Download The ecology of climate change and infectious diseases: comment

March 2010
COMMENTS
925
Ecology, 91(3), 2010, pp. 925–928
Ó 2010 by the Ecological Society of America
The ecology of climate change and
infectious diseases: comment
PAUL EPSTEIN1
Kevin Lafferty argues ‘‘. . . that while climate has
affected and will continue to affect the habitat suitability
for infectious diseases, climate change seems more likely
to shift rather than expand [their] geographic ranges . . . .’’
(Lafferty 2009).
There are several problems with this argument. One
involves the definition of climate change; the next
concerns the non-uniformity of global warming, in
space and time; and the third area is the breadth of
concerns.
First, climate change is not just a change in the global
temperature; it is also a change in the weather. While
temperatures affect the potential ranges of infectious
diseases and their vectors, weather affects the timing,
intensity and location of outbreaks. As warming occurs,
weather patterns are shifting, with more extremes of
both signs (hot and cold, wet and dry), more major
outliers, and the appearance of novel events (e.g., a
hurricane in the Southern Atlantic). Indeed, the
distribution no longer resembles a Gaussian bell-shaped
curve, but appears to be becoming more bimodal, with
more extremes at both ends.
With regard to extreme weather events (EWEs),
Lafferty addresses the associations between the El
Niño/Southern Oscillation (ENSO) and disease outbreaks. But ENSO is not synonymous with EWEs,
which are on the rise independent of ENSO. This is
primarily attributable to the physics of global warming:
since 1957, the world ocean has accumulated 22 times as
much heat as has the atmosphere (Barnett et al. 2005,
Levitus et al. 2005), accelerating the global hydrological
cycle. (And a warmer atmosphere holds more water
vapor: 7% more for each 18C it warms.) Heavy rains can
create floodplains where mosquitoes breed, as in the
outbreaks of Rift Valley fever in East Africa (Linthicum
et al. 1999, Anyamba et al. 2009). And storms, floods
and droughts can create conditions conducive to ‘‘clusters’’ of water-, mosquito- and rodent-borne diseases
(Epstein 1999, Relman et al. 2008). (One can only
project conditions conducive to outbreaks; their appearManuscript received 5 May 2009; revised 9 June 2009;
accepted 10 June 2009. Corresponding Editor: K. Wilson.
1 Center for Health and the Global Environment, Harvard
Medical School, 401 Park Drive, Boston, Massachusetts
02115 USA.
E-mail: [email protected]
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COMMENTS
ance is a function of a suite of social, biological, and
environmental conditions.)
Moreover, growing weather instability is breeding
sequences of extremes (e.g., droughts, punctuated by
heavy rains; series of strong hurricanes), and these can
be particularly conducive to disease outbreaks. Mozambique in 2000, for example, in a span of six weeks,
experienced three cyclones and incessant heavy rains,
leading to widespread flooding and a five-fold spike in
malaria in the affected regions (Epstein and Mills 2005).
The sequences of extremes can be especially destabilizing to the ecological (predator–prey and competitor)
relationships critical to the control of pests (especially
mosquitoes and rodents) that can carry pathogens
(Molyneux et al. 2008).
The issue of EWEs and their consequences for health
and public welfare, social systems and adaptation to the
coming climate is now being formally addressed by the
IPCC and by international relief agencies, such as the
International Federation of Red Cross and Red
Crescent Societies (2007). In the coming climate,
changing weather patterns may have more to do with
the distribution of outbreaks than will the rise in average
global temperatures.
Regarding the rise in temperature, itself, warming is
not occurring evenly across the globe, both spatially and
temporally. Warming is occurring disproportionately
closer to the poles; i.e., temperate, boreal, and arctic
regions are warming faster than are the tropics. While
average global temperatures rose about 1.48F (0.88C)
during the past century, for instance, average annual
temperatures in Alaska increased 3.18F (1.98C) from
1950 to 2006, and, consistent with global trends, the
average winter temperature increased 68F (3.38C) in the
same time frame (Demain et al. 2009; Alaska Climate
Research Center, data available online).2 Vectors and
microbes are thus experiencing less differential warming
in their lower latitude ranges than they are at higher
latitudes.
Temporally, since 1970, nighttime and winter temperatures (i.e., daily and yearly minimum temperatures
[TMINs]) haven risen twice as fast as overall warming
(Easterling et al. 1997). And winter warming is most
pronounced as one moves toward the poles. TMINs, not
temperature averages, are critical to the biological
responses to global warming. Paleo (fossil) records of
beetle distributions in Europe and North America
demonstrate, for example, that their distribution
changed in consort with changes in TMINs. The
Younger Dryas (YD)—the most well-known of the
many ‘‘cold reversals’’ to punctuate warming trends
depicted in the ice core records (the YD occurred some
13 000 years ago)—is precisely delineated by changes in
2 hhttp://climate.gi.alaska.edu/ClimTrends/change/
TempChange.htmli
Ecology, Vol. 91, No. 3
the distribution of beetle communities (Elias 1994;
mapping reproduced in Epstein et al. 1998).
Regarding tick populations, Lafferty states ‘‘. . . the
best predictor of changes in TBE [tick-borne encephalitis] from 1970 to 2005 is poverty . . . .’’ While this may
be so—and all outcome measures can be traced to a suite
of social and environmental determinants—Lindgren
and Gustafson (2001) demonstrate that TBE-bearing
tick populations moved north in Sweden in lockstep
with each warm winter. And there appears to be no
diminution of tick populations at the southern region of
their expanding range. Indeed, their maps indicate that
tick populations increased in abundance in the area of
their former distribution, centered on the Stockholm
Archipelago.
Regarding projections for tick populations, Brownstein and colleagues (2005) model suitable U.S. habitat
out to 2080 for Borrelia burgdorferi-bearing ticks (also
capable of carrying several viruses and the agents of
Ehrlichiosis and Babesiosis). Data, however, suggest
that changes in range are occurring much faster than the
models project, with the rise in TMINs at high
temperate and boreal latitudes the most plausible
explanation.
Forest pests are also expanding their range. In the
western United States from Arizona to Alaska, pine
bark beetles are overwintering, moving to higher
latitudes, higher altitudes, and getting in more generations each year, absent sustained killing frosts, e.g.,
when temperatures fall below 208F (approximately
78C) for 10 days. But their numbers and the damage
they are doing have not diminished in the southern
range or at lower altitudes (Van Sickle 1995, Carroll et
al. 2004, Solomon et al. 2007). Host (tree) resistance is
also lowered by extremes: repeated droughts dry the
resin that drowns the beetles as they try to drive through
the bark. In the northeast United States, the aphid-like
wooly adelgid is decimating the Eastern Hemlock trees
and is moving north after doing its damage at its
southern range, while the Asian longhorned beetle
threatens maple and other deciduous trees.
Such biological impacts of warming and extremes on
agents and hosts are increasing forest vulnerability to
nonlinear changes, such as diebacks and wildfires. And
unlike many human pests, the damage they leave behind
has long-lasting affects.
Changes of vector ranges and their impacts on human
populations can also occur by circuitous and nonlinear
routes. When excessive heat and prolonged drought do
render low latitude regions inhospitable for disease
vectors and pathogens, the warmth and drying can
produce unexpected results. Lafferty and other authors
in the same issue of Ecology (Harvell et al. 2009, Pascual
and Bouma 2009) address potential changes in the
distribution of animal hosts and reservoirs. People can
also move in response to changing environmental
March 2010
COMMENTS
conditions. In southern Honduras, for example, conditions have become so hot and the hydrological cycle so
altered (as a result of warming, deforestation and the
destruction of coastal mangroves to make way for
shrimp farming), that malaria is no longer a significant
health threat in the region around Choluteca. But,
concomitant loss of agricultural productivity and the
advancing water shortages have driven human populations north, where monoculture plantations and fragmented forests provide employment and favorable
conditions for malaria transmission.
Notably, malaria did spike even in the less-populated
south when Hurricane Mitch stalled over Honduras in
November, 1998, dropping six feet of rain over three
days.
On the other hand, droughts, which Lafferty states do
not contribute to infectious disease distribution, are
associated with a number of infectious ills. Droughts,
when people store water in containers about their
houses, are associated with upsurges of Aedes aegypti
mosquitoes, and outbreaks of dengue fever in the
Caribbean and chikungunya fever in East Africa and
Indian Ocean islands (Epstein 2007, Chrétien et al.
2007). For West Nile fever, a prolonged spring drought
and a three-week July heat wave that preceded its
explosive debut in Queens, New York in August 1999,
appear to have amplified viral circulation: increasing the
abundance of catch-basin-dwelling Culex pipiens (the
maintenance vector) and viral replication in the mosquitoes and birds (Epstein and Defilippo 2001). (Now,
with West Nile virus well established in wildlife in the
United States, warm wet conditions are conducive to
outbreaks.) In the African Sahel, meningococcal meningitis epidemics tend to occur during drought (Moore
and Broome 1994), the dried mucus membranes perhaps
playing a role in bacterial penetration. Several agricultural pests—aphids, locust and geminivirus-injecting
whiteflies—flourish during droughts, while floods foster
fungal growth and the proliferation of nematodes.
Lafferty addresses changes in marine-related diseases,
and has written about the mounting threats of warming
and diseases in coral reefs (Lafferty et al. 2004). But
several diseases of other marine organisms suggest that
ranges of diseases may be extending. DERMO and
MSX, for example, are two parasitic diseases that have
severely crippled oyster populations along the U.S. east
coast. And while they have moved up the coast into New
England from where they first appeared (in Chesapeake
Bay)—again moving with each warm winter—they are
also spreading south (Hofmann et al. 2001). Another
shell-fish resident, Vibrio parahaemolyticus, caused an
outbreak in humans consuming raw oysters from a local
shell-fish farm after daily water temperatures exceeded
158C (McLaughlin et al. 2005). The authors concluded
that ‘‘This investigation extends by 1000 km the
northernmost documented source of [oyster-related] V.
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parahaemolyticus in the U.S.’’ While complete data on
distribution of this bacteria are not readily available,
there is no reason to believe that V. parahaemolyticus
has left tropical climes, where ocean temperatures have
not experienced the same degree of warming as have
those (periodically, for sure) at higher latitudes.
Climate and ecological models, monitoring and
mapping can be employed to address the pests and
pathogens afflicting forests, crops, livestock, wildlife and
marine life (Relman et al. 2008). The combination of
warming, unstable weather patterns (e.g., early heat
waves coinciding with flowering), rising CO2 that favors
weeds over crops (Ziska et al. 2009), and changes in the
ranges and abundance of pests and pathogens pose
mounting threats for the health and integrity of
ecosystems.
In sum, our health, the final common pathway
integrating our environmental and social surroundings,
is threatened in multiple ways by growing climate
instability. Warming-induced range shifts, expansion
and spread of specific infectious diseases are part of a
much larger landscape of climate-related impacts on the
emergence, resurgence and redistribution of infectious
diseases occurring across a wide range of taxonomic
groups on a global scale. Unchecked, climate change
poses fundamental threats for our health and for the
health of the life-support systems upon which we
depend.
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