Review

Ecological Consequences of Recent Climate Change

JOHN P. McCARTY
AAAS Fellow, Global Change Research Program, U. S. Environmental Protection Agency, 401 M Street SW,
Washington, D.C. 20460, U.S.A., and Department of Biology, University of Maryland, College Park, MD 20742,
U.S.A., email jm395@umail.umd.edu

Abstract: Global climate change is frequently considered a major conservation threat. The Earth’s climate
has already warmed by 0.5⬚ C over the past century, and recent studies show that it is possible to detect the ef-
fects of a changing climate on ecological systems. This suggests that global change may be a current and fu-
ture conservation threat. Changes in recent decades are apparent at all levels of ecological organization: pop-
ulation and life-history changes, shifts in geographic range, changes in species composition of communities,
and changes in the structure and functioning of ecosystems. These ecological effects can be linked to recent
population declines and to both local and global extinctions of species. Although it is impossible to prove that
climate change is the cause of these ecological effects, these findings have important implications for conser-
vation biology. It is no longer safe to assume that all of a species’ historic range remains suitable. In drawing
attention to the importance of climate change as a current threat to species, these studies emphasize the need
for current conservation efforts to consider climate change in both in situ conservation and reintroduction
efforts. Additional threats will emerge as climate continues to change, especially as climate interacts with
other stressors such as habitat fragmentation. These studies can contribute to preparations for future chal-
lenges by providing valuable input to models and direct examples of how species respond to climate change.

Consecuencias Biológicas de Cambios Climáticos Recientes

Resumen: El cambio climático global es frecuentemente considerado como una gran amenaza para la con-
servación. Sin embargo, el clima de la tierra ya se ha calentado 0.5⬚ C a lo largo del siglo pasado y estudios
recientes muestran que es posible detectar los efectos de un clima cambiante en los sistemas ecológicos. Esto
sugiere que el cambio global puede ser una amenaza presente y futura para la conservación. Los cambios en
las décadas recientes son aparentes a todos los niveles de organización ecológica: cambios poblacionales y de
historia de vida, sesgos en el rango geográfico, cambios en la composición de especies en comunidades y cam-
bios en la estructura y funcionamiento de ecosistemas. Estos efectos ecológicos pueden estar ligados a dis-
minuciones poblacionales recientes y a la extinción de especies tanto en el ámbito local como global. A pesar
de que es imposible probar que el cambio climático es la causa de estos efectos ecológicos, estos estudios
tienen implicaciones importantes para la biología de la conservación. Ya no es seguro asumir que todo el
rango histórico de una especie permanece apto. Al llamar la atención sobre la importancia del cambio
climático como una amenaza actual para las especies, estos estudios hacen énfasis en la necesidad de esfuer-
zos de conservación contemporáneos que tomen en consideración el cambio climático tanto para esfuerzos
de conservación in situ, como de reintroducción. Emergerán amenazas adicionales en tanto el clima con-
tinúe cambiando, especialmente al interactuar el clima con otros estresores como la fragmentación del hábi-
tat. Estos estudios pueden contribuir en la preparación de desafíos a futuro al proveer datos valiosos para los
modelos y encauzar ejemplos sobre las respuestas de las especies al cambio climático.

Introduction discussed (Markham 1996; Halpin 1997; Sala et al. 2000).

Assessments based on computer models, paleoecologi-
Global climate change is often viewed as a looming con- cal studies of past climate change, and small-scale exper-
servation problem. Possible future implications for con- iments suggest that extensive disruptions of most eco-
servation of species and communities have been widely logical communities are likely under generally accepted
climate scenarios (Intergovernmental Panel on Climate
Address correspondence to University of Maryland address. Change [IPCC] 1996).
320

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McCarty Effects of Recent Climate Change 321

A growing number of studies suggest, however, that of the skewed sex ratio and resulting demographic prob-
global climate changes may not just be a conservation lems created by a warming climate.
problem for the future but may in fact be a current Precipitation levels also have direct effects on species.
threat to species and ecosystems. I review the rapidly ac- Water stress is one of the prime determinants of the dis-
cumulating, direct documentation of changes in species tribution of different vegetation types (Woodward 1987).
and ecosystems linked to global climate change (Hughes Natural systems can change rapidly in response to
2000). changes in precipitation. Distributions of ponderosa
The Earth’s climate has warmed 0.3⬚ to 0.6⬚ C over the pine forest (Pinus ponderosa) and piñon-juniper wood-
last 100 years (IPCC 1996). The rate of change has var- land (Pinus edulis and Juniperus monosperma) in New
ied, with warming occurring most rapidly during the pe- Mexico are sensitive to moisture levels that vary with el-
riods 1925–1944 and 1978–1997 ( Jones et al. 1999). Al- evation (Allen & Breshears 1998). Data from aerial pho-
though an average increase of 0.5⬚ C is significant for tos taken between 1935 and 1975 show a rapid change
many physiological and ecological systems, this single (2 km in ⬍5 years) in the distributions of these two com-
value understates the magnitude of the changes to munities in response to a regional drought (Allen & Bre-
which species have been exposed. Temperature changes shears 1998). Precipitation in the form of snow can have
vary geographically and tend to be greatest during the negative effects on browsing and grazing animals such
coldest months (Easterling et al. 1997). Between 1950 as muskoxen (Ovibos moschatus) and deer, making it
and 1993, for example, winter minimum temperatures more difficult for them to find food and avoid predators
rose almost 3⬚ C and spring maximum temperatures in- (Forchhammer & Boertmann 1993; Post & Stenseth 1999).
creased 1.4⬚ C in the northern hemisphere (Easterling et For many species, climate has indirect effects through
al. 1997 ). Changes in precipitation have also occurred the sensitivity of habitat or food supply to temperature
(IPCC 1996). and precipitation. For example, increases in winter
The observation that climate is already changing has snow depth on Isle Royale associated with the North At-
promoted reevaluation of long-term data sets. A number lantic oscillation result in grey wolves (Canis lupus)
of high-profile papers have resulted, establishing a plau- hunting in larger packs (Post et al. 1999). These larger
sible link between recent changes in climate and ob- packs reduce the population size of moose (Alces alces),
served changes in species and communities (e.g. Parme- which in turn allows higher productivity of balsam fir
san 1996; Brown et al. 1999; Parmesan et al. 1999; (Abies balsamea) (Post et al. 1999). Likewise, warming
Pounds et al. 1999; C. D. Thomas & Lennon 1999). climate may allow northward expansion of red fox ( Vulpes
Given the unavoidable constraint on establishing a defin- vulpes), which outcompetes arctic fox (Alopex lagopus)
itive causal link between large-scale climate patterns and (Hersteinsson & Macdonald 1992).
species and communities, the overall picture provided Climate variability and the frequency and magnitude
by the combination of these studies is needed to best of extreme events may also be changing (IPCC 1996;
evaluate the insights this emerging body of work can Easterling et al. 2000). Species and ecosystems respond
provide to conservation biology. to events such as storms (Mehlman 1997), drought
(Grant 1986; Allen & Breshears 1998), and periodic,
complex climate shifts such as the North Atlantic oscilla-
The Role of Climate in the Ecology of Species tion and the El Niño southern oscillation (ENSO) in the
Pacific (Barber & Chavez 1983; Chavez et al. 1999).
Climate has far-reaching effects on species and ecosys- The response of species to interannual or geographic
tems (Andrewartha & Birch 1954). The direct effects of variations in climate are well documented. Responses to
temperature on the physiology of organisms are well long-term directional trends in climatic conditions such
documented, and many mechanisms of action have been as those experienced in recent decades are most rele-
identified (Wieser 1973; Woodward 1987; Wood & Mc- vant to understanding the conservation implications of
Donald 1996). Some effects of temperature may present global climate change now and in the future.
unexpected challenges to conservation. For example,
the sex of developing turtle embryos is determined by
environmental temperature (Bull 1980). Painted turtle Recent Ecological Changes and the Link to
(Chrysemys picta) eggs raised under warmer conditions
Climate Change
produce female offspring, whereas males are produced
under cooler conditions ( Janzen 1994). Interannual dif- Changes in Populations and Reproductive Biology
ferences in the sex ratio of offspring produced are ex-
plained largely by variation in mean temperature in July Climatic warming during the past century may have sig-
( Janzen 1994). Janzen’s evidence indicates that under nificant effects on the population and reproductive biol-
some climate-change scenarios, painted turtles will suf- ogy of organisms. Recent population dynamics of dippers
fer local extinctions in the near future, solely as a result (Cinclus cinclus) in southern Norway have been heavily

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322 Effects of Recent Climate Change McCarty

influenced by climate, especially a trend toward warmer (Table 1). In the United Kingdom, systematic data on
winters which appears to allow easier access to foraging bird nesting has been collected for 60 years. From 1971
streams and subsequent increases in population size to 1995, 78% of 65 species examined started breeding
(Sæther et al. 2000). In Germany, Pied Flycatchers earlier (Crick et al. 1997). Within individual species,
(Ficedula hypoleuca) have undergone long-term changes there were significantly earlier breeding dates, averaging
in reproductive success associated with a springtime 9 days earlier in the spring (Crick et al. 1997). Tempera-
warming of 1.3⬚ C (Winkel & Hudde 1997). Both clutch ture and precipitation explain most of the variation in
size and the number of surviving offspring were higher in the timing of breeding (Crick & Sparks 1999).
warmer springs (Winkel & Hudde 1997), and a popula- Studies of the population biology of individual bird
tion breeding in Finland increased egg-laying effort in re- species also support this trend toward earlier breeding
cent, warmer years ( Järvinen 1994). Reed Warblers (Ac- (Table 1). Great Tits ( Parus major) in the United King-
rocephalus scirpaceus) in southern Germany have also dom and Germany now breed up to 10 days earlier
shown a greater tendency to produce young early in the than in 1970, when the region’s spring warming trend
season as spring temperatures have warmed (Bergmann began (Winkel & Hudde 1997; McCleery & Perrins
1999). In contrast, the average clutch size of arctic-breed- 1998). In the Canadian Arctic, breeding of Snow Goose
ing geese declined during the warming period from 1951 (Chen caerulescens) and Canada Goose (Branta ca-
to 1986 (MacInnes et al. 1990). nadensis) populations advanced by 30 days from 1951
The abundance of Sooty Shearwaters (Puffinus gri- to 1986 (MacInnes et al. 1990), whereas Mexican Jays
seus) declined by 90% off western North America be- (Aphelocoma ultramarina) in Arizona started nesting
tween 1987 and 1994 (Veit et al. 1996, 1997), associated 10 days earlier between 1971 and 1997 (Brown et al.
with a rapid warming of the California current. Periodic 1999).
changes in ocean temperature such as those associated One of the best examples of phenological change in a
with El Niño have widespread ecological effects (Barber single species is the advance in breeding date in Tree
& Chavez 1983). Increases in nearshore water tempera- Swallows ( Tachycineta bicolor). Dunn and Winkler
tures along the California Coast are associated with sig- (1999) used nest records collected across much of the
nificant changes in the population sizes of intertidal in- Tree Swallow’s range to document a shift in breeding
vertebrates (Barry et al. 1995). The role of atmospheric date of 5–9 days earlier in the season between 1959 and
warming in determining the frequency and magnitude 1991. Laying date was correlated with local tempera-
of these changes remains uncertain (IPCC 1996). tures and changed most rapidly during the 1960s and
In the Antarctic, temperature increases have caused 1980s (Dunn & Winkler 1999). This example empha-
dramatic changes in ice cover, which in turn have had sizes that phenological changes within a species influ-
far-reaching effects on animals such as penguins (Taylor enced by local conditions can produce patterns at conti-
& Wilson 1990; Fraser et al. 1992; R. C. Smith et al. nental scale.
1999). This warming trend is the likely explanation for Long-term data on the timing of bird migration is also
the increase in numbers of individuals and populations available. In New York, records of spring arrival for 76
of terrestrial plants in the Antarctic since the mid-1960s species of migrating landbirds date back to 1903 (Oglesby
(R. I. L. Smith 1994). & Smith 1995). Over a 90-year period, 39 species arrived
Recent climate change is linked to both increases and significantly earlier, 35 species showed no significant
declines in population size. The implications for conser- changes, and only 2 species arrived later in the spring
vation of the direction of change will depend on the spe- (Oglesby & Smith 1995). In Wisconsin, arrival of birds
cies and the effects on community interactions. Rapid during spring migration and date of first song has be-
declines in population are of direct concern. Increases come significantly earlier over the past 61 years for 8
in valued species (Dennis & Shreeve 1991) will likely be species, whereas only 1 species has started arriving
offset by population increases in groups such as invasive later (Bradley et al. 1999). An additional 7 species have
exotics (Bergstrom & Chown 1999; Dukes & Mooney shown trends toward earlier arrival. For some European
1999), disease vectors (Lindgren et al. 2000), and agri- passerines, fall migration is also occurring later in the
cultural pests (Cammell & Knight 1992; Whittaker & season (Gatter 1992; Bezzel & Jetz 1995).
Tribe 1998; Tenow et al. 1999). Negative effects of fur- Changes in phenology are not limited to birds (Table
ther increases in already abundant, aggressive species 1). Records of British butterfly species indicate that tim-
will likely overwhelm any benefits of climate change. ing of the first observation has changed along with cli-
mate (Sparks & Carey 1995; Sparks & Yates 1997). The
time of appearance of crop pests has also been moni-
Changes in Phenology tored in many areas. Analysis of data from the Rotham-
stead Insect Survey Network in Great Britain shows that,
A number of studies have documented long-term changes over 25 years, the flight period of five species of aphids
in phenology which may be caused by global change has become 3–6 days earlier (Fleming & Tatchell 1995).

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McCarty Effects of Recent Climate Change 323

Table 1. Ecological changes attributed to recent climate change.a

Variable observed Species observed Change Time spanb (years) Reference

Geographic range 59 bird species 18.9 km 20 C. D. Thomas & Lennon 1999
Geographic range Edith’s checkerspot butterfly 92 km 100 Parmesan 1996
Geographic range speckled wood butterfly 88–149 km 55 Hill et al. 1999
Geographic range 22 butterfly species 35–240 km 30–100 Parmesan et al. 1999
Elevational range 9 plant species 70–360 m 70–90 Grabherr et al. 1994
Breeding range Adelie Penguin 3 km 10 Taylor & Wilson 1990
Flowering date 6 wildflower species 19.8 days 50 Oglesby & Smith 1995
Flowering date 36 species 8.2 days 61 Bradley et al. 1999
Flight period 5 aphid species 3–6 days 25 Fleming & Tatchell 1995
Spawning date 2 frog species 14–21 days 17 Beebee 1995
Breeding migration 3 newt species 35–49 days 17 Beebee 1995
Breeding date 20 bird species 8.8 days 25 Crick et al. 1997
Breeding date 3 bird species 3–9 days 25 Winkel & Hudde 1997
Breeding date Pied Flycatcher 13 days 24 Slater 1999
Breeding date Tree Swallow 5–9 days 33 Dunn & Winkler 1999
Breeding date Great Tit 11.9 days 27 McCleery & Perrins 1998
Breeding date 2 bird species 30 days 35 MacInnes et al. 1990
Breeding date Mexican Jay 10.1 days 27 Brown et al. 1999
Migration date 4 bird species 11.9 days 50 Mason 1995
Migration date 39 bird species 5.5 days 50 Oglesby & Smith 1995
Migration date American Robin 14 days 19 Inouye et al. 2000
Migration date/first song 19 bird species 4.4 days 61 Bradley et al. 1999
End of hibernation yellow-bellied marmot 23 days 23 Inouye et al. 2000
Growing season Europe 10.8 days 34 Menzel & Fabian 1999
Growing season northern hemisphere 12 ⫾ 4 days 9 Myneni et al. 1997
Growing season northern hemisphere 7 days 20 Keeling et al. 1996
a
Only examples where the magnitude of change was estimated are included; some papers may have discussed additional species for which esti-
mates of the rate of change could not be calculated. Means for studies with multiple species may include species showing no response or re-
sponse counter to that predicted by climate warming.
b
Length of record examined.

Breeding of amphibians is also starting earlier in the tory events. For some species, shifting activities to a
spring. Based on 17 years of data on frogs and newts in cooler time of year may be a sufficient response to cli-
the United Kingdom, Beebee (1995) showed that migra- mate change. But it is not safe to assume that this will be
tion of breeding ponds and spawning dates has occurred a general pattern. Timing of life-history events depends
2–7 weeks earlier in recent years (Beebee 1995). on factors besides temperature, and a shift in phenology
The first appearance of spring wildflowers and the may disrupt important correlations with other ecologi-
leafing out of trees is strongly correlated with annual cal factors. Species that regularly move between habitats
variations in climate, although long-term directional trends may need to adjust to climate changes that are occurring
are not always evident (Fitter et al. 1995; Sparks & Carey at different rates in different areas, such as between high
1995). Oglesby and Smith (1995) found that the flower- and low elevations (Inouye et al. 2000).
ing dates of spring wildflowers in New York showed a Plant-animal interactions such as pollination and seed
directional trend consistent with climate warming dur- dispersal depend on synchrony between species. Spe-
ing this century. In 6 of the 15 species with available data, cies depend on the appearance of specific foods at criti-
blooming had advanced at a rate of 20 days per 50 years, cal times (Fitter et al. 1995; Sparks & Carey 1995; Sparks
and no species flowered significantly later (Oglesby & & Yates 1997). For many systems, species will respond
Smith 1995). In Wisconsin, 10 plants began flowering to climate change at similar rates and maintain syn-
significantly earlier between 1936 and 1998, and none chrony (Buse & Good 1996), whereas for other species
flowered significantly later in the season (Bradley et al. the loss of synchrony may have detrimental effects. In
1999). There was a trend toward early flowering in an the Netherlands, warmer springs have resulted in a mis-
additional 15 plants, whereas eleven species showed match between the time of peak availability of insects
nonsignificant trends toward later flowering (Bradley and the peak food demands of nestling Great Tits (Visser
et al. 1999). et al. 1998). In this population, the birds have not begun
At first glance, it may seem that changes in phenology breeding earlier, even though consistent warming over
are relatively benign. Indeed, these results even indicate 23 years has resulted in the peak availability of the in-
that many species have some capacity to respond rap- sects they eat occurring 9 days earlier (Visser et al.
idly to climate changes by altering the timing of life-his- 1998). Disruptions such as this will reduce the ability of

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324 Effects of Recent Climate Change McCarty

threatened species to cope with other environmental In mountains, climate changes more rapidly with ele-
stresses. vation (about 1⬚ C per 160 m) than it does with latitude
(about 1⬚ C per 150 km; IPCC 1996), so rapid changes
in montane communities are expected as climate changes.
Changes in Geographic Range Grabherr et al. (1994) surveyed montane plants on 26
mountain summits in the Swiss Alps and compared spe-
Climate is an important determinant of geographic range cies distributions to historical records. The relationship
for many species (Andrewartha & Birch 1954; Iverson & of species richness to elevation showed a pronounced
Prasad 1998; Venier et al. 1999). Recent northward shift to higher elevations over the past 40–90 years,
movements of species’ range boundaries consistent with consistent with the effects of warming (Grabherr et al.
climate warming have been observed in birds (Thomas & 1994). For 9 species for which they have more detailed
Lennon 1999), mammals (Payette 1987; Hersteinsson & records, the rate of upward shift was estimated to be
Macdonald 1992), and butterflies (Dennis 1993; Parme- 1–4 m per decade. These movements were slower than
san 1996; Hill et al. 1999; Parmesan et al. 1999). the 8–10 m per decade expected based solely on the
Northward expansion of bird species in North Amer- change in mean temperature over the last 90 years and
ica and Europe has been widely observed over the past may indicate that these plants are unable to respond
50 years (Kalela 1949; Williamson 1975; Brewer 1991; successfully to more rapid climate change (Grabherr et
Johnson 1994; Burton 1995; Root & Weckstein 1995). al. 1994).
Although numerous factors have been proposed that Other montane habitats may also be showing the ef-
might explain these range expansions, C. D. Thomas fects of climate change. Dieback of montane trees (Ham-
and Lennon (1999) present compelling evidence linking burg & Cogbill 1988; Fisher 1997) are consistent with
northward movements of British birds to climate change. the effects of warming climate. Climate change in the
The authors compared the breeding ranges of birds in montane cloud forests of Costa Rica (Still et al. 1999)
1968–1972 to ranges in 1988–1991. Of 59 species occu- have been accompanied by the loss of many cloud-forest
pying southern Great Britain, the northern boundary of species and invasion by species from lower elevations
their ranges shifted an average of 19 km to the north (in- (Pounds et al. 1999). Parmesan (1996) also documented
cluding those species showing no changes or southward an upward shift of 124 m in the distribution of Edith’s
retractions). Birds confined to the north (42 species) checkerspot butterfly, primarily in the Sierra Nevada
showed little change in the southern boundary of their mountains.
ranges (C. D. Thomas & Lennon 1999). This comparison
shows that the northern and southern range boundaries
Community- and Ecosystem-Level Changes
of species are not equally sensitive to climate change. By
statistically controlling for changes in total range size, Broad patterns of terrestrial vegetation types are deter-
Thomas and Lennon also provide evidence that the mined largely by a combination of temperature and pre-
northward shift in range is not simply a result of an over- cipitation (Woodward 1987; IPCC 1996). Vegetation is
all expansion of species into the central part of the is- sensitive to changes in temperature occurring on the
land (C. D. Thomas & Lennon 1999). scale of years and decades ( Jacoby et al. 1996). Experi-
Parmesan et al. (1999) examined changes in the north- mental studies indicate that plant communities are also
ern range boundaries of 52 species of European butter- sensitive to the direct effects of higher carbon dioxide
flies over the past 30–100 years. The northern bound- (CO2 ) concentrations (McLeod & Long 1999). Changes
aries of geographic ranges showed northward shifts in 34 in climate associated with the rise in CO2 may in part ex-
species, southward shifts in 1 species, and no change in plain recently observed changes in arctic (Oechel et al.
the remaining 17 species. The southern boundaries of 1993; Chapin et al. 1995), temperate (Hamburg & Cog-
species’ ranges were more stable over time. Of 40 spe- bill 1988; Brown et al. 1997; Alward et al. 1999), and
cies for which Parmesan et al. had appropriate data, 9 tropical (Phillips 1996) plant communities.
shifted north, 2 moved south, and 29 remained stable. Changes in precipitation patterns in the arid regions
Changes in other environmental factors, especially land of the southwestern United States have resulted in a
use, also influence the distribution and abundance of but- shift at some sites from arid grassland to desert shrub-
terflies (Pollard & Eversham 1995). Although explana- land, accompanied by the local extinction of several for-
tions not linked to climate cannot be ruled out, Parmesan merly abundant species of animals (Brown et al. 1997).
et al. (1999) omitted from analyses species with large In the shortgrass steppe of northeast Colorado, average
habitat losses or gains or species known to have been se- temperatures have risen 1.3⬚ C since 1970, largely be-
verely affected by habitat alteration. Parmesan et al. cause of a rapid increase in nighttime temperatures (Al-
(1999) also assert that habitat loss has actually been ward et al. 1999). Measurements of the annual net pri-
higher in the north than the south, indicating that in this mary productivity of the dominant native grass in this
case habitat loss is not driving changes in species’ ranges. habitat, Bouteloua gracilis, reveal a significant decline

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McCarty Effects of Recent Climate Change 325

over this period. Bouteloua gracilis accounted for 90% of lake-ice phenology (Anderson et al. 1996). Data from
of the groundcover in this ecosystem, and the magni- the Experimental Lakes Area of northwestern Ontario re-
tude of the decline in productivity (about one-third for veal a 2⬚-C increase in air and water temperatures since
each 1⬚ C of warming) suggests that major disruptions in the late 1960s (Schindler et al. 1990, 1996a). Associated
both ecosystem structure and functioning could result with this warming are changes in both physical and bio-
from further warming (Alward et al. 1999). Broadleaf logical characteristics of lakes.
plants showed the opposite trend in primary productiv- Significant increases in nearshore ocean-water temper-
ity and increased in abundance over time (Alward et al. atures have occurred over the last 60 years in California.
1999). The shift in species composition from drought- Barry and colleagues (1995) compared detailed records
and grazing-tolerant grass to intolerant forbs could also of the invertebrates of the rocky intertidal zone col-
reduce the value of these areas for livestock grazing. Ex- lected in the early 1930s to data collected at the same
otic species responded favorably to warming, raising the sites in the 1990s. Forty-five of the most abundant spe-
possibility of further invasions of the community by non- cies were classified as being near either the southern or
native weeds (Alward et al. 1999). northern limit of the range or as being cosmopolitan in
At an ecosystem level, increased activity of northern distribution. Over 60 years, eight of the nine southern
vegetation has been detected in measurements of global species increased in abundance, and five of the eight
CO2 concentration (Keeling et al. 1996). Seasonal northern species declined, but cosmopolitan species
growth of plants, especially in the high latitudes of the showed no overall trend (Barry et al. 1995). Although
northern hemisphere, results in a pattern of decreasing average water temperatures increased 0.75⬚ C overall,
atmospheric CO2 levels in summer as photosynthetic ac- this underestimates the increased heat stress northern
tivity removes CO2, followed by increasing CO2 in win- species suffered, as maximum summer temperatures in-
ter as plants respire and vegetation decays. Interannual creased by 2.2⬚ C. Near-shore ocean warming is also im-
differences in the amplitude of the CO2 cycle correlate plicated in similar changes in the reef-fish assemblage off
with temperature changes over the past 35 years, sug- southern California, where southern species have tended
gesting that plant growth at the ecosystem and global to replace northern ones (Holbrook et al. 1997).
scales are sensitive to temperature (Keeling et al. 1996). Open-ocean ecosystems have also responded to tem-
Since the early 1960s the amplitude of this seasonal CO2 perature changes on several scales (Aebischer et al.
cycle has increased by as much as 40%, suggesting in- 1990; Hayward 1997). Surveys off southern California
creased activity of terrestrial vegetation over time (Keel- since 1951 have shown an 80% decrease in the biomass
ing et al. 1996). This has occurred during a period of in- of macrozooplankton in conjunction with a long-term in-
creasing temperatures, especially in the northern spring crease of 0.8–1.5⬚ C in ocean surface temperature (Roem-
( Jones et al. 1999). The changes in the CO2 cycle likely mich & McGowan 1995). Declining zooplankton may in
reflect a combination of increased plant growth and in- turn be responsible for declines in species at higher
creased respiration (Chapin et al. 1996; Keeling et al. trophic levels, such as sea birds (Veit et al. 1996, 1997).
1996). Similar changes have also been detected in the North
Some of the change in primary productivity can be at- Sea (Aebischer et al. 1990). Long-term data are needed
tributed to longer growing seasons evident from several to distinguish between the effects of long-term climate
independent data sources (Table 1). The phase of the trends and periodic events such as El Niño (McGowan
CO2 cycle has shifted approximately 7 days earlier in the et al. 1998; Mullin 1998).
spring, indicating an increase in the length of the grow-
ing season (Keeling et al. 1996). Likewise, meteorologi-
cal satellites over the northern hemisphere measure
The Risk of Extinction
changes in reflectance showing an increase in the grow-
ing season of approximately 12 days since the early The contribution of climate change to future extinctions
1980s, primarily due to an advance in the onset of spring depends on how quickly species can respond to change.
by about 8 days (Myneni et al. 1997). Finally, observa- Ongoing climate change is an additional source of stress
tions of plant phenology in Europe suggest a 10.8-day for species already threatened by local and global environ-
lengthening of the growing season, including an ad- mental changes, increasing the risk of extinction.
vance in spring of 6 days and a delay in autumn of 4.8 Concerns have been raised about possible global de-
days (Menzel & Fabian 1999). These independent meth- clines in amphibian populations (Blaustein & Wake
ods provide a surprisingly consistent picture, strength- 1990). Population sizes of amphibians are sensitive to
ening the conclusion that growing seasons are getting fluctuations in the amount and timing of precipitation.
longer (Table 1). Drastic declines in populations of frogs in Puerto Rico
Long-term data on lakes in the northern hemisphere are correlated with recent years of low precipitation
reflect the ongoing trend toward a warmer climate. (Stewart 1995). Recent climate change may be directly
Moderating winter climate is clearly reflected in records responsible for the extinction of the golden toad ( Bufo

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326 Effects of Recent Climate Change McCarty

periglenes) from the Costa Rican cloud forest (Pounds Biotic Changes and Global Climate Change
& Crump 1994; Pounds et al. 1999). The sudden extinc-
tion of this species was associated with unusually warm The twentieth century saw an increase in the human
and dry conditions that also resulted in the local extinc- population from 1.6 billion to over 6.0 billion. Human ef-
tion of the harlequin frog (Atelopus varius) and drastic fects on the environment have increased at least as fast as
declines in populations of other species (Pounds & population, so the ecological systems described here
Crump 1994; Pounds et al. 1997). The failure of popula- have been subject to rapid changes in many aspects of
tions to recover from the rapid declines that occurred their environments in addition to changes in climate.
in the late 1980s suggests that long-term changes in cli- None of the ecological studies reviewed here can
mate are responsible (Pounds et al. 1997; Still et al. demonstrate that climate change has caused the recent
1999). changes in species and communities described (Hughes
Global warming may also be indirectly linked to am- 2000). Indeed, most authors have gone to considerable
phibian declines resulting from UV radiation (Blaustein effort to point out alternative explanations for these pat-
et al. 1995). Increasing temperatures are associated with terns. These studies do present plausible arguments for
decreases in dissolved organic carbon in lakes, which re- recent climate change as a primary agent of the ecologi-
sult in increased penetration of UV-B radiation (Schindler cal changes observed. Perhaps the strongest support for
et al. 1996b). This effect may lead to greater increases in the role of climate change comes from the remarkable
exposure to UV-B radiation than would be associated consistency in the types and magnitude of changes ob-
with decreases in stratospheric ozone alone ( Herman served across multiple studies (Table 1).
et al. 1996; Schindler et al. 1996b). The strengths of individual studies can provide impor-
Climate acts locally, and its effects will be most appar- tant guides for future analyses. Significant regional differ-
ent on the level of populations and metapopulations. ences exist in both past and expected future climate
Parmesan (1996) provides a clear picture of what may changes (IPCC 1996). Analyses need to incorporate lo-
become a familiar pattern. Shifts in a species’ range un- cal climate records when used to interpret recent eco-
der climate change will occur in part as a result of an in- logical changes. For example, four boreal species of
crease in the probability of more southerly populations small mammals in the central plains of North America
going extinct. In western North America, Edith’s check- expanded southward during the 1960s and 1970s (Frey
erspot butterfly ( Euphydryas editha) is distributed in 1992). This may appear to contradict the general trend
discrete populations that undergo periodic extinctions of poleward expansion described here, but in fact re-
and recolonizations (Harrison et al. 1988). Climate is gional climate data show a marked trend toward cooler
known to play an important role in determining the per- temperatures from the 1930s to the 1980s (Frey 1992).
sistence of populations (Singer & Thomas 1996; C. D. Likewise, in England, the present warming trend was
Thomas et al. 1996). Parmesan (1996) used museum preceded by a period of cool spring temperatures lasting
specimens and other historical records to locate and re- into the 1970s, and laying dates of birds reflect this pat-
survey 151 sites that had once hosted populations of tern (Crick & Sparks 1999).
Edith’s checkerspot. Population extinction rates were Although studies of individual species contribute to
higher in the southern part of the species’ historic the overall argument that recent climate change is hav-
range and at low elevations (Parmesan 1996). The re- ing effects, analyses of groups of organisms or entire
sult of this nonrandom pattern of extinctions was a shift communities provide more powerful tests. Ecosystems
in the species’ distribution of 124 m upward in eleva- are dynamic systems that show variation over time, even
tion and approximately 92 km north over the same time in the absence of human disturbance. Thus, even in the
period that isotherms in western North America shifted absence of climate change, we expect some species to
105 m upward and 105 km north (Parmesan 1996; move poleward, some to breed earlier, and others to in-
Parmesan et al. 1999; Parmesan 2001). The recognition crease or decrease in population size. This problem will
of the role of local extinctions and the importance of be compounded if studies that show results consistent
metapopulation dynamics in range shifts in response to with climate change are more likely to be published.
climate change is especially relevant given the local fo- Several of the studies presented here address this poten-
cus of many conservation efforts. Global extinctions as tial problem by analyzing changes in all members of a
a result of climate change can be expected, as demon- taxon within a region and find an overall change consis-
strated by the fate of the golden toad. But loss of local, tent with the predicted effects of global climate change,
familiar species and species serving important ecologi- even after averaging in species showing no changes or
cal roles may become the rule. This becomes a problem changes counter to those predicted (Oglesby & Smith
for conservation biology because stakeholders value lo- 1995; Crick et al. 1997; Parmesan et al. 1999; C. D. Thomas
cal species and because lost species are most likely to & Lennon 1999). In addition, those datasets that provide
be replaced by exotic, invasive species (Dukes & continuous records of how ecological variables have
Mooney 1999). changed will be most convincing, whereas those data-

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Volume 15, No. 2, April 2001
McCarty Effects of Recent Climate Change 327

sets providing only a “snapshot” of conditions in the past cific months (Beebee 1995; Sparks & Yates 1997; Brown
compared with current conditions will be most subject et al. 1999) are ecologically important but not obvious
to alternative explanations (Hughes 2000). targets of modeling efforts. Third, the amount and sea-
sonality of precipitation is likely to be at least as impor-
tant as temperature in determining the distribution and
Climate Change and Conservation abundance of organisms. To date, predictions of changes
in precipitation are less reliable than those for tempera-
Even as the significance of these results for global- ture. Coping with this uncertainty will increase the chal-
change biology may still be argued, the implications for lenges associated with managing species under chang-
conservation and resource management are clear. To- ing environmental conditions. Fourth, empirical studies
gether, these studies emphasize that conservation scien- should emphasize the importance of the indirect effects
tists need to look at climate change as a current, not just of climate on species (McKone et al. 1998; Visser et al.
a future, threat to species. Although a causal link to cli- 1998; Buse et al. 1999). Of special concern for conserva-
mate cannot yet be rigorously demonstrated, the consis- tion are possible changes in the abundance and range of
tent patterns indicate that the prudent course for con- pests and pathogens (McNulty et al. 1998; Harvell et al.
servation is to take these changes seriously. Certainly, 1999; Lindgren et al. 2000).
cases such as the extinction of the golden toad are of im- Although models provide guidance about the types
mediate concern, but changes in climate need to be and magnitude of changes to be expected, the studies I
taken into account as a possible factor contributing to have reviewed provide direct examples of what conser-
declines in other species. vation biologists can expect to see in the coming de-
Planning for the conservation of particular species or cades and identify areas where further research is
communities should take into account the fact that cli- needed.
mate change is ongoing. The assumption that conditions These studies demonstrate the wide range of re-
in the historic range of a species are still present will be sponses that species may have to climate changes, includ-
increasingly challenged. Additions to ongoing conserva- ing shifts in geographic range and in timing of life-his-
tion efforts include (1) explicit analysis of climatic re- tory events. An obvious gap to date is the dearth of
sponses, including recent changes in climate, when de- studies examining evolutionary changes. The calcula-
cisions are made about where to reintroduce species tions of Janzen (1994) of the evolutionary potential of
( Lindenmayer et al. 1991; Pearce & Lindenmayer 1998); turtles provides a good example of a starting point. The
(2) evaluation of physiological responses to climate to amount of genetic variation within populations and the
ensure that in situ conservation efforts are directed at heritability of responses to climate-based selection will
appropriate sites ( J. A. Thomas et al. 1999); (3) recogni- vary greatly and will have enormous implications for the
tion of the importance of relatively small changes in cli- rate of evolutionary change (Billington & Pelham 1991;
mate to species reproduction and survival, with empha- Hairston 1996; Rodríguez-Trelles & Rodríguez 1998;
sis on the need for conserving microclimatic variation Hayes & O’Connor 1999). Creative efforts are needed,
within habitat types (Weiss et al. 1988; Kindvall 1996; perhaps taking advantage of stored seeds and natural
J. A. Thomas et al. 1999); and (4) increased efforts to seed banks, repeating physiological measurements of
monitor invasive species from warmer climates and slow thermal response from published studies, or examining
migration to higher latitudes or elevations (Dukes & genetic changes in species exposed to thermal pollution
Mooney 1999). from power plants.
The available evidence indicates that changes in the The rate at which species’ boundaries can change is
Earth’s climate will likely continue and even accelerate thought to be of key importance to understanding how
over the next 50–100 years (IPCC 1996). Accurate pre- species will respond to climate change. Past efforts have
dictions of how species and ecosystems will respond to focused on trying to infer rates of change from fossil pol-
climate change will assist in preparing for future conser- len or other indirect indicators. Studies of the type I
vation challenges. The direct observations of species’ re- have reviewed provide a direct measure of the minimum
sponses to climate change that I have reviewed will rate at which species’ boundaries can change. The abil-
complement models, small-scale experiments, and paleo- ity of butterflies to move 35–240 km during a period
ecology studies in several ways. First, predictions of eco- when isotherms shifted 120 km shows that many spe-
logical models can be evaluated by simulating recent cies are capable of matching the recent rate of climate
ecological changes in much the same way climate mod- change (Parmesan et al. 1999), but it doesn’t preclude
els have been evaluated by simulating recent climate. faster change. Additional work is needed to understand
Second, ecologically relevant climate variables can be factors limiting the rate at which geographic range
identified for future models. Variables such as dry-season shifts.
mist frequency (Pounds et al. 1999), minimum spring Studies of groups of species show that most, but not
temperature (Alward et al. 1999), or temperature in spe- all, species are responding to climate change; attention

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Volume 15, No. 2, April 2001
328 Effects of Recent Climate Change McCarty

needs to be directed toward those species not respond- Allen, C. D., and D. D. Breshears. 1998. Drought-induced shift of a for-
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arid ecosystem in response to recent climate change. Proceedings
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of Science, the National Center for Environmental As- Brown, J. L., S. H. Li, and N. Bhagabati. 1999. Long-term trend toward
sessment of the Environmental Protection Agency, and earlier breeding in an American bird: a response to global warm-
the University of Maryland Department of Biology for ing? Proceedings of the National Academy of Science of the United
States of America 96:5565–5569.
support during preparation of this paper. In particular, I Bull, J. J. 1980. Sex determination in reptiles. Quarterly Review of Biol-
am grateful for the support of J. D. Scheraga, M. W. Sli- ogy 55:3–21.
mak, and D. E. Gill. S. S. Herrod-Julius, C. Thomas, L. L. Burton, J. F. 1995. Birds and climate change. Christopher Helm, London.
Wolfenbarger, and an anonymous reviewer provided Buse, A., and J. E. G. Good. 1996. Synchronization of larval emergence
helpful comments and discussion. The views expressed in winter moth (Operophtera brumata L.) and budburst in pedun-
culate oak (Quercus robur L.) under simulated climate change.
are the author’s own and do not represent those of the Ecological Entomology 21:335–343.
U.S. Environmental Protection Agency. Buse, A., S. J. Dury, R. J. W. Woodburn, C. M. Perrins, and J. E. G.
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