What contributions have the authors mentioned in the paper "Climate warming and disease risks for terrestrial and marine biota" ?

In this paper, the authors identify four priorities for research to improve the ability to predict impacts of climate change on disease: 1 ) Collect baseline data on diseases of wild populations.

(Open Access) Climate Warming and Disease Risks for Terrestrial and Marine Biota (2002) | C. Drew Harvell

Q: What factors are important in driving recent malaria expansions?

In fact, expansion of antimalarial resistance and failed vector control programs are probably as important as climate factors in driving recent malaria expansions.

Q: What is the common climatic anomaly to initiate coral disease?

Another climatic anomaly hypothesized to initiate coral disease is transport of aeolian dust from Saharan Africa (mediated by a shift in the North Atlantic Oscillation) to the Caribbean (61).

Q: What are some of the recent examples of vector-borne diseases?

vector-borne diseases of livestock, particularly African horse sickness and bluetongue viruses, recently ex-panded their ranges (27).

REVIEW: ECOLOGY

Climate Warming and Disease Risks for

Terrestrial and Marine Biota

C. Drew Harvell,

* Charles E. Mitchell,

1,2

Jessica R. Ward,

Sonia Altizer,

3,4

Andrew P. Dobson,

Richard S. Ostfeld,

Michael D. Samuel

Infectious diseases can cause rapid population declines or species extinctions. Many

pathogens of terrestrial and marine taxa are sensitive to temperature, rainfall, and

humidity, creating synergisms that could affect biodiversity. Climate warming can

increase pathogen development and survival rates, disease transmission, and host

susceptibility. Although most host-parasite systems are predicted to experience more

frequent or severe disease impacts with warming, a subset of pathogens might decline

with warming, releasing hosts from disease. Recently, changes in El Nin˜o–Southern

Oscillation events have had a detectable inﬂuence on marine and terrestrial patho-

gens, including coral diseases, oyster pathogens, crop pathogens, Rift Valley fever, and

human cholera. To improve our ability to predict epidemics in wild populations, it will

be necessary to separate the independent and interactive effects of multiple climate

drivers on disease impact.

nfectious diseases are strong biotic forces

that can threaten biodiversity by catalyzing

population declines and accelerating ex-

tinctions. Pathogens are implicated in recent

declines of Australian and Central American

frogs (1, 2), Hawaiian forest birds, and Afri-

can wild dogs (3). Invertebrate extinctions

associated with disease include the Polyne-

sian tree snail (4) and a marine limpet (5).

Pathogens also contribute to declines of

threatened species such as lions (Fig. 1),

cranes, eagles, and black-footed ferrets (6, 7).

Plant pathogens can cause problems not only

for their immediate hosts but also for their

associated fauna and ecological communities.

For example, the Asian chestnut blight fun-

gus (Cryphonectria parasitica) effectively

extirpated the American chestnut (Castanea

dentata) from eastern United States forests

(8), causing the apparent extinction of sev-

eral phytophagous insects (9). In Australia,

the root-infecting fungus Phytophthora

cinnamomi converted large areas of Euca-

lyptus forest to monocot-dominated open

savanna (10), eliminating potential nest

sites and food for many animals (11, 12).

Anthropogenic climate change is having

measurable effects on ecosystems, communi-

ties, and populations (13). Understanding

links between infectious disease and climate

is more difficult, given the paucity of baseline

disease data, the multivariate nature of cli-

mate change, and nonlinear thresholds in

both disease and climate processes (14). As-

sociations between climate and disease do not

necessarily imply causation, but results from

correlational studies and short-term experi-

ments can help us to separate the effects of

climate from other components of global

change. We review the potential consequenc-

es of temperature changes on infectious dis-

eases and consider the hypothesis that climate

warming will affect host-pathogen interac-

tions by (i) increasing pathogen development

rates, transmission, and number of genera-

tions per year; (ii) relaxing overwintering

restrictions on pathogen life cycles (Fig. 2);

and (iii) modifying host susceptibility to in-

fection. Changes in these mechanisms could

cause pathogen range expansions and host

declines, or could release hosts from disease

control by interfering with the precise condi-

tions required by many parasites. Clearly, not

all pathogens have equal potential to control

host populations or to be affected by warm-

ing. We predict that climate warming will

disproportionately affect pathogens with

complex life cycles or those that infect non-

homeothermic hosts during one or more life

cycle phases.

Despite known impacts of infectious dis-

eases, the combined effects of climate change

and disease on biodiversity have rarely been

considered (2, 15–17). Difficulty in separat-

ing directional climate change from short-

term variation has made it challenging to

associate climate warming with disease prev-

alence or severity. For most wild populations,

there are no long-term records of disease

prevalence or baseline estimates of disease

impacts on fitness. Recent work on human,

crop, and forest pathogens, for which long-

term data exist, shows sensitivity of some

pathogens and vectors to climate factors (18–

23). It is therefore likely that pathogens af-

fecting wild populations will experience sim-

ilar climate-driven changes.

Climate: Current and Predicted

Changes

Terrestrial systems. The rate of climate

change resulting from increased greenhouse

gases and changes in land and water use is

expected to be rapid on an evolutionary time

scale (16 ). The Intergovernmental Panel on

Climate Change (IPCC) (24 ) provides pro-

jections for terrestrial ecosystems. Mean

global surface air temperature is projected to

increase by 1.4° to 5.8°C by 2100 relative to

1990, with the magnitude of the increase

varying both spatially and temporally. Conti-

nental regions and higher latitudes are pro-

jected to warm more than coastal regions and

the tropics. Nighttime minimum temperatures

are expected to increase more than daytime

maximum temperatures, and winter tempera-

tures are expected to increase more than sum-

mer temperatures. Warming will alter other

aspects of climate relevant to disease, partic-

ularly humidity and precipitation. Some areas

will experience more intense precipitation

events and increased humidity while others

have an increased risk of drought. Generally,

globally averaged water vapor pressure,

evaporation, and precipitation are projected

to increase (24 ). However, predicted changes

in hydrologic variables are much less robust

than changes in temperature, so we focus on

the potential effects of temperature.

Marine systems. The direct components of

predicted climate change affecting marine or-

ganisms over the next century are (i) temper-

ature increase, (ii) sea level increase and sub-

sequent changes in ocean circulation, and (iii)

decrease in salinity (24 ). Coastal ocean tem-

perature increases are expected to be slightly

lower than the IPCC projected increases for

land, but still rise measurably. Sea level is

Department of Ecology and Evolutionary Biology,

Cornell University, Ithaca, NY 14853, USA.

Depart-

ment of Ecology, Evolution and Behavior, University

of Minnesota, St. Paul, MN 55108, USA.

Department

of Environmental Studies, Emory University, Atlanta,

GA 30322, USA.

Cornell Laboratory of Ornithology,

159 Sapsucker Woods Road, Ithaca, NY 14850, USA.

Department of Ecology and Evolutionary Biology,

Princeton University, Princeton, NJ 08544, USA.

In-

stitute of Ecosystem Studies, Box AB, 65 Sharon

Turnpike, Millbrook, NY 12545, USA.

U.S. Geological

Survey–National Wildlife Health Center, Madison, WI

53711, USA.

*To whom correspondence should be addressed. E-

mail: cdh5@cornell.edu

S CIENCE’ S C OMPASS

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REVIEW

21 JUNE 2002 VOL 296 SCIENCE www.sciencemag.org2158

expected to rise by 0.09 to 0.88 m. Effects on

ocean circulation and potential climate

feedbacks cause large uncertainty in many

climate predictions. For example, the direc-

tion of the North Atlantic Oscillation,

which influences temperate climate and has

been hypothesized to affect Caribbean dis-

ease outbreaks (25), is determined by

warming in tropical oceans (20). In addi-

tion to a mean increase in temperature,

extremes are expected to increase and in-

termittent phenomena such as El Nin˜o may

change (21, 22).

Impacts of Climate

on Disease

Plant disease. Climate

change can influence

plant disease by altering

biological processes of

the pathogen, host, or

disease-spreading or-

ganisms. Direct effects

on pathogens are likely

to be strongest, al-

though different patho-

gen life stages may vary

in their climatic suscep-

tibilities. Winter is a

major period of patho-

gen mortality, potential-

ly killing more than

99% of the pathogen

population annually

(26). Greater overwin-

tering success of patho-

gens will likely increase

disease severity. Be-

cause temperatures are

expected to increase

more in winter than in

other seasons, this pop-

ulation bottleneck may

be removed for many

pathogens.

Several plant dis-

eases are more severe

after mild winters or

during warmer temper-

atures (27), which sug-

gests that directional

climate warming will alter plant disease

severity (23). For example, laboratory and

Australian field studies indicate that the

fungus causing Mediterranean oak decline,

Phytophthora cinnamomi, causes more se-

vere root rot at higher temperatures than the

current Mediterranean average (28). In a

14-year field study in England, the Dutch

elm disease fungus (Ophiostoma novo-

ulmi) caused greater defoliation in warmer

years (29). In a 39-year dendrochronologi-

cal study in Maine, beech bark cankering

by Nectria spp. was worse after mild win-

ters or dry autumns—conditions favoring

survival and spread of the beech scale in-

sect, which predisposes beech to fungal

infection (30). Wheat stripe rust (Puccinia

striiformis) in the Pacific Northwest was less

severe during years of low temperature and

rainfall from 1969 to 1986 (18).

The number of generations for polycyclic

pathogens and seasonal growth of other patho-

gens may increase under climate change

through two mechanisms—longer growing sea-

sons and accelerated pathogen development.

Temperature optima for within-host growth of

fungal pathogens are generally 20° to 25°C,

with maxima of 30°C or higher (31, 32), so

effects of climate warming on growth will de-

pend on pathogens and locales. Because of

nonlinear effects of temperature on growth, the

effect of climate warming on pathogen growth

rate will depend not only on changes in mean

temperature, but also on temperature variability

(31).

For foliar fungi, temperature and water

availability interact to determine fungal infec-

tion (initial penetration of the plant) and sporu-

lation. Both infection and sporulation often re-

quire close to 100% relative humidity. These

moist conditions occur most commonly dur-

ing overnight dewfall, making temperature at

this time a critical variable. Because night

temperatures are projected to increase more

than day temperatures, climate warming may

increase or decrease fungal infection and

sporulation, depending on whether tempera-

tures move closer to or farther from the typ-

ical optimum of 24°C (32) (Fig. 1).

Climatic variation can also influence

host resistance and growth. Warming can

decrease plant resistance to both fungi and

viruses (27 ). Plant species that have faster

growth rates in warmer climates may also

experience increased disease severity, be-

cause higher host density increases the

transmission of many pathogens (33).

Also, increased above ground plant bio-

mass influences canopy humidity, which of-

ten affects foliar fungal disease spread (32).

The most severe and least predictable dis-

ease outbreaks might occur if climate change

alters host or pathogen geographic ranges,

causing formerly disjunct species and popu-

lations to converge (34). The potential for

such outbreaks is illustrated by the import of

Asian chestnut and European elm logs to the

United States, thereby introducing chestnut

blight and Dutch elm disease, which then

spread rapidly through their new hosts (8,

Fig. 1. Diseases of potential conservation signiﬁcance or with climate links. (A) Spores of the protozoan parasite

Ophryocystis elektroschirrha are sandwiched between abdominal scales of their host, the monarch butterﬂy. Climate

warming that extends the breeding season of their hosts in temperate North America may also increase the prevalence

of this disease, and heavily infected populations currently persist in mild climates where hosts breed year-round. [Photos

by Karen Oberhauser and De Cansler] (B) Diseased lion infested with Stomoxys ﬂies during a canine distemper outbreak

(81) in the Ngorongoro Crater, Africa (February 2001). [Photo by Craig Packer] (C) Lesions and tumors on sea fans

(Gorgonia ventalina) caused by the temperature-sensitive fungus Aspergillus sydowii. Scale bar, 5 cm. [Photo by Kiho Kim]

(D) A leaf spot disease of Aster azureus caused by the fungus Septoria sp. The spread of such foliar fungal pathogens often

depends critically on temperature and moisture. [Photo by Charles Mitchell]

S CIENCE’ S C OMPASS

www.sciencemag.org SCIENCE VOL 296 21 JUNE 2002 2159

35). Conversely, after the introduction of

wheat from the Old World to Brazil and

coffee from Africa to Asia, each crop suf-

fered epidemics caused by fungi native to its

new habitat (36, 37).

Wildlife diseases. Climate

change is most likely to affect

free-living, intermediate, or

vector stages of pathogens in-

fecting terrestrial animals. Of

these, vector-borne diseases

are the strongest candidates

for altered abundance and

geographic range shifts be-

cause rising temperatures will

affect vector distribution, par-

asite development, and trans-

mission rates (38). Many vec-

tor-transmitted diseases are

climate limited because para-

sites cannot complete devel-

opment before the vectors die.

Vector-borne human patho-

gens such as malaria, African

trypanosomiasis, Lyme dis-

ease, tick-borne encephalitis,

yellow fever, plague, and den-

gue have increased in inci-

dence or geographic range in

recent decades (39, 40). Sim-

ilarly, vector-borne diseases

of livestock, particularly Afri-

can horse sickness and blue-

tongue viruses, recently ex-

panded their ranges (27 ). Most of these diseas-

es have expanded into regions of higher lati-

tude, in each case accompanied by apparent

expansion in the ranges of mosquito, tick, and

midge vectors. Whether these expansions are

due primarily to climate change or other anthro-

pogenic influences (e.g., habitat alteration or

drug-resistant pathogen strains) is controversial,

as is predicting future distributional changes in

disease prevalence. For example, location-spe-

cific, long-term data show that climate did not

change in an African highland area where ma-

laria increased (41). In fact, expansion of anti-

malarial resistance and failed vector control

programs are probably as important as climate

factors in driving recent malaria expansions.

The hypothesis that warming in recent de-

cades has caused latitudinal shifts of vectors

and diseases is supported by laboratory and

field studies showing that (i) arthropod vectors

and parasites die or fail to develop below

threshold temperatures (42); (ii) rates of vector

reproduction, population growth, and biting in-

crease (up to a limit) with increasing tempera-

ture; and (iii) parasite development rates and

period of infectivity increase with temperature

(42). Another line of evidence supporting

strong links between climate and vector-borne

disease consists of correlations between warm-

er, wetter conditions associated with El Nin˜o

events and outbreaks of malaria, dengue, Rift

Valley fever, African horse sickness, and

plague (27). Correlations between El Nin˜o

events and disease outbreaks, however, are not

perfect, in part because El Nin˜o does not always

produce heavy rains, and in part because other

biophysical and epidemiological factors are in-

volved (43).

Helminth parasites of terrestrial wildlife that

release eggs or free-living stages into the envi-

ronment or use invertebrate intermediate hosts

are susceptible to changes in temperature and

humidity at several stages of their life cycles.

Bioclimatographs that combine local data on

moisture and temperature have traditionally

been used to monitor and predict outbreaks of

gastrointestinal nematodes of livestock. Several

processes control associations between cli-

mate and the abundance and geographic range

of nematodes and other macroparasites. First,

development and embryonation success are

temperature dependent in larval parasites, and

a degree-days concept is widely used to es-

tablish conditions that optimize parasite

growth (44). For example, in Schistosoma

mansoni, a human pathogen in an interme-

diate host, a 10°C increase in temperature

can cut development time in half [from 35

to 12 days (45)]. However, predicting the

net impact of climate warming on these

parasites is difficult because warming in-

creases both development rates and larval

mortality rates. Resolving the impact of

climate warming in such systems remains a

research priority. Another climate-sensitive

process in terrestrial nematodes and other

parasites is timing of hypobiosis, or arrested

development, determined by temperature and

moisture (27). For example, in Trichostrongy-

lus tenuis, a nematode parasite of red grouse,

larval hypobiosis occurs dur-

ing winter and is responsible

for seasonal disease occur-

rence and springtime mortal-

ity in red grouse (46).

Disease and climate-medi-

ated synergies affect many

wild avian populations. Field

and laboratory studies demon-

strate that avian malaria (Plas-

modium relictum) and pox

(Poxvirus avium) introduced

into Hawaii caused marked

declines in endemic forest

birds (Fig. 3) (47 ), and that

disease risk follows an eleva-

tion gradient. Malaria and pox

transmission are more intense

in mid-elevation forests where

mosquitoes and endemic birds

have the greatest overlap, and

are lowest at high elevations

where mosquitoes are limited

by cool temperatures. Trans-

mission of malaria and pox

therefore varies from endemic

transmission in warm, low-el-

evation forests to irregular

outbreaks at mid-elevation

forests. Temperature differ-

ences along this gradient affect factors that

contribute to vector capacity and determine the

basic reproductive ratio of this disease (48),

including the abundance of mosquito vectors,

vector oviposition rate, larval development,

adult survival, biting rate, and incubation time

(27). These factors contribute to vector capacity

and determine the basic reproductive ratio of

this disease (48) in birds.

The spread of certain viral, protozoan, and

nematode parasites in temperate insects may be

favored by warmer climates that increase the

host’s breeding season. Prevalence of the pro-

tozoan parasite Ophryocystis elektroscirrha

(Fig. 1) is higher in monarch butterfly popula-

tions that breed year-round in warm regions

than in more seasonal climates where monarchs

migrate long distances between breeding in-

tervals (49). Substantial decay of gypsy moth

nuclear polyhedrosis virus on host egg cases

during winter results in small epidemics early

in the summer, followed by a larger wave of

infection later in the season (50). Thus, con-

ditions that enhance pathogen winter survival

or extend host breeding periods should in-

crease the abundance of many viral and pro-

tozoan insect parasites.

Warming might limit certain emerging

wildlife diseases. Amphibian population de-

clines in Central America and Australia are

linked to emerging chytrid and iridoviral dis-

Fig. 2. The inﬂuence of an average 1.5° rise in temperature on the basic reproduc-

tive number R

of a hypothetical pathogen. When R

is above 1, a pathogen will

increase. The lower blue line illustrates the average weekly temperature before

climate change; the upper red line illustrates average weekly temperature after an

average 1.5° temperature increase. The lower green line corresponds to R

⫽ 1;

below this temperature the pathogen declines in abundance. The pathogen increas-

es at temperatures above this, and we assume that disease problems become

severe when temperature exceeds the pink line and epidemic above the purple line.

The ﬁgure illustrates that increases in temperature not only allow the peak value

of R

to increase, but also lead to an increased annual duration of the period during

which the pathogen is a problem.

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eases (1). The geographic ranges of the chytrid

epizootic are currently limited by a requirement

for cool, moist, high-altitude conditions; hence,

this pathogen may be one of a few for which

climate warming could disrupt disease spread

(27). Entomopathogenic fungi of insects are

also projected to decrease with climate warm-

ing. Fungal entomopathogens typically have

higher prevalence and cause greater mortality

under cool, humid conditions. The gypsy moth

fungus (Entomophaga maimaiga) released to

North America in the early 1900s did not affect

host populations until the cool, wet spring of

1989 (51). Outbreaks of another insect patho-

gen (Entomophthora muscae) in muscoid flies

usually coincide with periods of high rainfall

and cool temperatures (52). Hot, dry conditions

are thought to limit fungal growth and sporula-

tion and may also enhance insect immunity and

behavioral fevers (52). Thus, climate warming

may limit some fungal entomopathogens and

release insects from pathogen pressure (27 ).

Significant climate change will restructure

communities as the current geographic ranges

of species shift poleward. If vector-transmit-

ted pathogens expand their ranges out from

the tropics, they will experience a decreased

diversity of hosts in temperate environments.

This will focus the biting activities of their

vectors on a less diverse host community,

increasing the impact of pathogens on poten-

tially novel hosts and reducing the dilution

effect proposed by Schmidt and Ostfeld (53).

Ecological restructuring and

impacts on parasite-host rela-

tionships have at least three im-

portant implications for terres-

trial conservation biology: (i)

increasing the spread of patho-

gens into the temperate zone,

where lower net biodiversity

should reduce buffering effects

that occur in more diverse trop-

ical communities (53); (ii) trig-

gering elevational changes of

pathogen distribution in moun-

tainous regions; and (iii) modi-

fying seasonal patterns of

pathogen outbreaks in temper-

ate regions (Fig. 2).

Marine diseases. Recent pa-

pers have shown links between

pathogens and changing ocean

temperatures, including human

diseases such as cholera (19, 54 )

and emerging coral pathogens

(55). The coral bleaching associ-

ated with the 1998 El Nin˜o event was the most

geographically extensive and severe in recorded

history (56, 57), causing pronounced mortality

worldwide. Although reported only as bleach-

ing-related mortality, the demise of some corals

in the 1998 bleaching was accelerated by op-

portunistic infections, such as the mass mortal-

ity of the gorgonian coral Briareum asbestinum

(58). Three coral pathogens grow well at tem-

peratures close to or exceeding probable host

optima, which suggests that they would in-

crease in warmer seas (27) (Fig. 1). The bacte-

rium Vibrio shiloi is temperature sensitive and

causes bleaching in the coral Oculina patag-

onica (59). Heat-induced viruses could also be

involved in temperature-induced coral bleach-

ing (60). Another climatic anomaly hypothe-

sized to initiate coral disease is transport of

aeolian dust from Saharan Africa (mediated by

a shift in the North Atlantic Oscillation) to the

Caribbean (61).

Growth rates of marine bacteria (62) and

fungi (63) are positively correlated with

temperature. Among marine fungi, opti-

mum temperatures for growth coincide

with thermal stress and bleaching for many

corals (63, 64), leading to likely co-occur-

rence of bleaching and fungal infection.

Among marine invertebrates and eelgrass,

many epizootics of unidentified pathogens

are linked to temperature increases, but the

mechanisms for pathogenesis are unknown

(27 ). In 1999, gorgonian corals, scleractin-

ian corals, zoanthids, and sponges in the

Ligurian Sea were affected by a tempera-

ture-linked epizootic, where mortality like-

ly resulted from the effects of environmen-

tal stress and an unidentified opportunistic

pathogen (65). Although many disease-re-

lated mass mortalities in the ocean are as-

sociated with warming waters, coldwater

disease of salmonids is favored by low

temperatures. Signs of infection appear

when water temperatures are 4° to 10°C

and disappear in warmer water (66 ).

Increased ocean temperature also causes

pathogen range expansions. A notable exam-

ple is the mid-1980s northward expansion of

oyster diseases (67, 68). Eastern oyster dis-

ease on the U.S. east coast (Perkinsus mari-

nus) extended its range from Long Island to

Maine during a winter warming trend in

which the winter cold-water barrier to patho-

gen growth was removed. El Nin˜o events are

also implicated in Eastern oyster diseases in

the Gulf of Mexico, where Perkinsus is en-

demic. Gulf-wide P. marinus infection inten-

sity and prevalence drop during cold, wet El

Nin˜o events and rise during warm, dry La

Nin˜a events (69).

Although there is evidence for temper-

ature- and climate-related links in some

marine diseases, lack of reliable baselines

and incomplete disease time series compli-

cate the partitioning of climate effects and

other anthropogenic disturbances. A time

series sufficiently long to detect climate

effects is only available for oyster disease

(70) and cholera (19, 71). Hayes et al.(25)

posit a detectable increase in biological

disturbances related to the North Atlantic

Oscillation, but lack of baselines prevents

accounting for the contribution of other

anthropogenic factors such as eutrophica-

tion, overfishing (72), and aquaculture.

Conclusions

Links between climate change and disease will

increase the severity of threats associated with

climate warming. Increased disease can con-

tribute to population or species declines, espe-

cially for generalist pathogens infecting multi-

ple host species. The greatest im-

pacts of disease may result from a

relatively small number of emer-

gent pathogens. Epidemics

caused when these infect new

hosts with little resistance or tol-

erance may lead to population de-

clines, such as those that fol-

lowed tree pathogen invasions in

North America during the last

century. Although we have em-

phasized threats of intensified

parasitism, the loss of parasites

can also affect biodiversity by re-

leasing hosts from a major source

of population regulation.

The most detectable effects

of directional climate warming

on disease relate to geographic

range expansion of pathogens

such as Rift Valley fever, den-

gue, and Eastern oyster disease.

Factors other than climate

change—such as changes in

land use, vegetation, pollution, or increase in

drug-resistant strains—may underlie these

range expansions. Nonetheless, the numerous

mechanisms linking climate warming and

disease spread support the hypothesis that

climate warming is contributing to ongoing

range expansions.

We found no unequivocal examples of nat-

Fig. 3. Culex mosquitoes are the vectors responsible for transmitting avian

malaria (Plasmodium relictum) and avian pox (Poxvirus avium) to endemic

Hawaiian forest birds such as the apapne (Himatione sanguinea). [Photo by

Jack Jeffrey]

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www.sciencemag.org SCIENCE VOL 296 21 JUNE 2002 2161

ural changes in severity or prevalence resulting

from directional climate warming per se. How-

ever, current data on temperature-dependent

pathogen development and replication rates, and

on associations between disease occurrence and

climate variation, suggest several ways in which

climate warming has altered and will alter dis-

ease severity or prevalence. In the temperate

zone, shorter, milder winters are expected to

increase disease spread. In tropical oceans,

warmer summers may increase host susceptibil-

ity through thermal stress. Decreased severity or

prevalence with increasing temperature is ex-

pected for several types of diseases, such as

amphibian chytridiomycosis, coldwater disease

of fish, and fungal pathogens of insects.

Given the challenge of linking disease im-

pacts and directional climate change for well-

studied agricultural, maricultural, and human

diseases, it is not yet possible to predict the

consequences for biodiversity. Very few empir-

ical studies directly explore the relationship be-

tween climate and transmission of or resistance

to disease. Even fewer explore interactions be-

tween temperature and components of a patho-

gen’s life cycle (29, 73, 74). We therefore iden-

tify four priorities for research to improve our

ability to predict impacts of climate change on

disease:

1. Collect baseline data on diseases of wild

populations. Baseline disease data are critical to

predict changes in a warming climate, but such

data are rarely collected for nonhuman, nonag-

ricultural, or noncommercial systems. Monitor-

ing programs for the prevalence and severity of

wildlife diseases and their population- and com-

munity-level impacts must be implemented for

a wider range of natural systems.

2. Separate the effects of multiple cli-

mate variables on disease. To accurately

predict future responses to climate change,

we must quantify the direct and synergistic

effects of multiple climate variables, such

as temperature and moisture, on disease.

Separating the effects of these variables

will require experimental manipulation in

the lab or field. Pathogens with complex

life cycles present a particular challenge

because different life stages may be affect-

ed by variables with opposite effects on

parasite fitness.

3. Forecast epidemics. Forecasting models

using climate variables can effectively predict

outbreaks for some crop and human diseases.

Crop disease programs have long been in effect:

Potato late blight (Phytophora infestans) is cor-

rectly forecasted 92% of years on the basis of

number of days of rain (75), and rice blast

(Pyricularia oryzae) models based on tempera-

ture and moisture forecast when an epidemic

will start and when to apply fungicide for opti-

mal control (76 ). Such forecasting programs are

also in development for human diseases with

climate sensitivity, such as Rift Valley fever,

which is associated with warm El Nin˜o events

of high rainfall (43, 77 ), and cholera is predict-

able from sea surface temperature associations

with El Nin˜o (19). The National Oceanic and

Atmospheric Administration’s coral bleaching

program uses sea surface temperature increases

in a location-specific algorithm to predict when

and where coral bleaching will occur (78). Sim-

ilar disease forecasting models should be devel-

oped for other threatened populations and cou-

pled to models predicting epidemic impacts on

host abundance. Implementing such forecasting

systems for diseases of threatened populations

would allow intervention before climate-in-

duced epidemics endanger host populations.

4. Evaluate the role of evolution. The rate of

adaptation and evolution is an important un-

known in any prediction of climate impacts

(79). Overlooking the role of evolution can be

particularly dangerous with infectious diseases

(80). If shifts in host or parasite ranges lead to

disease emergence, the rate of pathogen evo-

lution and host evolutionary response could

be critical to predicting disease spread and

subsequent effects on biological diversity.

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Supplementary Online Material

www.sciencemag.org/cgi/content/full/296/5576/2158/

DC1

Table S1

S CIENCE’ S C OMPASS

21 JUNE 2002 VOL 296 SCIENCE www.sciencemag.org2162

Climate Warming and Disease Risks for Terrestrial and Marine Biota

Figures

Citations

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Climate Change, Human Impacts, and the Resilience of Coral Reefs

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Depletion, Degradation, and Recovery Potential of Estuaries and Coastal Seas

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Climate change 2001: the scientific basis

Ecological responses to recent climate change.

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Frequently Asked Questions (19)

Q1. What contributions have the authors mentioned in the paper "Climate warming and disease risks for terrestrial and marine biota" ?

Q2. What factors are important in driving recent malaria expansions?

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