Ecological and Evolutionary Responses to Recent Climate Change

Ecological and Evolutionary Responses to Recent Climate Change Author(s): Camille Parmesan Reviewed work(s): Source: Annual Review of Ecology, Evolution, and Systematics, Vol. 37 (2006), pp. 637-669 Published by: Annual Reviews Stable URL: http://www.jstor.org/stable/30033846 . Accessed: 25/10/2012 11:39

Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp

. JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected].

Annual Reviews is collaborating with JSTOR to digitize, preserve and extend access to Annual Review of Ecology, Evolution, and Systematics.

http://www.jstor.org Ecologicaland Evolutionary Responsesto Recent ClimateChange CamilleParmesan Sectionof Integrative Biology, University ofTexas, Austin, Texas 78712; email:[email protected]

Annu.Rev. Ecol. Evol. Syst.2006. 37:637-69 Key Words First onlineas a Reviewin Advance published aquatic,global warming, phenology, range shift, terrestrial, trophic on August24, 2006 asynchrony The AnnualReview of Ecology, Evolution, and Systematicsis online at Abstract http://ecolsys.annualreviews.org in the and distributionof and This article'sdoi: Ecological changes phenology plants animals are in all well-studied and 10.2307/annurev.ecolsys.37.091305.30000024 occurring marine,freshwater, terrestrialgroups. These observedchanges are heavilybiased in the @ 2006 AnnualReviews. Copyright by directions from and have been linkedto All rightsreserved predicted global warming local or climate correlationsbetween cli- 1543-592X/06/1201-0637$20.00 regional changethrough mateand biologicalvariation, field and laboratoryexperiments, and physiologicalresearch. Range-restricted species, particularly polar and mountaintopspecies, show severerange contractions and have been the firstgroups in whichentire species have gone extinctdue to recentclimate change. Tropical coral reefsand amphibianshave been mostnegatively affected. Predator-prey and plant-insectinter- actionshave been disruptedwhen interacting species have responded differentlyto warming.Evolutionary adaptations to warmercondi- tionshave occurredin theinteriors of species'ranges, and resource use and dispersalhave evolvedrapidly at expandingrange margins. Observedgenetic shifts modulate local effectsof climate change, but thereis littleevidence that they will mitigatenegative effects at the specieslevel.

637 INTRODUCTION

HistoricalPerspective Climatechange is not a new topicin biology.The studyof biological impacts of climatechange has a richhistory in thescientific literature, since long beforethere were politicalramifications. Grinnell (1917) firstelucidated the role ofclimatic thresholds in constrainingthe geographic boundaries of many species, followed by major works byAndrewartha & Birch(1954) and MacArthur(1972). Observationsof range shifts in parallelwith climatechange have been particularlyrich in northernEuropean countries,where observational records for many birds, butterflies, herbs, and trees dateback to themid-1700s. Since the early part of the twentieth century, researchers have documentedthe sensitivityof insects to springand summertemperatures (Bale et al. 2002, Dennis 1993, Uvarov 1931). Ford (1945) describednorthward range shiftsof severalbutterflies in England,attributing these shiftsto a summerwarm- ing trendthat began around 1915 in Britain.Ford noted thatone of thesespecies, Limenitiscamilla, expanded to occupyan area whereattempted introductions prior to thewarming had failed.Kaisila (1962) independentlydocumented range shifts of Lepidoptera(primarily moths) in Finland,using historical data on rangeboundaries datingback to 1760.He showedrepeated instances of southward contractions during decades of "harsh"climatic conditions (cold wet summers),followed by northward range expansionduring decades withclimate "amelioration" (warm summers and lack of extremecold in winter).Further corroboration came fromthe strongcorre- lationsbetween summer temperatures and the northernrange boundaries for many butterflies(Dennis 1993). Similar databasesexist for northernEuropean birds.A burstof papers docu- mentedchanged abundances and northerlyrange shifts of birdsin Iceland,Finland, and Britainassociated with the 1930s-1940swarming period (Gudmundsson 1951; Harris 1964; Kalela 1949, 1952; Salomonsen1948). A secondwave of papersin the 1970sdescribed the subsequent retreats of many of these temperate bird and butterfly speciesfollowing the cool, wet period of the 1950s-1960s(Burton 1975, Heath 1974, Severnty1977, Williamson 1975). Complementingthis rich observational database is morethan 100 yearsof basic researchon theprocesses by which climate and extremeweather events affect plants and animals.As earlyas the 1890s,Bumpus (1899) notedthe differentialeffects of an extremewinter storm on the introducedhouse sparrow(Parus domesticus), resulting in stabilizingselection for intermediate body size in femalesand directionalselection forlarge body size in males (Johnstonet al. 1972). The firstextensive studies of cli- matevariability as a powerfuldriver of populationevolution date backto the 1940s, when Dobzhansky(1943, 1947) discoveredrepeated cycles of seasonal evolutionof temperature-associatedchromosomal inversions within Drosophila pseudoobscura pop- ulationsin responseto temperaturechanges from spring through summer. In summary,the historyof biologicalresearch is rich in both mechanisticand observationalstudies of the impactsof extremeweather and climate change on wild species: Research encompassesimpacts of single extremeweather events; experimentalstudies of physiologicaltolerances; snapshot correlationsbetween

638 Parmesan climaticvariables and species' distributions; and correlations through time between climatictrends and changes in distributions,phenologies, genetics, and behaviors of wildplants and animals. Detection:ability to discernlong-term trends above and Climate yearlyvariability Anthropogenic Change realchanges from apparent In spiteof this wealth of literature on thefundamental importance of climate to wild changesbrought about by havebeen reluctant to believe that modern changesin sampling biota,biologists (greenhousegas-driven) and/or climate is a causeof concern for In hisintroduction to the 1992 methodology change biodiversity. samplingintensity AnnualReview and volumeon "Global Environmental ofEcology,Evolution, Systematics Attribution: out Vitousek climate hasthe teasing Change," wrote,"ultimately, changeprobably greatestpo- climatechange as thecausal tentialto alter the functioning ofthe Earth system .... nevertheless,the major effects driverof an observed ofclimate change are mostly in thefuture while most of the others are already with biologicalchange amid a us."Individual authors in thatvolume tended to agree-paperswere predominantly backdrop of potential factors concernedwith other global change factors: land use change, nitrogen fertilization, confounding andthe direct effects of increased atmospheric CO2 on plantecophysiology. Globallycoherent: a commonterm in economics, Just14 years later, the direct impacts of anthropogenic climate change have been a processor event is globally documentedon every continent, inevery ocean, and in most major taxonomic groups coherentwhen it has similar (reviewedin Badeck et al. 2004;Hoegh-Guldberg 1999, 2005b; Hughes 2000; IPCC effectacross multiple 2001a; Parmesan2005b; Parmesan & Galbraith2004; Parmesan& Yohe 2003; systemsspread across Pefiuelas& Filella2001; Poundset al. 2005; Root & Hughes2005; Root et al. differentlocations theworld 2003; Sparks& Menzel2002; Thomas 2005; Walther et al. 2002,2005). The is- throughout sue ofwhether observed biological changes can be conclusivelylinked to anthropogenicclimate change has beenanalyzed and discussed at lengthin a plethoraof syntheses,including those listed above. Similarly, complexity surrounding method- ologicalissues of detection(correctly detecting a realtrend) and attribution(as- signingcausation) has been explored in depth(Ahmad et al. 2001;Dose & Menzel 2004;Parmesan 2002, 2005a,b; Parmesan & Yohe2003; Parmesan et al. 2000;Root et al. 2003,Root & Hughes2005, Schwartz 1998, 1999; Shoo et al. 2006).The consensusis that,with proper attention to samplingand otherstatistical issues andthrough the use ofscientific inference, studies of observed biological changes can providerigorous tests of climate-changehypotheses. In particular,indepen- dentsyntheses of studies worldwide have provided a clear, globally coherent conclu- sion:Twentieth-century anthropogenic global warming has already affected Earth's biota.

Scopeof This Review This reviewconcentrates on studiesof particularly long time series and/or partic- ularlygood mechanistic understanding of causes of observedchanges. It dealsex- clusivelywith observed responses of wild biological species and systems to recent, anthropogenicclimate change. In particular,agricultural impacts, human health, and ecosystem-levelresponses (e.g., carbon cycling) are not discussed. Because they have beenextensively dealt with in previous publications, this review does not repeat dis- cussionsof detection and attribution, nor of the conservation implications ofclimate

www.annualreviews.org* Climate-Change Impacts 639 change.Rather, some of the best-understood cases are presented to illustrate the com- plexways in which various facets of climatic change impact wild biota. The choiceof studiesfor illustration attempts to drawattention to thetaxonomic and geographic breadthof climate-change impacts and to the most-recent literature not already rep- resentedin prior reviews. Researchershave frequently associated biological processes with indices of ocean- atmospheredynamics, such as the El NifioSouthern Oscillation and theNorth AtlanticOscillation (Blenckner & Hillebrand2002, Holmgren et al. 2001,Ottersen etal. 2001).However, the nature of the relationship between atmospheric dynamics, oceancirculation, and temperature is changing (Alley et al. 2003,IPCC 2001b, Karl & Trenberth2003, Meehl et al. 2000).Therefore, there is large uncertainty as to how pastrelationships between biological systems and ocean indices reflect responses to ongoinganthropogenic climate change. Although I use individualexamples where appropriate,this complex topic is notfully reviewed here.

OVERVIEW OF IMPACTS LITERATURE Anextensive, but not exhaustive, literature search revealed 866 peer-reviewed papers thatdocumented changes through time in speciesor systemsthat could, in whole or in part,be attributedto climatechange. Some interesting broad patterns are revealed.Notably, the publication rate of climate-change responses increases sharply eachyear. The numberof publications between 1899 and January 2003 (the date of twomajor syntheses) was 528. Therefore, approximately 40% ofthe 866 papers com- piled forthis review were published in thepast three years (January 2003 toJanuary 2006). The studiesare spread broadly across taxonomic groups. Whereas distributional studiesconcentrated onanimals rather than plants, the reverse istrue of phenological timeseries. This may simply be becausehistorical data on speciesrange boundaries havehigher resolution for animals than for plants. Conversely, local records of spring eventsare muchmore numerous for plants (e.g., flowering and leaf out) than for animals(e.g., nesting). Althoughthere is stilla terrestrialbias, studies in marine and freshwater environ- mentsare increasing in proportional representation. The largestgaps are geographic ratherthan taxonomic. In absolutenumbers, most biological impact studies are from NorthAmerica, northern Europe and Russia. Few biological studies have come from SouthAmerica, and there are large holes in Africa and Asia, with most of the studies fromthese two continents coming from just two countries: South Africa and Japan. In pastdecades, Australia's impact studies have stemmed predominantly from the coral reefcommunity, but in recentyears scientists have dug deep to findhistorical data, andterrestrial impact studies are now emerging. Similarly, the Mediterranean/North Africanregion (Spain, France, Italy, and Israel) has recently spawned a spate of studies. Antarcticastands out as a regionwhere impacts (or lack of impacts) on mostspecies andsystems have been documented, even though data often have large geographic ortemporal gaps.

640 Parmesan Few studieshave been conductedat a scale thatencompasses an entirespecies' range (i.e., a continentalscale), withonly a moderatenumber at the regionalscale the United or Most have been conductedat local scales, (e.g., Kingdom Germany). Meta-analysis:set of typicallyat a researchstation or preserve.Continental-scale studies usually cover statisticaltechniques mostor all ofa species'range in terrestrialsystems (Both et al. 2004, Burton1998a,b, designedto synthesize Dunn & Winkler1999, Menzel & Fabian 1999, Parmesan 1996, Parmesanet al. quantitativeresults from 1999). However,even a continentalscale cannot encompassthe entireranges of similarand independent experiments manyoceanic species (Ainley& Divoky 1998, Ainleyet al. 2003, Beaugrandet al. 2002, Croxallet al. 2002, Hoegh-Gulberg1999, McGowan et al. 1998, Reid et al. 1998, Spear & Ainley1999). Terrestrialendemics, in contrast,can have such small rangesthat regional, or even local, studiesmay represent impacts on entirespecies (Pounds et al. 1999,2006).

Meta-Analysesand Syntheses:Globally Coherent Signalsof Climate-Change Impacts A handfulof studies have conductedstatistical meta-analyses of species' responses or havesynthesized independent studies to revealemergent patterns. The clearconclu- sion acrossglobal syntheses is thattwentieth-century anthropogenic global warming has alreadyaffected the Earth'sbiota (IPCC 2001a; Parmesan2005a,b; Parmesan & Galbraith2004; Parmesan& Yohe 2003; Pefiuelas& Filella 2001; Pounds et al. 2005; Root & Hughes 2005; Root et al. 2003; Thomas 2005; Waltheret al. 2002, 2005). One studyestimated that more than half (59%) of 1598 speciesexhibited measur- able changesin theirphenologies and/or distributions over the past 20 to 140 years (Parmesan& Yohe 2003). Analysesrestricted to speciesthat exhibited change documentedthat these changes were not random:They weresystematically and predom- inantlyin the directionexpected from regional changes in the climate(Parmesan & Yohe 2003, Root et al. 2003). Respondingspecies are spreadacross diverse ecosystems(from temperate grasslands to marineintertidal zones and tropicalcloud forests) and come froma wide varietyof taxonomicand functionalgroups, including birds, butterflies,alpine flowers, and coralreefs. A meta-analysisof range boundary changes in the Northern Hemisphere estimatedthat northern and upper elevationalboundaries had moved,on average, 6.1 km per decade northwardor 6.1 m per decade upward(P < 0.02) (Parmesan & Yohe 2003). Quantitativeanalyses of phenologicalresponses gave estimatesof advancementof 2.3 daysper decade acrossall species(Parmesan & Yohe 2003) and 5.1 daysper decade forthe subset of species showing substantive change (> 1 dayper decade) (Root et al. 2003). A surprisingresult is thehigh proportion of species responding to recent,relatively mild climatechange (global averagewarming of 0.60C). The proportionof wild speciesimpacted by climate change was estimatedat 41% of all species(655 of 1598) (Parmesan& Yohe 2003). This estimatewas derivedby focusingon multispecies studiesthat reported stable as well as respondingspecies. Because respondersand

www.annualreviews.org* Climate-Change Impacts 64I stablespecies were often sympatric, variation of response is notmerely a consequence of differentialmagnitudes of climatechange experienced.

PHENOLOGICAL CHANGES

By far,most observationsof climate-changeresponses have involvedalterations of species'phenologies. This is partlya resultof the tight links between the seasons and agriculture:Planting and harvestdates (and associatedclimatic events such as dayof last frost)have been well recorded,dating back hundredsof yearsfor some crops. But the plethoraof recordsalso stemsfrom the strongsociological significance of the changeof the seasons,particularly in high-latitudecountries. Peoples of Great Britain,the Netherlands,Sweden, and Finlandhave been keen on (some mightsay even obsessedwith) recording the firstsigns of spring-the firstleaf on an oak, the firstpeacock butterfly seen flying,the first crocus in bloom-as a markthat the long, darkwinter is finallyover. Fall has not capturedas muchenthusiasm as spring,but some good recordsexist, for example, for the turning of leaf color fortrees. The longestrecords of direct phenological observations are for flowering of cherry treesPrunusjamasakura and forgrape harvests.Menzel & Dose (2005) show that timingof cherryblossom in Japanwas highlyvariable among years,but no clear trendswere discernedfrom 1400 to 1900. A statisticallysignificant change point is firstseen in theearly 1900s, with steady advancement since 1952. Recent advancement exceedsobserved variation of the previous 600 years.Menzel (2005) analyzedgrape- harvestdates across Europe, forwhich April-August temperatures explain 84% of thevariation. She foundthat the 2003 Europeanheat wave standsout as an extreme earlyharvest (i.e., the warmest summer) going back 500 years.Although such lengthy observationalrecords are extremelyrare, these two unrelated plants on oppositesides of the world add an importanthistorical perspective to resultsfrom shorter time series. Severallines of evidenceindicate a lengtheningof vegetativegrowing season in the NorthernHemisphere, particularly at higherlatitudes where temperature rise has been greatest.Summer photosynthetic activity (normalized difference vegeta- tion index estimatesfrom satellite data) increasedfrom 1981-1991 (Myneniet al. 1997),concurrent with an advanceand increasein amplitudeof the annual CO2 cycle (Keelinget al. 1996).White et al. (1999) modeledmeteorological and satellitedata to estimateactual growing season length each year from 1900-1987 in theUnited States. Growingseason was unusuallylong duringthe warmperiod of the 1940s at all 12 sites.However, patterns have recentlydiverged. Since 1966, growingseason length has increasedonly in fourof the coldest,most-northerly zones (420-450 latitude), not in the threewarmest zones (320-370 latitude).Across the European Phenolog- ical Gardens (experimentalclones of 16 species of shrubsand treesat sites across Europe),a lengtheningof the growing season by 10.8 daysoccurred from 1959-1993 (Menzel 2000, Menzel & Fabian 1999). Analysisof climatological variables (e.g., last frostdate of springand firstfrost date of fall)mirrors this finding, with an estimated lengtheningof the growingseason of 1.1-4.9 daysper decade since 1951 (Menzel et al. 2003).

642 Parmesan Bradleyet al. (1999) built on Aldo Leopold's observationsfrom the 1930s and 1940s on thetiming of springevents on a Wisconsinfarm. Of 55 speciesresurveyed in the 1980sand 1990s,18 (35%) showedadvancement of springevents, whereas the restshowed no changein timing(with the exceptionof cowbirdsarriving later). On average,spring events occurred 7.3 daysearlier by the 1990scompared with 61 years before,coinciding with March temperaturesbeing 2.80C warmer. Anotherlong-term (100-year) study by Gibbs & Breisch(2001) comparedrecent records(1990-1999) ofthe calling phenology of six frog species in Ithaca,New York, witha turn-of-the-centurystudy (1900-1912). They showed a 10-13-dayadvance associatedwith a 1.0-2.3°C rise in temperatureduring critical months. Amphibian breedinghas also advancedin England,by 1-3 weeks per decade (Beebee 1995). Ecophysiologicalstudies in frogshave shownthat reproduction is closelylinked to bothnighttime and daytimetemperatures (Beebee 1995). In the United Kingdom,Crick et al. (1997), analyzingmore than 74,000 nest recordsfrom 65 bird species between1971 and 1995, foundthat the mean laying dates of firstclutches for 20 species had advancedby an average8.8 days. Brown et al. (1999) founda similarresult for the Mexican jay (Aphelocomaultramarina) in the mountainsof southernArizona. In theNorth Sea, migrantbirds have advanced theirpassage dates by 0.5-2.8 daysper decade since 1960, withno significantdif- ferencebetween short- and long-distancemigrants (Hiippop & Hiippop 2003). In contrast,Gordo et al. (2005) foundthat three of sixlong-distance migrant birds had significantlydelayed arrival to breedinggrounds in Spain,with arrival date highly correlatedwith climatic conditions in theiroverwintering grounds in the southern Sahara. Butterfliesfrequently show a highcorrelation between dates of first appearance and springtemperatures, so it is not surprisingthat their first appearance has advanced for26 of 35 species in the United Kingdom (Roy & Sparks2000) and for all 17 species analyzedin Spain (Stefanescuet al. 2003). Seventypercent of 23 species of butterflyin centralCalifornia have advancedtheir first flight date over 31 years,by an averageof 24 days(Forister & Shapiro2003). Climatevariables explained 85% of variationin flightdate in theCalifornia study, with warmer, drier winters driving early flight. There are onlytwo continental-scale studies of bird phenology. Dunn & Winkler (1999) analyzedchanges in breedingfor tree swallows (Tachycineta bicolor) from 1959 to 1991 overthe entirebreeding range in thecontiguous United Statesand Canada. Laying date was significantlycorrelated with mean May temperatureand had advanced by an averageof nine days over the 32-yearperiod. In a complementary study,Both et al. (2004) analyzedthe pied flycatcher(Ficedula hypoleuca) at 23 sites acrossEurope and founda significantadvance in layingdate fornine of the populations,which also tendedto be thosewith the strongest warming trends. Continental- scale studiesof both lilac (Syringavulgaris) and honeysuckle(Lonicera tatarica and L. korolkowii)in thewestern United States have shownan advancein meanflowering datesof 2 and 3.8 daysper decade,respectively (Cayan et al. 2001). Aquaticsystems exhibit similar trends to thoseof terrestrialsystems. In a lake in thenorthwestern United States, phytoplankton bloom has advancedby 19 daysfrom

www.annualreviews.org* Climate-Change Impacts 643 1962 to 2002, whereaszooplankton peak is morevaried, with some speciesshowing advanceand othersremaining stable (Winder & Schindler2004). The Arcticseabird Brunnich'sguillemot, Uria lomvia,has advancedits egg-layingdate at its southern boundary(Hudson Bay) withno changeat its northernboundary (Prince Leopold Island);both trends are closelycorrelated with changes in sea-icecover (Gaston et al. 2005). Roetzeret al. (2000) explicitlyquantified the additional impacts of urban warming by comparingphenological trends between urban and ruralsites from 1951 to 1995. Urban sites showed significantlystronger shifts toward earlier spring timing than nearbyrural sites, by 2-4 days.An analysisof greeningacross the United Statesvia satelliteimagery also concludedthat urban areas have experienced an earlieronset of springcompared with rural areas (White et al. 2002). Researchersgenerally report phenological changes as a separatecategory from changesin species'distributions, but these two phenomena interplay with each other and withother factors, such as photoperiod,to ultimatelydetermine how climate changeaffects each species(Bale et al. 2002, Chuine & Beaubien2001).

INTERACTIONS ACROSS TROPHIC LEVELS: MATCHES AND MISMATCHES Speciesdiffer in theirphysiological tolerances, life-history strategies, probabilities of populationextinctions and colonizations,and dispersalabilities. These individualistic traitslikely underlie the highvariability in strengthof climateresponse across wild species,even among those subjectedto similarclimatic trends (Parmesan & Yohe 2003). For manyspecies, the primaryimpact of climatechange may be mediated througheffects on synchronywith that species' food and habitatresources. More crucialthan any absolutechange in timingof a singlespecies is the potentialdis- ruptionof coordinationin timingbetween the life cycles of predatorsand theirprey, herbivorousinsects and theirhost plants, parasitoids and theirhost insects, and insect pollinatorswith flowering plants (Harrington et al. 1999,Visser & Both 2005). In Britain,the butterflyAnthocharis cardamines has accuratelytracked phenological shifts of itshost plant, even when bud formationcame twoto threeweeks early (Sparks & Yates 1997). However,this may be the exceptionrather than the rule. Visser & Both (2005) reviewedthe literatureand foundonly 11 species' interactions in which sufficientinformation existed to addressthe question of altered synchrony.Nine of thesewere predator-prey interactions, and twowere insect-host plantinteractions. In spiteof small sample size, an importanttrend emerged from this review:In the majorityof cases (7 of 11), interactingspecies responded differently enough to climatewarming that they are more out of synchronynow than at the startof the studies.In manycases, evidence for negative fitness consequences of the increasingasynchrony has been eitherobserved directly or predictedfrom associated studies(Visser & Both 2005). In one example,Inouye et al. (2000) reportedresults of monitoring between 1975 and 1999at Rocky Mountain Biological Laboratory in Colorado,where there has been a 1.4°C risein local temperature.The annualdate ofsnowmelt and plant flowering did

644 Parmesan not changeduring the studyperiod, but yellow-bellied marmots (Marmotaflaviven- tris)advanced their emergence from hibernation by 23 days,changing the relative phenologyof marmotsand theirfood plants. In a similarvein, Winder & Schindler IntergovernmentalPanel documenteda between bloom and (2004) growingasynchrony peak phytoplankton on ClimateChange: a peak zooplanktonabundances in a freshwaterlake. scientificpanel formed More complexphenomena resulting from trophic mismatches have also been underthe auspices of the UnitedNations and the documented.For example,phenological asynchrony has been linkedto a rangeshift WorldMeteorological in thebutterfly Euphydryas editha. Warm and/or dry years alter insect emergence time Organizationfor the relativeto both the senescencetimes of annualhosts and the timeof of blooming purposeof synthesizing nectarsources (Singer 1972, Singer & Ehrlich1979, Singer & Thomas 1996,Thomas literatureand forming et al. 1996, Weiss et al. 1988). Field studieshave documentedthat butterfly-host scientific consensus on climate andits asynchronyhas resulteddirectly in populationcrashes and extinctions.Long-term change impacts censusesrevealed that population extinctions occurred during extreme droughts and low snowpackyears (Ehrlich et al. 1980, Singer& Ehrlich1979, Singer& Thomas 1996,Thomas et al. 1996),and theseextinctions have been highly skewed with respect to bothlatitude and elevation,shifting mean location of extant populations northward and upward(Parmesan 1996, 2003, 2005a). Van Nouhuys& Lei (2004) showedthat host-parasitoid synchrony was influenced signficantlyby earlyspring temperatures. Warmer springs favored the parasitoid wasp Cotesiamelitaearum by bringing it morein synchronywith its host, the butterfly Melitaeacinxia. Furthermore, they argue that because most butterfly populations are protandrous(i.e., males pupatingearlier than females), temperature-driven shifts in synchronywith parasitoids may affect butterfly sex ratios.

OBSERVED RANGE SHIFTS AND TRENDS IN LOCAL ABUNDANCE Expecteddistributional shifts in warmingregions are polewardand upwardrange shifts.Studies on theseshifts fall mainly into two types: (a) thosethat infer large-scale rangeshifts from small-scale observations across sections of a rangeboundary (with thetotal study area often determined by a politicalboundary such as state,province, or countrylines) and (b)those that infer range shifts from changes in species'composition (abundances)in a local community.Studies encompassing the entire range of a species, or at leastthe northern and southern(or lowerand upper)extremes, are fewand have been concentratedon amphibians(Pounds et al. 1999, 2006), a mammal(Beever et al. 2003), and butterflies(Parmesan 1996, Parmesanet al. 1999). The paucityof whole-rangestudies likely stems from the difficultiesof gatheringdata on the scale of a species'range-often covering much of a continent.

Shiftsat PolarLatitudes

Broad impactsof climatechange in polar regions-fromrange shifts to community restructuringand ecosystemfunctioning-have been reviewedby the Intergovern- mentalPanel on ClimateChange (Anisimovet al. 2001), theArctic Climate Impact Assessment(2004) and theMillenium Ecosystem Assessment (Chapin et al. 2006).

www.annualreviews.org* Climate-Change Impacts 645 Antarctic. Plant,bird, and marinelife of Antarcticahave exhibitedpronounced responses to anthropogenicclimate change. These responseshave been largelyat- tributedto extensive in sea-ice whichin turn SST: seasurface changes(mostly declines) extent, appears to have stimulateda cascade effectin Declines in sea-ice temperature trophic biologicalsystems. extentand durationsince 1976 have apparentlyreduced abundances of ice algae, in turnleading to declinesin krill(from 38%-75% per decade) in a largeregion where theyhave been historically concentrated, the southwest Atlantic (Atkinson et al. 2004). Krill (Euphausiasuperba) is a primaryfood resource for many fish, seabirds, and ma- rinemammals. Interestingly, McMurdo Dry Valleys,which actually cooled between 1990 and 2000, also showeddeclines in lake phytoplanktonabundances and in soil invertebrateabundances (Doran et al. 2002). Penguins and other seabirdsin Antarcticahave shown dramaticresponses to changesin sea-iceextent over the past century (Ainley et al. 2003, Croxallet al. 2002, Smithet al. 1999). The sea-ice dependentAd6lie and emperorpenguins (Pygoscelis adeliaeand Aptenodytesforsteri, respectively) have nearly disappeared from their north- ernmostsites around Antarctica since 1970.Emperors have declined from 300 breeding pairsdown to just 9 in the westernAntarctic Peninsula (Gross 2005), withless severedeclines at Terre Adelie (66 S), wherethey are now at 50% ofpre-1970s abundances (Barbraud& Weimerskirch2001). Addlieshave declinedby 70% on Anvers Island(64o-650 S alongthe Antarctic peninsula (Emslie et al. 1998,Fraser et al. 1992), whereasthey are thrivingat themore-southerly Ross Island at 770 S (Wilson et al. 2001)-effectivelyshifting this species poleward. In thelong-term, sea-ice-dependent birdswill suffer a generalreduction of habitatas ice shelvescontract [e.g., as has al- readyoccured in the Ross Sea (IPCC 2001b)] or collapse [e.g.,as did the LarsenIce Shelvesalong theAntarctic Peninsula in 2002 (Alleyet al. 2005)]. In contrast,open-ocean feeding penguins-the chinstrapand gentoo-invaded southwardalong theAntarctic Peninsula between 20 and 50 yearsago, withpaleo- logical evidencethat gentoo had been absentfrom the Palmerregion for 800 years previously(Emslie et al. 1998, Fraseret al. 1992). Plantshave also benefitedfrom warmingconditions. Two Antarcticvascular plants (a grass,Deschampsia antarctica, and a cushionplant, Colobanthus quitensis) have increased in abundanceand begunto colonizenovel areas overa 27-yearperiod (Smith 1994).

Arctic. Nearlyevery Arctic ecosystem shows marked shifts. Diatom and invertebrate assemblagesin Arcticlakes have shownhuge species' turnover,shifting away from benthicspecies towardmore planktonicand warm-water-associatedcommunities (Smol et al. 2005). Acrossnorthern Alaska, Canada, and partsof Russia,shrubs have been expandinginto the tundra(Sturm et al. 2005). Field studies,experimentation, and modelinglink this major community shift to warming air temperatures, increased snowcover, and increased soil microbial activity (Chapin et al. 1995;Sturm et al. 2001, 2005). Populationsof a pole-polemigrant, the sooty shearwater (Puffinusgriseus), have shiftedtheir migration routes by hundreds of kilometersin concertwith altered sea surfacetemperature (SST) in the Pacific(Spear & Ainley1999). Sea-ice declinein theArctic has been more evenly distributed than in theAntarctic. Becauseof differing geology, with an ocean at thepole ratherthan land, Arctic species

646 Parmesan thatare sea-icedependent are effectivelylosing habitat at all rangeboundaries. Polar bearshave suffered significant population declines at opposite geographic boundaries. At theirsouthern range boundary (Hudson Bay), polar bears are decliningboth in numbersand in meanbody weight (Stirling et al. 1999). Climatechange has causeda lengtheningof ice-free periods on Hudson Bay,periods during which the bears starve and liveon theirreserves because an ice shelfis necessaryfor feeding. Furthermore, researchershave also linkedwarming trends to reductionsof the bears' main food, the ringedseal (Derocher et al. 2004, Fergusonet al. 2005). At the bears' northern rangeboundaries off Norway and Alaska,sea ice has also been reduced,but poorer recordsmake it is less clearwhether observed declines in bodysize and the number of cubs per femaleare linkedto climatetrends or to more basic density-dependent processes(Derocher 2005, Stirling2002).

Shiftsin Northern-HemisphereTemperate Species On a regionalscale, a studyof the 59 breedingbird species in GreatBritain showed both expansionsand contractionsof northernrange boundaries,but the average boundarychange for 12 species thathad not experiencedoverall changes in den- sitywas a mean northwardshift of 18.9 km over a 20-yearperiod (Thomas & Lennon 1999). For a fewwell-documented bird species, their northern U.K. bound- arieshave trackedwinter temperatures for over 130 years(Williamson 1975). Phys- iological studiesindicate that the northernboundaries of North Americansong- birdsmay generally be limitedby winter nighttime temperatures (Burger 1998, Root 1988). Analogousstudies exist for Lepidoptera (butterflies and moths),which have un- dergonean expansionof northern boundaries situated in Finland(Marttila et al. 1990, Mikkola 1997), Great Britain(Hill et al. 2002, Pollard 1979, Pollard & Eversham 1995, Warren1992), and acrossEurope (Parmesanet al. 1999). Dependingon the study,some 30% to 75% ofnorthern boundary sections had expandednorth; a smaller portion(<20%) had contractedsouthward; and theremainder were classified as stable. In a studyof 57 nonmigratoryEuropean butterflies,data were obtainedfrom bothnorthern and southernrange boundaries for 35 species(Parmesan et al. 1999). Nearlytwo thirds (63 %) had shiftedtheir ranges to thenorth by 35-240 km,and only twospecies had shiftedto thesouth (Parmesan et al. 1999).In themost-extreme cases, the southernedge contractedconcurrent with northern edge expansion.For example, thesooty copper (Heodes tityrus) was commonin theMontseny region of central Cataloniain the 1920s,but modernsightings are onlyfrom the Pyrenees,50 km to thenorth. Symmetrically, H. tityrusentered Estonia for the first time in 1998,by 1999 had establishedseveral successful breeding populations, and by2006 had reachedthe BalticSea (Parmesanet al. 1999; T. Tammaru,personal communication). Anothercharismatic insect group with good historicalrecords is Odonata (drag- onfliesand damselflies).In a studyof all 37 speciesof resident odonates in theUnited Kingdom,Hickling et al. (2005) documentedthat 23 ofthe 24 temperatespecies had expandedtheir northern range limit between 1960-1995, with mean northward shift of 88 km.

www.annualreviews.org* Climate-Change Impacts 647 Nondiapausing(i.e., active year-round) butterfly species are also moving north- wardwith warmer winters. The northern boundary of the sachem skipper butterfly has expandedfrom California to Washington State (420 miles) in just 35 years(Crozier 2003,2004). During a singleyear-the warmest on record (1998)-it moved75 miles northward.Laboratory and field manipulations showed that individuals are killed by a single,short exposure to extremelow temperatures (-10OC) or repeated exposures to -4°C, indicatingwinter cold extremes dictate the northern range limit (Crozier 2003,2004). The desertorange tip (Colotis evagore), which historically was confined to northernAfrica, has established resident populations in Spainwhile maintaining thesame ecological niche. Detailed ecological and physiological studies confirm that C. evagorehas remained a specialist of hot microclimates, needing more than 164 days atgreater than 120C to mature. It hasnot undergone a host switch in its new habitat, andit has not evolved a diapausestage (Jordano et al. 1991). In theNetherlands between 1979 and 2001, 77 newepiphytic lichens colonized fromthe south, nearly doubling the total number of species for that community (van Herket al. 2002).Combined numbers of terrestrial and epiphytic lichen species increasedfrom an average of 7.5 per site to 18.9per site. An alternate approach to docu- mentingcolonizations isto document extinction patterns. Comparing recent censuses acrossNorth America (1993-1996) with historical records (1860-1986), Parmesan (1996)documented that high proportions ofpopulation extinctions along the southernrange boundary of Edith's checkerspot butterfly (E. editha)had shifted the mean locationof living populations 92 kmfarther north (Parmesan 1996, 2003, 2005a).

Shiftsof Tropical Species Ranges Warmingtrends at lower latitudes are associated with movements oftropical species intomore-temperate areas. The rufoushummingbird has undergone a dramatic shift in itswinter range (Hill et al. 1998).Thirty years ago itwintered mainly in Mexico, andbetween 1900 and 1990, there were never more than 30 winter sightings per year alongthe Gulf Coast of the United States. In theearly 1990s, sightings increased to morethan 100 per year in thesouthern United States. The numberof sightings hasincreased steadily since then-up to 1,643by 1996, with evidence that, by 1998, residentpopulations had colonized400 kminland (Howell 2002). Over this same period,winter temperatures rose by approximately 1C (IPCC 2001b).In Florida, fivenew species of tropical dragonfly established themselves in 2000,an apparently naturalinvasion from Cuba and the Bahamas (Paulson 2001). Similarly,North African species are moving into Spain and France, and Mediter- raneanspecies are moving up intothe continental interior. The Africanplain tiger butterfly(Danaus chrysippus) established its first population in southern Spain in 1980 andby the 1990s had established multiple, large metapopulations (Haeger 1999).

Elevational Shifts Montanestudies have generally been scarcer and less well documented (lower sam- plingresolution), but a fewgood data sets show a generalmovement ofspecies upward

648 Parmesan in elevation.By comparingspecies compositionsin fixedplots along an elevational gradientin MonteverdeNational Park, Costa Rica,Pounds et al. (1999, 2005) documentedthat lowland birds have begun breeding in montanecloud-forest habitat over the past 20 years.A similarstudy across 26 mountainsin Switzerlanddocumented thatalpine flora have expanded toward the summits since the plots were first censused in the 1940s(Grabherr et al. 1994,Pauli et al. 1996). Upwardmovement of treelines has been observedin Siberia(Moiseev & Shiyatov2003) and in theCanadian Rocky Mountains,where temperatures have risenby 1.5°C (Luckman& Kavanagh2000). The few studiesof lower elevationallimits show concurrentcontractions up- wardof these warm range boundaries. Because warmboundaries generally have data gaps throughtime, these studies have conductedrecensuses of historicallyrecorded (sedentary)populations and lookedfor nonrandom patterns of long-term population extinctions. A 1993-1996 recensusof Edith's checkerspotbutterfly (E. editha)populations recorded1860-1986 throughout its range (Mexico to Canada) documentedthat more than 40% of populationsfrom 0-2400 m were extinct(in spite of havingsuitable habitat),whereas less than15% wereextinct at thehighest elevations (2400-3500 m) (Parmesan1996). Over the past 50-100 years,snowpack below 2400 m has become lighterby 14% and melts7 days earlier,whereas higher elevations (2400-3500 m) have 8% heaviersnowpack and no change in melt date (Johnsonet al. 1999). In concertwith altered snow dynamics,the mean locationof E. edithapopulations has shiftedupward by 105 m (Parmesan1996, 2003, 2005a). In southernFrance, metapopulations of the cool-adapted Apollo butterfly (Parnas- siusapollo) have gone extinct over the past 40 yearson plateausless than 850 m highbut haveremained healthy where plateaus were greater than 900 m high(Descimon et al. 2006). The data suggestthat dispersal limitation was important,and thisstrong flyer can persistwhen nearby higher elevation habitats exist to colonize.In Spain,the lower elevationallimits of 16 speciesof butterfly have risen an averageof 212 m in 30 years, concurrentwith a 1.3°C risein mean annualtemperatures (Wilson et al. 2005). In the Great Basin of thewestern United States,7 out of 25 recensusedpopula- tionsof the pika (Ochotonaprinceps, Lagomorpha) were extinctsince beingrecorded in the 1930s(Beever et al. 2003). Human disturbanceis minimalbecause pika habitat is high-elevationtalus (scree) slopes,which are not suitablefor ranching or recre- ationalactivities. Extinct populations were at significantlylower elevations than those stillpresent (Parmesan & Galbraith2004). Field observationsby Smith(1974) documentedthat adult pika stopped foraging in themidday heat in Augustat low elevation sites.Subsequent experiments showed that adults were killedwithin a halfhour at morethan 31 C (Smith1974).

Marine CommunityShifts Decades ofecological and physiologicalresearch document that climatic variables are primarydrivers of distributions and dynamicsof marine plankton and fish(Hays et al. 2005, Roessiget al. 2004). Globallydistributed planktonic records show strong shifts of phytoplanktonand zooplanktoncommunities in concertwith regionaloceanic

www.annualreviews.orgo Climate-Change Impacts 649 climateregime shifts, as well as expectedpoleward range shifts and changesin timing of peak biomass(Beaugrand et al. 2002, deYounget al. 2004, Hays et al. 2005, Richardson& Schoeman2004). Some copepod communitieshave shiftedas much as 1000 kmnorthward (Beaugrand et al. 2002). Shiftsin marinefish and invertebrate communitieshave been been particularlywell documentedoff the coastsof western North Americaand the United Kingdom.These two systemsmake an interesting contrast(see below) because the west coast of North Americahas experienceda 60-yearperiod of significantwarming in nearshoresea temperatures,whereas much ofthe U.K. coastexperienced substantial cooling in the 1950sand 1960s,with warm- ingonly beginning in the 1970s(Holbrook et al. 1997,Sagarin et al. 1999,Southward et al. 2005). Sagarinet al. (1999) relateda 20C riseof SST inMonterey Bay, California, between 1931 and 1996 to a significantincrease in southern-rangedspecies and decreaseof northern-rangedspecies. Holbrook et al. (1997) foundsimilar shifts over the past 25 yearsin fishcommunities in kelphabitat off California. Much ofthe data from the North Atlantic, North Sea, andcoastal United Kingdom have exceptionallyhigh resolutionand long time series,so theyprovide detailed informationon annualvariability, as well as long-termtrends. Over 90 years,the timingof animalmigration (e.g., veined squid, Loligoforbesi, and flounderPlatichthys flesus)followed decadal trendsin ocean temperature,being later in cool decades and up to 1-2 monthsearlier in warmyears (Southward et al. 2005). In theEnglish Channel, cold-adapted fish (e.g., herring Clupea harengus) declined duringboth warmingperiods (1924 to the 1940s, and post-1979),whereas warm- adaptedfish did the opposite(Southward et al. 1995, 2005). For example,pilchard Sardinapilchardus increased egg abundancesby two to threeorders of magnitude dur- ingrecent warming. In theNorth Sea, warm-adaptedspecies (e.g., anchovy Engraulis encrasicolusand pilchard)have increased in abundancessince 1925 (Beare et al. 2004), and sevenout of eight have shifted their ranges northward (e.g., bib, Trisopterus luscus) by as much as 100 km per decade (Perryet al. 2005). Recordsdating back to 1934 forintertidal invertebrates show equivalentshifts between warm- and cold-adapted species(e.g., thebarnacles Semibalanus balanoides and Chthamalusspp., respectively), mirroringdecadal shifts in coastaltemperatures (Southward et al. 1995,2005).

Pest and Disease Shifts

Pest speciesare also movingpoleward and upward.Over the past 32 years,the pine processionarymoth (Thaumetopoea pityocampa) has expanded87 km at its northern rangeboundary in France and 110-230 m at its upperaltitudinal boundary in Italy (Battistiet al. 2005). Laboratoryand fieldexperiments have linked the feeding behav- ior and survivalof thismoth to minimumnighttime temperatures, and its expansion has been associatedwith warmer winters. In theRocky Mountain range of the United States,mountain pine beetle (Dendroctonusponderosae) has respondedto warmer temperaturesby alteringits life cycle.It now only takes one year per generation ratherthan its previous two years, allowing large increases in populationabundances, which,in turn,have increased incidences of a fungusthey transmit (pine blisterrust,

650 Parmesan Cronartiumribicola) (Logan et al. 2003). Increasedabundance of a nemotodeparasite has also occurredas its lifecycle shortened in responseto warmingtrends. This has had associatednegative impacts on itswild musk oxen host, causing decreased survival and fecundity(Kutz et al. 2005). In a singleyear (1991), the oysterparasite Perkinsus marinus extended its range northwardfrom Chesapeake Bay to Maine-a 500 km shift.Censuses from1949 to 1990 showed a stable distributionof the parasitefrom the Gulf of Mexico to its northernboundary at Chesapeake Bay. The rapid expansionin 1991 has been linkedto above-averagewinter temperatures rather than human-driven introduction or geneticchange (Ford 1996).A kidneydisease has been implicatedin low-elevation troutdeclines in Switzerland.High mortalityfrom infection occurs above 150-16oC, and watertemperatures have risenin recentdecades. High infectionrates (27% of fishat 73% of sites)at sitesbelow 400 m have been associatedwith a 67% declinein catch;mid-elevation sites had lowerdisease incidence and onlymoderate declines in catch;and thehighest sites (800-3029 m) had no diseasepresent and relativelystable catchrates (Hari et al. 2006). Changesin thewild also affecthuman disease incidence and transmissionthrough alterationsin disease ecologyand in distributionsof theirwild vectors(Parmesan & Martens2006). For example,in Sweden,researchers have documentedmarked increasesin abundancesof the disease-transmitting tick Ixodes ricinus along its north- ernmostrange limit (Lindgren & Gustafson2001). Betweenthe early 1980s and 1994, numbersof ticksfound on domesticcats and dogs increasedby 22%-44% alongthe tick'snorthern range boundary across central Sweden. In the same timeperiod, this regionhad a markeddecrease in the numberof extremelycold days (<-120C) in winterand a markedincrease in warmdays (> 100C) duringthe spring, summer, and fall.Previous studies on temperaturedevelopmental and activitythresholds indicated theobserved warmer temperatures cause decreased tick mortality and longergrowing seasons(Lindgren & Gustafson2001).

Trees and Treelines: Complex Responses A complexof interactingfactors determines treeline, often causing difficultiesin interpretationof twentieth-centurytrends. Some speciesare "well behaved"in that theyshow similar patterns of increasedgrowth at treelineduring the earlywarming in the 1930s and 1940s as duringthe recentwarming of the past 20 years.In recent decades, treelineshave shiftednorthward in Sweden (Kullman 2001) and eastern Canada (Lescop-Sinclair& Payette 1995), and upwardin Russia (Meshinevet al. 2000, Moiseev & Shiyatov2003) and New Zealand (Wardle& Coleman 1992). However,in otherstudies, researchers saw a strongresponse to warmingin the late 1930s and 1940s but a weaker (or absent) responsein recentwarm decades (Innes 1991,Jacoby & D'Arrigo 1995, Lescop-Sinclair& Payette1995, Briffaet al. 1998a,b),possibly resulting from differences in rainfallbetween the two warm periods. In Alaska,recent decades have been relativelydry, which may have preventedtrees fromresponding to currentwarming as theydid before(Barber et al. 2000, Briffa et al. 1998b). In contrast,treelines in the arid southwestUnited States,which has

www.annualreviews.orgo Climate-Change Impacts 651 had increasedrainfall, have shown unprecedented increased tree-ring growth at high elevations(Swetnam & Betancourt1998). An impressivestudy across all ofnorthern Russia from 1953-2002 showeda shift in treeallometries. In areaswhere summer temperatures and precipitationhave both increased,a generalincrease in biomass(up 9%) is primarilya resultof increased greenery(33 % more carbonin leaves and needles),rather than woody parts(roots and stem).In areas thathave experiencedwarming and dryingtrends, greenery has decreased,and bothroots and stemshave increased(Lapenis et al. 2005).

EXTINCTIONS

Amphibians Documentedrapid loss of habitableclimate space makesit no surprisethat the first extinctionsof entirespecies attributedto global warmingare mountain-restricted species.Many cloud-forest-dependentamphibians have declinedor gone extincton a mountainin Costa Rica (Poundset al. 1999,2005). Amongharlequin frogs in Central and SouthAmerican tropics, an astounding67% have disappearedover the past 20- 30 years.Pounds et al. (2006) hypothesisedthat recent trends toward warmer nights and increaseddaytime cloud coverhave shiftedmid-elevation sites (1000-2400 m), wherethe preponderance of extinctions have occurred, into thermally optimum con- ditionsfor the chytrid fungus, Batrachochytrium dendrobatidis.

TropicalCoral Reefs Elevated sea temperaturesas small as 1C above long-termsummer averages lead to bleaching(loss of coral algal symbiont),and global SST has risenan averageof 0.1 -0.20C since 1976 (Hoegh-Guldberg1999, IPCC 2001b).A moreacute problem forcoral reefsis the increasein extremetemperature events. El Nifio eventshave been increasingin frequencyand severitysince recordsbegan in the early 1900s, and researchersexpect this trend to continueover coming decades (Easterling et al. 2000, IPCC 2001b,Meehl et al. 2000). A particularlystrong El Nifio in 1997-1998 caused bleachingin everyocean (up to 95% ofcorals bleached in theIndian Ocean), ultimatelyresulting in 16% of corals renderedextinct globally (Hoegh-Guldberg 1999, 2005b; Wilkinson2000). Recentevidence for genetic variation among the obligatealgal symbiontin tem- peraturethresholds suggests that some evolutionaryresponse to higherwater tem- peraturesmay be possible(Baker 2001, Rowan2004). Changesin genotypefrequencies towardincreased frequency of high-temperature-tolerantsymbiont appear to have occurredwithin some coralpopulations between the mass bleachingevents of 1997-1998 and 2000-2001 (Bakeret al. 2004). However,other studies indicate that many entirereefs are alreadyat theirthermal tolerance limits (Hoegh-Guldberg 1999). Coupled withpoor dispersalof symbiontbetween reefs, this has led several researchersto concludethat local evolutionaryresponses are unlikely to mitigatethe negativeimpacts of futuretemperature rises (Donner et al. 2005, Hoegh-Guldberg et al. 2002).

652 Parmesan One optimisticresult suggests that corals, to some extent,may be able to mirror terrestrialrange shifts. Two particularlycold-sensitive species (staghorn coral, Acro- pora ceervicornis,and elkhorncoral, Acropora palmata) have recentlyexpanded their rangesinto the northern Gulf of Mexico (firstobservation in 1998),concurrent with risingSST (Precht& Aronson2004). Althoughcontinued poleward shift will be lim- ited by lightavailability at some point (Hoegh-Guldberg1999), small range shifts mayaid in developingnew refugiaagainst extreme SST eventsin future. Althoughimpacts have not yet been observed,the fate of coral reefsmay be as, or more,affected in comingdecades by the directeffects of CO2 ratherthan temperaturerise. Increased atmospheric CO2 sinceindustrialization has significantly loweredocean pH by0.1. The moredire projections (a doublingto triplingof current CO2 levels) suggestthat, by 2050, oceans may be too acidic for corals to calcify (Caldeira & Wickett2003, Hoegh-Guldberg2005a, Orr et al. 2005).

Population ExtinctionsLeading to Range Contractions Many specieshave suffered reduced habitable area due to recentclimate change. For thosespecies that have alreadybeen drivenextinct at theirequatorial or lowerrange boundaries,some have eitherfailed to expandpoleward or are unableto expanddue to geographicbarriers. Such specieshave sufferedabsolute reductions in rangesize, puttingthem at greaterrisk of extinctionin thenear future. This is particularlyevident in polar species,as theseare alreadypushed against a geographicallimit. Researchers have seen largereductions in populationabundances and generalhealth along the extremesouthern populations of Arcticpolar bears (Derocher2005, Derocheret al. 2004, Stirlinget al. 1999) and theextreme northern populationsofAntarctic Addlie and emperor penguins (Ainley et al. 2003,Croxall et al. 2002, Emslieet al. 1998,Fraser et al. 1992,Smith et al. 1999,Taylor & Wilson 1990, Wilson et al. 2001). In the United Kingdom,four boreal odonateshave contracted northwardby an averageof 44 kmover 40 years(Hickling et al. 2005). Similarly,high numbers of populationextinctions have occurredalong the lower elevationalboundaries of mountaintopspecies, such as pikasin the westernUnited States(Beever et al. 2003) and theApollo butterflyin France(Descimon et al. 2006). For 16 mountain-restrictedbutterflies in Spain,warming has alreadyreduced their habitatby one thirdin just 30 years(Wilson et al. 2005). Warmingand dryingtrends on Mt. Kiliminjarohave increasedfire impacts, which have caused a 400-m down- wardcontraction of closed (cloud) forest,now replacedby an open,dry alpine system (Hemp 2005). Temperatelow-elevation species are not immune:Twenty-five per- cent of temperatebutterflies in Europe contractednorthward by 35-50 km over a 30-70-yearperiod. For one of these,its northern range boundary had not expanded, so it sufferedan overallcontraction of rangesize (Parmesanet al. 1999).

EVOLUTION AND PLASTICITY

Species ranges are dynamic.Historically, ecologists have viewed species' niches as static and range shiftsover time as passive responsesto major environmental changes(global climateshifts or geologicalchanges in corridorsand barriers).

www.annualreviews.org* Climate-Change Impacts 653 There is no doubtthat climate plays a majorrole in limitingterrestrial species' ranges (Andrewartha& Birch1954; Bale et al. 2002; Parmesanet al. 2000, 2005; Prechtet al. 1973; Webb & Bartlein1992; Weiser 1973; Woodward1987). Recentphysiological and biogeographicstudies in marinesystems also implicatetemperature as a primary driverof species' ranges (Hoegh-Guldberg 1999, 2005b; Hoegh-Guldberg& Pearse 1995). However,evolutionary processes clearly can substantiallyinfluence the patterns and ratesof response to climatechange. Theoretically, evolution can also driverange shiftsin the absenceof environmentalchange (Holt 2003). A primeexample of this is thehybridization of twospecies of Australian fruit fly that led to noveladaptations, allowingrange expansion with no concomitantenvironmental change (Lewontin & Birch 1966). The problemof estimating the relative roles of evolution and plasticityis tractable withextensive, long-term ecological and geneticdata. For example,genetic analysis of a populationof red squirrelsin the Arcticindicated that 62% of the change in breedingdates occurring over a 10-yearperiod was a resultof phenotypicplasticity, and 13% was a resultof genetic change in thepopulation (Berteaux et al. 2004, Reale et al. 2003). Geneticistsin the 1940snoticed that certain chromosomal inversions in fruitflies (Drosophila)were associatedwith heat tolerance(Dobzhansky 1943, 1947). These "hot" genotypeswere more frequentin southernthan in northernpopulations and increasedwithin a populationduring each season,as temperaturesrose fromearly springthrough late summer. Increases in thefrequencies of warm-adapted genotypes have occurredin wild populationsof Drosophilassp in Spain between1976 and 1991 (Rodriguez-Trelles& Rodriguez1998, Rodriguez-Trelleset al. 1996, 1998),as well as in the United Statesbetween 1946 and 2002 (Levitan2003). The changein the United Stateswas so greatthat populations in New Yorkin 2002 wereconverging on genotypefrequencies found in Missouriin 1946. In contrast,red deer in Norwayshow completelyplastic responses. Their body size respondsrapidly to yearlyvariability of wintertemperatures. Warmer winters cause developingmales to become largerwhile females become smaller(Post et al. 1999). In consequence,the end resultof a gradualwinter warming trend has been an increasein sexualdimorphism. A surprisingtwist is thatspecies whose phenologyis underphotoperiodic con- trolhave also respondedto temperature-drivenselection for spring advancement or fall delay.Bradshaw & Holzapfel (2001) showed thatthe pitcherplant mosquito, Wyeomyiasmithii, has evolveda shortercritical photoperiod in associationwith a longer growingseason. Northernpopulations of thismosquito now use a shorter day-lengthcue to enterwinter diapause, doing so laterin the fall than theydid 24 yearsago.

The Role of Evolution in Shaping Species' Impacts Increasingnumbers of researchersuse analysesof currentintraspecific genetic vari- ationfor climate tolerance to arguefor a substantiverole of evolutionin mitigating

654 Parmesan negativeimpacts of futureclimate change (Baker2001, Bakeret al. 2004, Davis & Shaw 2001, Rowan 2004). However,in spite of a plethoraof data indicatinglocal adaptationto climatechange at specificsites, the fossilrecord shows little evidence forthe evolution of novel phenotypes across a speciesas a whole.Pleistocene glacia- tionsrepresent shifts 5-10 timesthe magnitude of twentieth-century global warming. These did not resultin majorevolution at the specieslevel (i.e., appearanceof new formsoutside the bounds of known variation for that species), nor in majorextinction or speciationevents. Existing species appearedto shifttheir geographical distribu- tionsas thoughtracking the changingclimate, rather than remaining stationary and evolvingnew forms(Coope 1994,Davis & Zabinski1992, Huntley 1991). Most of the empiricalevidence for rapid adaptationto climatechange comes fromexamples of evolution in theinteriors of species' ranges toward higher frequen- cies of alreadyexisting heat-tolerant genotypes. In studiesthat focus on dynamicsat the edge of a species' rangeor across an entirerange, a differentpicture emerges. Several studiessuggest that the effectsof both geneticconstraints and asymmet- rical gene floware intensifiedclose to species' borders(Antonovics 1976, Garcia- Ramos & Kirkpatrick1997, Hoffmann& Blows 1994). It is expectedthat a warming climatestrengthens climate stress at equatorialrange boundariesand reduces it at polewardboundaries. Equatorial boundary populations are oftenunder natural selectionfor increased tolerance to extremeclimate in the absence of climate change,but may be unable to responddue to lack of necessarygenetic variance. Furthermore,gene flowfrom interior populations may stifle response to selectionat therange limits, even when sufficient genetic variation exists (Kirkpatrick & Barton 1997). Because ofstrong trade-offs between climate tolerance and resource/habitatpref- erences,a relaxationof selectionon climatetolerance at northernboundaries may cause rapid evolutionof these correlatedtraits. This processhas been investigated in the European butterflyAricia agestis,in which populationsnear the northern range boundaryhad previouslyadapted to cool conditionsby specializingon the host genus,Helianthemum, which growsin hot microclimatesand hence supports fastlarval growth. Climate warming did not initiallycause rangeexpansion because Helianthemumwas absentto theimmediate north of the range limit. However, warming did permitrapid evolution of a broaderdiet at the rangelimit, to a hostused in more southernpopulations, Geranium, which grows in cooler microclimates.Once thislocal dietevolution occurred, the boundary expanded northward across the band fromwhich Helianthemum was absentbut Geranium was present (Thomas et al. 2001). This exampleshows how a complexinterplay may occur betweenevolutionary processesand ecologicalresponses to extremeclimates and climatechange. How- ever,these evolutionary events did not constitutealternatives to ecologicalresponses to climatechange; they modulated those changes. Adaptive evolution of host prefer- ence occurredat the northernrange boundary in responseto temperaturerise, but geneticvariation for host use alreadyexisted within the A. agestisbutterfly. In this case, evolutionaryprocesses are not an alternativeto rangemovement, but instead modulatethe magnitudeand dynamicsof the range shift.This is not likelyto be an isolatedexample because populationsof otherspecies near polewardboundaries

www.annualreviews.org* Climate-Change Impacts 655 are knownto specializeon resourcesthat mitigate the effectsof cool climate.Such resourceseither support rapid growth or occurin thehottest available microclimates (Nylin 1988, Scriber& Lederhouse1992, Thomas et al. 2001). In additionto resourcechoice, dispersal tendency evolves at rangemargins in responseto climatechange. In nonmigratoryspecies, the simplest explanation of north- wardrange expansions is thatindividuals have alwayscrossed the species' boundary, and withclimate warming, some of theseemigrants are successfulat foundingnew populationsoutside the formerrange. When dispersaltendency is heritable,these new populationscontain dispersive individuals and higherrates of dispersal will soon evolveat the expandingboundary. Evolutiontoward greater dispersal has indeedbeen documentedin severalspecies of insect.Two speciesof wing-dimorphic bush crickets in theUnited Kingdom have evolvedlonger wings at theirnorthern range boundary, as mostlylong-winged forms participatedin therange expansion and short-winged forms were left behind (Thomas et al. 2001). Adultsof newlycolonized populations of the speckledwood butterfly (Parargeaegeria) in the United Kingdomhave largerthoraces and greaterflight ca- pabilitythan historical populations just to the south(Hill et al. 1999). Variationin dispersalabilities can be cryptic.Newly founded populations of the butterfly M. cinxia containedfemales that were genetically superior dispersers due to increasedproduc- tionof ATP (Hanski et al. 2004). Overall,empirical evidence suggests that evolution can complement,rather than supplant,projected ecological changes. However, there is littletheoretical or experi- mentalsupport to suggestthat climate warming will cause absolute climatic tolerances of a speciesto evolvesufficiently to allowit to conserveits geographic distribution in theface of climate change and therebyinhabit previously unsuitable climatic regimes (Donner et al. 2005; Hoegh-Guldberg1999, 2005b; Hoegh-Guldberget al. 2002; Jump& Pefiuelas2005).

CONCLUDING THOUGHTS ON EVOLUTION AND CLIMATE CHANGE

For species-levelevolution to occur,either appropriate novel mutations or novelge- neticarchitecture (new gene complexes)would have to emergeto allowa responseto selection.Lynch & Lande (1993) used a geneticmodel to inferrates of environmental changethat would allow populationsto respondadaptively. However, Travis & Futuyma(1993)-discussing thesame questionfrom broad paleontological, population,genetic, and ecologicalperspectives-highlighted the complexity of predicting futureresponses from currently known processes. Fifteen years later, answers still lie verymuch in empiricalobservations. These observationsindicate that, although local evolutionaryresponses to climatechange have occurredwith high frequency,there is no evidencefor change in the absoluteclimate tolerances of a species.This view is supportedby the disproportionatenumber of population extinctions documented along southernand low-elevationrange edges in responseto recentclimate warming,resulting in contractionof species' rangesat thesewarm boundaries, as well as by extinctionsof manyspecies.

656 Parmesan SUMMARYPOINTS

1. The advanceof springevents (bud burst,flowering, breaking hibernation, migrating,breeding) has been documentedon all but one continentand in all major oceans forall well-studiedmarine, freshwater, and terrestrial groups. 2. Variationin phenologicalresponse between interacting species has already resultedin increasingasynchrony in predator-preyand insect-plantsystems, withmostly negative consequences. 3. Polewardrange shifts have been documentedfor individual species, as have expansionsof warm-adapted communities, on all continentsand in mostof themajor oceans forall well-studiedplant and animalgroups. 4. These observedchanges have been mechanisticallylinked to local or re- gionalclimate change through long-term correlations between climate and biologicalvariation, experimental manipulations in thefield and laboratory, and basic physiologicalresearch. 5. Shiftsin abundancesand rangesof parasites and theirvectors are beginning to influencehuman disease dynamics. 6. Range-restrictedspecies, particularly polar and mountaintopspecies, show more-severerange contractions than other groups and have been the first groups in which whole species have gone extinctdue to recentclimate change.Tropical coral reefs and amphibiansare thetaxonomic groups most negativelyimpacted. 7. Althoughevolutionary responses have been documented(mainly in insects), thereis littleevidence that observed genetic shifts are ofthe type or magni- tudeto preventpredicted species extinctions.

FUTUREISSUES 1. Ocean-atmosphereprocesses are dynamicallychanging in responseto an- thropogenicforcings. Indices such as theEl NifioSouthern Oscillation and the North AtlanticOscillation may be a poor basis forprojecting future biologicalimpacts. 2. Projectionsof impactswill be aided by a bettermechanistic understanding ofecological, behavioral, and evolutionaryresponses to complexpatterns of climatechange, and in particularto impactsof extreme weather and climate events.

www.annualreviews.org* Climate-Change Impacts 657 ACKNOWLEDGMENTS

I would like to give manythanks to C. Britt,M. Butcher,J. Mathews,C. Metz, and P. van der Meer forhelp withthe literaturesearch and to D. Simberloffand D. Futuymafor helpful comments on earlierversions. I also want to give special appreciationto M.C. Singerfor his critiqueand editorialassistance.

LITERATURE CITED

AhmadQK, WarrickRA, DowningTE, NishiokaS, ParikhKS, et al. 2001. Methods and tools. See IPCC 2001a, pp. 105-43 AinleyDG, BallardG, EmslieSD, FraserWR, WilsonPR, WoehlerEJ. 2003. Adelie penguinsand environmentalchange. Science 300:429-30 AinleyDG, DivokyGJ. 1998. Climatechange and seabirds:a reviewof trends in the easternportion of thePacific Basin. Pac. Seab.25:20 AlleyRB, ClarkPU, HuybrechtsP, Joughin I. 2005. Ice-sheetand sea-levelchanges. Science310:456-60 AlleyRB, MarotzkeJ, Nordhaus WD, OverpeckJT,Peteet DM, et al. 2003. Abrupt climatechange. Science 299:2005-10 AndrewarthaHG, Birch LC. 1954. The Distributionand Abundanceof Animals. Chicago,IL: Univ.Chicago Press AnisimovO, FitzharrisB, Hagen JO, JefferiesR, MarchantH, et al. 2001. Polar regions(Arctic and Antarctic).See IPCC 2001a, pp. 801-47 AntonovicsJ. 1976. The natureof limitsto naturalselection. Ann. Mo. Bot. Gard. 63:224-47 ArcticClimate Impact Assessment. 2004. Impactsof a WarmingArctic. Cambridge, UK: CambridgeUniv. Press AtkinsonA, SiegelV, PakhomovE, RotheryP. 2004. Long-termdecline in krillstock and increasein salpswithin the Southern Ocean. Nature432:100-3 BadeckFW, BondeauA, B6ttcherK, DoktorD, LuchtW, et al. 2004. Responsesof springphenology to climatechange. New Phytol. 162:295-309 BakerAC. 2001. Reefcorals bleach to survivechange. Nature 411:765-66 BakerAC, StargerCJ, McClanahan TR, GlynnPW. 2004. Coral reefs:corals' adap- tiveresponse to climatechange. Nature 430:741 BaleJS, Masters GJ, Hodkinson ID, AwmackC, BezemerTM, et al. 2002. Herbivory in global climatechange research: direct effects of risingtemperature on insect herbivores.Glob. Change Biol. 8:1-16 BarberVA, Juday GP, FinneyBP. 2000. Reduced growthof Alaskanwhite spruce in the twentiethcentury from temperature-induced drought stress. Nature 405:668-73 BarbraudC, WeimerskirchH. 2001. Emperorpenguins and climatechange. Nature 411:183-86 BattistiA, StastnyM, NethererS, RobinetC, SchopfA, et al. 2005. Expansionof geographicrange in the pine processionarymoth caused by increasedwinter temperatures.Ecol. Appl. 15:2084-96

658 Parmesan Beare DJ, BurnsF, Greig A, JonesEG, Peach K, et al. 2004. Long-termincreases in prevalenceof North Sea fisheshaving southern biogeographic affinities. Mar. Ecol.Prog. Ser 284:269-78 BeaugrandG, Reid PC, Ibanez F, LindleyJA, Edwards M. 2002. Reorganizationof NorthAtlantic marine copepod biodiversityand climate.Science 296:1692-94 Beebee TJC. 1995. Amphibianbreeding and climate.Nature 374:219-20 Beever EA, BrussardPF, BergerJ. 2003. Patternsof apparentextirpation among isolatedpopulations of pikas(Ochotona princeps) in the Great Basin.J. Mammal. 84:37-54 BerteauxD, Reale D, McAdamAG, BoutinS. 2004. Keepingpace withfast climate change:Can Arcticlife count on evolution?Integr. Comp. Biol. 44:140-51 BlencknerT, HillebrandH. 2002. NorthAtlantic Oscillation signatures in aquatic and terrestrialecosystems: a meta-analysis.Glob. Change Biol. 8:203-12 Both C, ArtemyevAV, Blaauw B, Cowie RJ,Dekhuijzen AJ, et al. 2004. Large-scale geographicalvariation confirms that climate change causes birdsto lay earlier. Proc.R. Soc.London Ser. B 271:1657-62 BradleyNL, Leopold AC, RossJ, Wellington H. 1999. Phenologicalchanges reflect climatechange in Wisconsin.Proc. Natl. Acad. Sci. USA 96:9701-4 BradshawWE, HolzapfelCM. 2001. Geneticshift in photoperiodicresponse correlatedwith global warming. Proc. Natl. Acad. Sci. USA 98:14509-11 BriffaKR, SchweingruberFH, JonesPD, OsbornTJ, Harris IC, et al. 1998a. Trees tellof past climates, but are theyspeaking less clearlytoday? Philos. Trans. R. Soc. LondonSer. B 353:65-73 BriffaKR, SchweingruberFH, JonesPD, Osborn TJ, ShiyatovSG, VaganovEA. 1998b.Reduced sensitivity of recent tree-growth to temperatureat high northern latitudes.Nature 391:678-82 BrownJL, Li SH, BhagabatiN. 1999. Long-temtrend toward earlier breeding in an Americanbird: a responseto global warming?Proc. Natl. Acad. Sci. USA 96:5565-69 Bumpus HC. 1899. The eliminationof the unfitas illustratedby the introduced sparrow,Passer domesicus. In BiologicalLectures Delivered at theMarine Biological Laboratoryof Wood's Holl, 1896-97,pp. 209-26. Boston:Ginn & Co BurgerM. 1998. Physiologicalmechanisms limiting the northern boundary of the winter rangeof the northern cardinal (Cardinalis cardinalis). PhD diss.Univ. Mich., Ann Arbor BurtonJ. 1975. The effectsof recentclimatic change on Britishinsects. Bird Study 22:203-4 BurtonJF. 1998a. The apparenteffects of climaticchanges since 1850 on European lepidoptera.Mim. Soc.R. BelgeEntomol. 3 8:125-44 BurtonJF. 1998b. The apparentresponses of European lepidotterato the climate changesof thepast hundred years. Atropos 5:24-30 CaldeiraK, WickettME. 2003. Anthropogeniccarbon and oceanpH. Nature425:365 Cayan DR, KammerdienerSA, DettingerMD, Caprio JM, PetersonDH. 2001. Changesin theonset of spring in thewestern United States.Bull. Am. Meteorol. Soc. 82:399-415

www.annualreviews.org* Climate-Change Impacts 659 Chapin FS III, BermanM, CallaghanTV, ConveyP, CrepinAS, et al. 2006. Polar systems.In MillenniumEcosystem Assessment, Ecosystems and Human Well-Being, Volume1: CurrentState and Trends,ed. R Hassan,R Scholes,N Ash,pp. 717-43. Washington,DC: Island Press ChapinFS III, ShaverGR, GiblinAE, NadelhofferKG, LaundreJA. 1995. Response ofArctic tundra to experimentaland observed changes in climate.Ecology 76:694- 711 ChuineI, BeaubienE. 2001. Phenologyis a majordeterminant of tree species range. Ecol.Lett. 4:500-10 Coope GR. 1994. The responseof insectfaunas to glacial-interglacialclimatic fluc- tuations.Philos. Trans. R. Soc.London Ser B. 344:19-26 Crick HQ, Dudley C, Glue DE. 1997. UK birds are layingeggs earlier.Nature 388:526 CroxallJP, TrathanPN, MurphyEJ. 2002. Environmentalchange and Antarctic seabirdpopulations. Science 297:1510-14 CrozierL. 2003. Winterwarming facilitates range expansion: cold toleranceof the butterflyAtalopedes campestris. Oecologia 135:648-56 CrozierL. 2004. Warmerwinters drive butterfly range expansion by increasing sur- vivorship.Ecology 85:231-41 Davis MB, ShawRG. 2001. Rangeshifts and adaptiveresponses to quaternaryclimate change.Science 292:673-79 Davis MB, ZabinskiC. 1992. Changesin geographicalrange resulting from green- housewarming: effects on biodiversityin forests.In GlobalWarming and Biological Diversity,ed. TEL Peters,R Lovejoy,pp. 297-308. New Haven, CT: Yale Univ. Press Dennis RLH. 1993. Butterfliesand ClimateChange. Manchester, UK: Manchester Univ.Press DerocherAE. 2005. Populationecology of polar bearsat Svarlbad,Norway. Popul. Ecol.47:267-75 DerocherAE, Lunn NJ, StirlingI. 2004. Polar bears in a warmingclimate. Integr. Comp.Biol. 44:163-76 Descimon H, BachelardP, BoitierE, PierratV. 2006. Decline and extinctionof Parnassiusapollo populations in France-continued.In Studieson theEcology and ConservationofButterflies in Europe(EBIE), ed. E Kiihn,R Feldmann,J Settele. Bulgaria:PENSOFT. In press deYoungB, HarrisR, AlheitJ,Beaugrand G, MantuaN, ShannonL. 2004. Detecting regimeshifts in the ocean: data considerations.Prog. Oceanogr. 60:143-64 DobzhanskyTH. 1943. Geneticsof naturalpopulations. IX. Temporalchanges in thecomposition of populationsof Drosophila pseudoobscura. Genetics 28:162-86 DobzhanskyTH. 1947. A responseof certaingene arrangementsin the thirdchro- mosomeof Drosophilapseudoobscura to natural selection. Genetics 32:142-60 Donner SD, SkirvingWJ, Little CM, OppenheimerM, Hoegh-Guldberg0. 2005. Global assessmentof coral bleachingand requiredrates of adaptationunder climatechange. Glob. Change Biol. 11:2251-65 Doran PT, PriscuJC, Lyons WB, Walsh JE, FountainAG, et al. 2002. Antarctic climatecooling and terrestrialecosystem response. Nature 415:517-22

66o Parmesan Dose V, MenzelA. 2004.Bayesian analysis of climate change impacts in phenology. Glob.Change Biol. 10:259-72 DunnPO, WinklerDW. 1999.Climate change has affected the breeding date of tree swallowsthroughout North America. Proc. R. Soc.London Ser B 266:2487-90 EasterlingDR, MeehlJ, ParmesanC, ChagnonS, KarlTR, MearnsLO. 2000. Climateextremes: observations, modeling, and impacts. Science 289:2068-74 EhrlichPR, Murphy DD, SingerMC, SherwoodCB, WhiteRR, Brown IL. 1980. Extinction,reduction, stability and increase: the responses of checkerspot but- terflypopulations to the California drought. Oecologia 46:101-5 EmslieSD, FraserW, SmithRC, WalkerW. 1998.Abandoned penguin colonies andenvironmental change in the Palmer Station area, Anvers Island, Anatarctic Peninsula.Antarct. Sci. 10:257-68 FergusonSH, StirlingI, McLoughlinP. 2005.Climate change and ringed seal (Phoca hispida)recruitment inwestern Hudson Bay. Mar Mamm.Sci. 21:121-35 FordEB. 1945.Butterflies. London: Collins FordSE. 1996.Range extension by the oyster parasite Perkinsus marinus into the northeasternUnited States: response to climatechange? J. ShellfishRes. 15:45- 56 ForisterML, ShapiroAM. 2003. Climatic trends and advancing spring flight of but- terfliesin lowland California. Glob. Change Biol. 9:1130-35 FraserWR, Trivelpiece WZ, Ainley DC, TrivelpieceSG. 1992.Increases in Antarctic penguinpopulations: reduced competition with whales or a lossof sea ice due to environmentalwarming? Polar Biol. 11:525-31 Garcia-RamosG, KirkpatrickM. 1997.Genetic models of adaptation and gene flow inperipheral populations. Evolution 51:21-28 GastonAJ, Gilchrist HG, HipfnerM. 2005. Climatechange, ice conditionsand reproductioninan Arctic nesting marine bird: Brunnich's guillemot (Uria lomvia L.). J.Anim. Ecol. 74:832-41 GibbsJP, Breisch AR. 2001.Climate warming and calling phenology of frogs near Ithaca,New York, 1900-1999. Conserv. Biol. 15:1175-78 GordoO, BrotonsL, RerrerX, ComassP. 2005.Do changesin climatepatterns in winteringareas affect the timing of the spring arrival of trans-Saharan migrant birds?Glob. Change Biol. 11:12-21 GrabherrG, GottfriedM, PauliH. 1994.Climate effects on mountain plants. Nature 369:448 GrinnellJ. 1917.Field tests of theories concerning distributional control. Am. Nat. 51:115-28 GrossL. 2005.As theAntarctic ice packrecedes, a fragileecosystem hangs in the balance.PLoS Biol. 3(4):e127 GudmundssonF. 1951.The effectsof the recent climatic changes on thebird life of Iceland.Proc. 10th Int. Ornithol. Congr., Uppsala, June 1950, pp. 502-14 GurevitchJ,Hedges LV. 1999.Statistical issues in ecologicalmeta-analyses. Ecology 80:1142-49 HaegerJF. 1999. Danaus chrysippus (Linnaeus 1758) en la PeninsulaIbarica: migra- cioneso dinimicade metapoblaciones?Shilap 27:423-30

www.annualreviews.org* Climate-Change Impacts 661 Hanski I, ErilahtiC, KankareM, OvaskainenO, SirenH. 2004. Variationin migra- tionpropensity among individuals maintained by landscape structure. Ecol. Lett. 7:958-66 Hari RE, LivingstoneDM, SiberR, Burkhardt-HolmP, GiittingerH. 2006. Conse- quences of climaticchange for water temperature and browntrout population in Alpinerivers and streams.Glob. Change Biol. 12:10-26 HarringtonR, Woiwod I, SparksT. 1999. Climatechange and trophicinteractions. TrendsEcol. Evol. 14:146-50 HarrisG. 1964.Climatic changes since 1860 affecting European birds. Weather 19:70- 79 Hays GC, RichardsonAJ, Robinson C. 2005. Climatechange and marineplankton. TrendsEcol. Evol. 20:337-44 Heath J. 1974. A centuryof changesin the lepidoptera.In The ChangingFlora and Fauna ofBritain, ed. DL Hawkesworth,6:275-92. London: Syst.Assoc. Hemp A. 2005. Climatechange-driven forest fires marginalize the impact of ice cap wastingon Kilimanjaro.Glob. Change Biol. 11:1013-23 HicklingR, Roy DB, HillJK,Thomas CD. 2005. A northwardshift of range margins in BritishOdonata. Glob.Change Biol. 11:502-6 Hill GE, SargentRR, SargentMB. 1998. Recentchange in thewinter distribution of RufousHummingbirds. Auk 115:240-45 Hill JK,Thomas CD, Fox R, TelferMG, WillisSG, et al. 2002. Responsesof butter- fliesto twentiethcentury climate warming: implications for future ranges. Proc. R. Soc.London Ser. B 269:2163-71 HillJK,Thomas CD, Lewis OT. 1999.Flight morphology in fragmentedpopulations of a rareBritish butterfly, Hesperia comma. Biol. Conserv. 87:277-84 Hoegh-Guldberg0. 1999. Climate change,coral bleachingand the futureof the world'scoral reefs. Mar. Freshw.Res. 50:839-66 Hoegh-GuldbergO. 2005a. Low coral coverin a high-CO2world. J. Geophys.Res. 110:C09S06 Hoegh-GuldbergO. 2005b. Marine ecosystemsand climatechange. See Lovejoy & Hannah 2005, pp. 256-71 Hoegh-GuldbergO, Jones RJ,Ward S, Loh WK. 2002. Is coral bleachingreally adaptive?Nature 415:601-2 Hoegh-GuldbergO, PearseJS. 1995. Temperature,food availability, and the devel- opmentof marineinvertebrate larvae. Am. Zool.35:415-25 HoffmannAA, BlowsMW. 1994. Species borders:ecological and evolutionaryper- spectives.Trends Ecol. Evol. 9:223-27 Holbrook SJ,Schmitt RJ, Stephens JS Jr. 1997. Changes in an assemblageof tem- peratereef fishes associated with a climaticshift. Ecol. Appl. 7:1299-310 HolmgrenM, SchefferM, EzcurraE, GutierrezJR, Mohren GMJ. 2001. El Nifio effectson the dynamicsof terresrialecosystems. Trends Ecol. Evol. 16:89-94 Holt RD. 2003. On theevolution ecology of species' ranges. Evol. Ecol. Res. 5:159-78 Howell SNG. 2002. HummingbirdsofNorth America. San Diego, CA: Academic Hughes L. 2000. Biologicalconsequences of global warming:Is the signalalready apparent?Trends Ecol. Evol. 15:56-61

662 Parmesan HuntleyB. 1991. How plantsrespond to climatechange: migration rates, individu- alismand theconsequences for the plant communities. J. Bot.67:15-22 Hiippop O, Hiippop K. 2003. NorthAtlantic Oscillation and timingof springmi- grationin birds.Proc. R. Soc.London Ser. B 270:233-40 Innes JL. 1991. High-altitudeand high-latitudetree growthin relationto past, present,and futureglobal climatechange. Holocene 1:168-73 Inouye DW, Barr B, ArmitageKB, Inouye BD. 2000. Climate change is affecting altitudinalmigrants and hibernatingspecies. Proc. Natl. Acad. Sci. USA 97:1630- 33 IPCC (IntergovernmentalPanel ClimateChange). 2001a. ClimateChange 2001: Im- pacts,Adaptation, and Vulnerability,Contribution ofWorking Group II to theInter- governmentalPanel on ClimateChange Third Assessment Report, ed. JJMcCarthy, OF Canziani,NA Leary,DJ Dokken,KS White. Cambridge,UK: Cambridge Univ.Press IPCC (IntergovernmentalPanel ClimateChange). 2001b. ClimateChange 2001: The Scienceof Climate Change, Contribution ofWorking Group I tothe Intergovernmental Panel on ClimateChange Third Assessment Report, ed. JT Houghton,Y Ding, DJ Griggs,M Noguer, PJ van der Linden, X Dai, K Maskell, CA Johnson. Cambridge,UK: CambridgeUniv. Press JacobyGC, D'ArrigoRD. 1995.Tree ringwidth and densityevidence of climatic and potentialforest change in Alaska.Glob. Biogeochem. Cycles 9:227-34 JohnsonT, Dozier J,Michaelsen J. 1999. Climatechange and SierraNevada snowpack.IAHS Publ.256:63-70 JohnstonRF, Niles DM, RohwerSA. 1972. Hermon Bumpusand naturalselection in thehouse sparrowPasser domesticus. Evolution 26:20-3 1 JordanoD, RetamosaEC, FernandezH. 1991. Factorsfacilitating the continued presenceof Colotisevagore (Klug 1829) in southernSpain. J. Biogeogr.18:637-46 JumpAS, PefiuelasJ. 2005. Runningto standstill: adaptation and the responseof plantsto rapidclimate change. Ecol. Lett. 8:1010-20 KaisilaJ. 1962. Immigrationund Expansionder Lepidopterenin Finnlandin den Jahren1869-1960. Acta Entomol. Fenn. 18:1-452 Kalela 0. 1949. Changesin geographicranges in theavifauna of northern and central Europe in responseto recentchanges in climate.Bird-Band. 20:77-103 Kalela 0. 1952.Changes in thegeographic distribution of Finnish birds and mammals in relationto recentchanges in climate.In The RecentClimatic Fluctuation in Finlandand itsConsequences: A Symposium, ed. I Hustichi,pp. 38-51. Helsinki: Fennia KarievaPM, KingsolverJG,Huey RB, eds. 1993.Biotic Interactions and GlobalChange. Sunderland,MA: Sinauer Karl TR, TrenberthKE. 2003. Modern globalclimate change. Science 302:1719-23 Keeling CD, Chin JFS,Whorf TP. 1996. Increasedactivity of northernvegetation inferredfrom atmospheric CO2 measurements.Nature 382:146-49 KirkpatrickM, BartonNH. 1997. Evolutionof a species'range. Am. Nat. 150:1-23 KullmanL. 2001. 20thcentury climate warming and tree-limitrise in the southern Scandesof Sweden.Ambio 30:72-80

www.annualreviews.org* Climate-Change Impacts 663 Kutz SJ,Hoberg EP, Polley L, JenkinsEJ. 2005. Global warmingis changingthe dynamicsof Arctic host-parasite systems. Proc. R. Soc.London Ser. B 272:2571-76 Lapenis A, ShvidenkoA, ShepaschenkoD, Nilsson S, AiyyerA. 2005. Acclimation of Russianforests to recentchanges in climate.Glob. Change Biol. 11:2090-102 Lescop-SinclairK, PayetteS. 1995. Recentadvance of theArctic treeline along the easterncoast of Hudson Bay.J. Ecol.83:929-36 LevitanM. 2003. Climaticfactors and increasedfrequencies of 'southern'chromo- someforms in naturalpopulations of Drosophila robusta. Evol. Ecol. Res. 5:597-604 LewontinRC, BirchLC. 1966. Hybridizationas a sourceof variation for adaptation to new environments.Evolution 20:315-36 LindgrenE, GustafsonR. 2001. Tick-borneencephalitis in Sweden and climate change.Lancet 358:16-18 Logan JA,Regniere J, Powell JA. 2003. Assessingthe impacts of global warmingon forestpest dynamics. Front. Ecol. Environ. 1:130-37 Lovejoy T, Hannah L, eds. 2005. In ClimateChange and Biodiversity.New Haven, CT: Yale Univ.Press LuckmanB, KavanaghT. 2000. Impactof climatefluctuations on mountainenvi- ronmentsin the Canadian Rockies.Ambio 29:371-80 LynchM, Lande R. 1993. Evolutionand extinctionin responseto environmental change.See Karievaet al. 1993,pp. 234-50 MacArthurRM. 1972. GeographicalEcology. New York:Harper & Row MarttilaO, HaahtelaT, AarnioH, OjalainenP. 1990.Suomen Piiivdperhoset. Helsinki: Kirjayhtymii McGowanJA, Cayan DR, Dorman LM. 1998. Climate-oceanvariability and ecosys- temresponse in theNortheast Pacific. Science 281:210-17 Meehl GA, Zwiers F, EvansJ, KnutsonT, Mearns LO, WhettonP. 2000. Trends in extremeweather and climateevents: issues related to modelingextremes in projectionsof futureclimate change. Bull. Am. Meteorol.Soc. 81:427-36 Menzel A. 2000. Trendsin phenologicalphases in Europe between1951 and 1996. Int.J. Biometeorol.44:76-81 Menzel A. 2005. A 500 year pheno-climatologicalview on the 2003 heatwavein Europe assessedby grapeharvest dates. Meteorol. Z. 14:75-77 Menzel A, Dose V. 2005. Analysisof long-term time-series of beginning of flowering by Bayesianfunction estimation. Meteorol. Z. 14:429-34 Menzel A, Fabian P. 1999. Growingseason extendedin Europe. Nature397:659 Menzel A, JakobiG, Ahas R, ScheifingerH, EstrellaN. 2003. Variationsof the climatologicalgrowing season (1951-2000) in Germanycompared with other countries.Int. J. Climatol.23:793-812 MeshinevT, ApostolovaI, Koleva E. 2000. Influenceof warming on timberlinerising: a case studyon Pinuspeuce Griseb. in Bulgaria.Phytocoenologia 30:431-38 Mikkola K. 1997. Population trendsof Finnish Lepidopteraduring 1961-1996. Entomol.Fenn. 3:121-43 Moiseev PA, ShiyatovSG. 2003. The use of old landscapephotographs for study- ing vegetationdynamics at the treelineecotone in the Ural Highlands,Rus- sia. In AlpineBiodiversity in Europe,ed. L Nagy,G Grabherr,C K6rner,DBA Thompson,pp. 423-36. Berlin:Springer-Verlag

664 Parmesan MyneniRB, Keeling CD, TuckerCJ, Asrar G, Nemani RR. 1997. Increasedplant growthin thenorthern high latitudes from 1981 to 1991. Nature386:698-702 NylinS. 1988. Host plantspecialization and seasonalityin a phytophagousbutterfly, Polygoniac-album (Nymphalidae). Oikos 53:381-86 OrrJC, FabryVJ, Aumont O, Bopp L, Doney SC, et al. 2005. Anthropogenicocean acidificationover the twenty-first century and itsimpact on calcifyingorganisms. Nature437:681-86 OttersenG, Planque B, BelgranoA, Post E, Reid PC, StensethNC. 2001. Ecological effectsof theNorth Atlantic Oscillation. Oecologia 128:1-14 ParmesanC. 1996. Climateand species'range. Nature 382:765-66 ParmesanC. 2002. Detectionof range shifts: general methodological issues and case studiesusing butterflies. In FingerprintsofClimate Change: Adapted Behaviour and ShiftingSpecies' Ranges, ed. G-R Walther,CA Burga,PJ Edwards,pp. 57-76. Dordrecht,Netherlands: Kluwer Acad./Plenum ParmesanC. 2003. Butterfliesas bio-indicatorsof climate change impacts. In Evolution and EcologyTaking Flight: Butterflies as Model Systems, ed. CL Boggs,WB Watt, PR Ehrlich,pp. 541-60. Chicago: Univ.Chicago Press Parmesan C. 2005a. Detection at multiplelevels: Euphydryaseditha and climate change.Case study.See Lovejoy & Hannah 2005, pp. 56-60 ParmesanC. 2005b. Range and abundancechanges. See Lovejoy & Hannah 2005, pp. 41-55 ParmesanC, Gaines S, Gonzalez L, KaufmanDM, KingsolverJ, et al. 2005. Em- piricalperspectives on species'borders: environmental change as challengeand opportunity.Oikos 108:58-75 ParmesanC, GalbraithH. 2004. ObservedEcological Impacts of Climate Change in North America.Arlington, VA: Pew Cent. Glob. Clim. Change ParmesanC, MartensP. 2006. Climatechange. In Biodiversity,Health and theEnvi- ronment:SCOPE/Diversitas Rapid Assessment Project, ed. O Sala, L Meyerson,C Parmesan.Washington, DC: Island Press.In press ParmesanC, Root TL, Willig MR. 2000. Impactsof extremeweather and climate on terrestrialbiota. Bull. Am. Meteorol.Soc. 81:443-50 ParmesanC, RyrholmN, StefanescuC, Hill JK, Thomas CD, et al. 1999. Pole- wardshifts in geographicalranges of butterflyspecies associated with regional warming.Nature 399:579-83 ParmesanC, Yohe G. 2003. A globallycoherent fingerprint of climatechange impacts acrossnatural systems. Nature 421:37-42 Pauli H, GottfriedM, GrabherrG. 1996. Effectsof climatechange on mountain ecosystems:upward shifting of mountainplants. World Res. Rev. 8:3 82-90 Paulson DR. 2001. Recentodonata records from southern Florida: effects of global warming?Int. J. Odonatol.4:57-69 PefiuelasJ, Filella I. 2001. Responsesto a warmingworld. Science 294:793-94 PerryAL, Low PJ,Ellis JR, ReynoldsJD. 2005. Climate change and distribution shiftsin marinefishes. Science 308:1912-15 PollardE. 1979.Population ecology and change in rangeof the white admiral butterfly Ladogacamilla L. in England.Ecol. Entomol. 4:61-74

www.annualreviews.org* Climate-Change Impacts 665 PollardE, EvershamBC. 1995. Butterflymonitoring 2: interpretingthe changes.In Ecologyand Conservation ofButterflies, ed. AS Pullin,pp. 23-36. London: Chapman & Hall PostE, LangvatnR, ForchhammerMC, StensethNC. 1999.Environmental variation shapessexual dimorhism in red deer.Proc. Natl. Acad. Sci. USA 96:4467-71 Pounds JA, BustamenteMR, Coloma LA, ConsuegraJA, Fogden MPL, et al. 2006. Widespreadamphibian extinctions from epidemic disease driven by global warming.Nature 439:161-67 PoundsJA, Fogden MPL, CampbellJH.1999. Biologicalresponse to climatechange on a tropicalmountain. Nature 398:611-15 PoundsJA, Fogden MPL, MastersKL. 2005. Responsesof naturalcommunities to climatechange in a highlandtropical forest. Case study.See Lovejoy& Hannah 2005, pp. 70-74 PrechtH, ChristophersenJ, Hensel H, LarcherW. 1973. Temperatureand Life. New York:Springer-Verlag PrechtWF, AronsonRB. 2004. Climateflickers and rangeshifts of reef corals. Front. Ecol.Environ. 2:307-14 Reale D, McAdamA, Outin G, BerteauxS. 2003. Geneticand plasticresponse of a northernmammal to climatechange. Proc. R. Soc.London Ser. B 270:591-96 Reid PC, EdwardsM, Hunt HG, WarnerAJ. 1998. Phytoplanktonchange in the NorthAtlantic. Nature 391:546 RichardsonAJ, Schoeman DS. 2004. Climateimpact on planktonecosystems in the NortheastAtlantic. Science 305:1609-12 Rodriguez-TrellesF, AlvarezG, Zapata C. 1996. Time-seriesanalysis of seasonal changes of the O inversionpolymorphism of Drosophilasubobscura. Genetics 142:179-87 Rodriguez-TrellesF, RodriguezMA. 1998. Rapid micro-evolutionand loss of chromosomal diversityin Drosophilain responseto climatewarming. Evol. Ecol. 12:829-38 Rodriguez-TrellesF, RodriguezMA, ScheinerSM. 1998.Tracking the genetic effects of globalwarming: Drosophila and othermodel systems. Conserv. Ecol. 2:2 RoessigJM,Woodley CM, CechJJ,Hansen LJ.2004. Effectsof global climate change on marineand estuarinefishes. Rev. Fish Biol. Fish. 14:215-75 Roetzer T, WittenzellerM, Haeckel H, NekovarJ. 2000. Phenologyin central Europe: differenceand trendsof springphenophases in urbanand ruralareas. Int.J. Biometeorol.44:60-66 Root TL. 1988. Energyconstraints on avian distributionsand abundances.Ecology 69:330-39 Root TL, Hughes L. 2005. Presentand futurephenological changes in wild plants and animals.See Lovejoy & Hannah 2005, pp. 61-69 Root TL, PriceJT, Hall KR, SchneiderSH, RosenzweigC, PoundsJA. 2003. Fin- gerprintsof globalwarming on wildanimals and plants.Nature 421:57-60 Rowan R. 2004. Thermaladaptation in reefcoral symbionts.Nature 430:742 Roy DB, SparksTH. 2000. Phenologyof British butterflies and climatechange. Glob. ChangeBiol. 6:407-16

666 Parmesan SagarinRD, BarryJP, Gilman SE, BaxterCH. 1999. Climate-relatedchange in an intertidalcommunity over short and long timescales. Ecol. Monogr. 69:465-90 SalomonsenF. 1948. The distributionof birdsand therecent climatic change in the NorthAtlantic area. Dansk.Orn. Foren. Tidsskr. 42:85-99 SchwartzMD. 1998. Green-wavephenology. Nature 394:839-40 SchwartzMD. 1999. Advancingto fullbloom: planningphenological research for the21st century. Int. J. Biometeorol.42:113-18 ScriberJM, Lederhouse RC. 1992. The thermalenvironment as a resourcedictating geographicpatterns of feedingspecialization of insectherbinores. In Effectsof ResourceDistribution on Plant-AnimalInteractions, ed. MR Hunter,T Ohgushi, PW Price,pp 429-66. New York:Academic SeverntyDL. 1977. The use of data on the distributionof birdsto monitorclimatic changes.Emu 77:162-66 Shoo LP, Williams SE, Hero JM. 2006. Detectingclimate change inducesrange shifts:Where and how shouldwe be looking?Aust. Ecol. 31:22-29 Singer MC. 1972. Complex componentsof habitatsuitability within a butterfly colony.Science 176:75-77 SingerMC, EhrlichPR. 1979. Population dynamicsof the checkerspotbutterfly Euphydryaseditha. Fortschr. Zool. 25:53-60 SingerMC, Thomas CD. 1996.Evolutionary responses of a butterflymetapopulation to humanand climate-causedenvironmental variation. Am. Nat. 148:S9-39 SmithAT. 1974. The distributionand dispersalof pikas:influences of behaviorand climate.Ecology 55:1368-76 SmithRC, AinleyD, Kaber K, Domack E, Emslie S, et al. 1999. Marine ecosys- temsensitivity to historicalclimate change in theAntarctic Peninsula. BioScience 49:393-404 SmithRIL. 1994. Vascularplants as bioindicatorsof regional warming in Antarctica. Oecologia99:322-28 SmolJP, Wolfe AP, BirksHJB, Douglas MSV, JonesVJ, et al. 2005. Climate-driven regimeshifts in thebiological communities of Arctic lakes. Proc. Natl. Acad. Sci. USA 102:4397-402 SouthwardAJ, Hawkins SJ, BurrowsMT. 1995. Seventyyears' observationsof changesin distributionand abundanceof zooplanktonand intertidalorganisms in thewestern English Channel in relationto risingsea temperature.J. Therm. Biol.20:127-55 SouthwardAJ, Langmead O, Hardman-MountfordNJ, Aiken J, Boalch GT, et al. 2005. Long-termoceanographic and ecologicalresearch in thewestern English Channel.Adv. Mar. Biol.47:1-105 Sparks TH, Menzel A. 2002. Observed changes in seasons, an overview.Int. J. Climatol.22:1715-26 SparksTH, YatesTJ. 1997.The effectof spring temperature on theappearance dates of Britishbutterflies 1883-1993. Ecography 20:368-74 Spear LB, AinleyDG. 1999. Migrationroutes of sootyshearwaters in the Pacific Ocean. Condor101:205-18 StefanescuC, PeiiuelasJ, Filella I. 2003. Effectsof climatic change on thephenology ofbutterflies in thenorthwest Mediterranean Basin. Glob.Change Biol. 9:1494

www.annualreviews.orgo Climate-Change Impacts 667 StirlingI. 2002. Polar bears and seals in the eastern Beaufort Sea andAmundsen Gulf: a synthesisofpopulation trends and ecological relationships over three decades. Arctic55:59-76 StirlingI, LunnNJ, lacozza J. 1999.Long-term trends in thepopulation ecology of polarbears in western Hudson Bay in relation to climatic change. Arctic 52:294- 306 SturmM, RacineC, TapeK. 2001.Increasing shrub abundance in the Arctic. Nature 411:546-47 SturmM, SchimelJ, Mechaelson G, WelkerJM, Oberbauer SF, et al. 2005.Winter biologicalprocesses could help convert Arctic tundra to shrubland.BioScience 55:17-26 SwetnamTW, BetancourtJL.1998. Mesoscale disturbance and ecological response to decadalclimatic variability inthe American Southwest. J. Clim.11:3128-47 TaylorRH, WilsonPR. 1990.Recent increase and southernexpansion of Adelie penguinpopulations in theRoss Sea, Antarctica, related to climaticwarming. N.Z.J. Ecol.14:25-29 ThomasC. 2005. Recentevolutionary effects of climatechange. See Lovejoy& Hannah2005,. pp. 75-90 ThomasCD, BodsworthEJ, Wilson RJ, Simmons AD, DaviesZG, etal. 2001.Eco- logicaland evolutionary processes at expanding range margins. Nature 411:577- 81 ThomasCD, LennonJJ. 1999. Birds extend their ranges northwards. Nature 399:213 ThomasCD, SingerMC, BoughtonD. 1996.Catastrophic extinction ofpopulation sourcesin a butterflymetapopulation. Am. Nat. 148:957-75 TravisJ,Futuyma DJ. 1993. Global change: lessons from and for evolutionary biology. See Karievaet al. 1993,pp. 234-50 UvarovBP. 1931.Insects and climate. R. Entomol.Soc. London 79:174-86 vanHerk CM, AptrootA, van DobbenHF. 2002. Long-termmonitoring in the Netherlandssuggests that lichens respond to globalwarming. Lichenologist 34:141-54 VanNouhuys S, Lei G. 2004.Parasitoid-host metapopulation dynamics: the causes andconsequences of phenological asynchrony. J.Anim. Ecol. 73:526-35 VisserME, BothC. 2005.Shifts in phenology due to global climate change: the need fora yardstick.Proc. R. Soc.B 272:2561-69 WaltherGR, HughesL, VitousekP, StensethNC. 2005. Consensuson climate change.Trends Ecol. Evol. 20:648-49 WaltherGR, PostE, ConveryP, MenzelA, ParmesanC, et al. 2002. Ecological responsesto recentclimate change. Nature 416:389-95 WardleP, ColemanMC. 1992.Evidence for rising upper limits of fournative NewZealand forest trees. N.Z. J. Bot.30:303-14 WarrenMS. 1992.The conservationofBritish butterflies. In The Ecology ofButterflies inBritain, ed. RLH Dennis,pp. 246-74. Oxford, UK: OxfordUniv. Press WebbT III, BartleinPJ. 1992. Global changes during the last 3 millionyears: climatic controlsand biotic responses. Annu. Rev. Ecol. Syst. 23:141-73 WeiserW, ed. 1973.Effects of Temperature on Ectothermic Organisms. New York: Springer-Verlag

668 Parmesan Weiss SB, MurphyDD, White RR. 1988. Sun, slope and butterflies:topographic determinantsof habitatquality for Euphydryas editha. Ecology 69:1486-96 White MA, Nemani RR, ThorntonPE, RunningSW. 2002. Satelliteevidence of phenologicaldifferences between urbanized and rural areas of the eastern United Statesdeciduous broadleaf forest. Ecosystems 5:260-73 WhiteMA, RunningSW, ThorntonPE. 1999.The impactof growing-season length variabilityon carbonassimilation and evapotranspirationover 88 yearsin the easternUS deciduousforest. Int. J. Biometeorol.42:139-45 WilkinsonCR, ed. 2000. GlobalCoral Reef Monitoring Network: Status of Coral Reefs of theWorld in 2000. Townsville,Qld: Aust.Inst. Mar. Sci. WilliamsonK. 1975. Birdsand climaticchange. Bird Study 22:143-64 WilsonJW,Gutierrez D, MartinezD, AgudoR, MonserratVJ. 2005. Changesto the elevationallimits and extentof species rangesassociated with climate change. Ecol.Lett. 8:1138-46 Wilson PR, AinleyDG, Nur N, JacobsSS, BartonKJ, et al. 2001. Ad6liepenguin populationchange in the pacificsector of Antarctica:relation to sea-ice extent and theAntarctic Circumpolar Current. Mar. Ecol.Prog. 213:301-9 WinderM, SchindlerDE. 2004. Climatechange uncouples trophicSer. interactions in an aquaticecosystem. Ecology 85:2100-6 Woodward FI. 1987. Climateand Plant Distribution.Cambridge, UK: Cambridge Univ.Press

RE LKTEDt RESOU R.C(ES Alford,RA, RichardsSJ. 1999. Global amphibiandeclines: a problemin applied ecology.Annu. Rev. Ecol. Syst. 30:133-65 GlynnPW. 1988. El Nifio-SouthernOscillation 1982-1983: nearshorepopulation, community,and ecosystemresponses. Annu. Rev. Ecol. Syst. 19:309-45 LudwigD, Marc M, Haddad B. 2001. Ecology,conservation, and publicpolicy. Annu. Rev.Ecol. Syst. 32:481-517 SmithSV, BuddemeierRW. 1992. Global changeand coral reefecosystems. Annu. Rev.Ecol. Syst. 23:89-118 StevensGC, Fox JE 1991. The causes of treeline.Annu. Rev. Ecol. Syst. 22:177-91