issue p 101126scienceaaf7671 Sciencewe move forward into a warming worldUnderstanding the causes consequences and potential mitigation of these changes will be essential asacross genes species and ecosystems to reveal a world already undergoing substantial change

review the set of impacts that have been observedet aland being amplified more broadly Scheffers the changing climate that are particular to species or regions but individual impacts are accumulating

ofhaving increased by 1degC from preindustrial levels Many studies have documented individual impacts Anthropogenic climate change is now in full swing our global average temperature already

Accumulating impacts

This copy is for your personal non-commercial use only

Article Tools

httpsciencesciencemagorgcontent3546313aaf7671article tools Visit the online version of this article to access the personalization and

PermissionshttpwwwsciencemagorgaboutpermissionsdtlObtain information about reproducing this article

is a registered trademark of AAAS ScienceAdvancement of Science all rights reserved The title Avenue NW Washington DC 20005 Copyright 2016 by the American Association for thein December by the American Association for the Advancement of Science 1200 New York

(print ISSN 0036-8075 online ISSN 1095-9203) is published weekly except the last weekScience

on

Nov

embe

r 10

201

6ht

tp

scie

nce

scie

ncem

ago

rg

Dow

nloa

ded

from