Do rising temperatures matter?

Relationships between the environment and population dynamics in ecology have a long history of polarized debates usually involving two alternative and opposite explanations that exclude each other. One of the best known examples is found in the early question of what regulates populations and the role of extrinsic vs. intrinsic factors, opposing the importance of the environment (or density-independent factors) to that of feedbacks within the nonlinear dynamics of the population itself (or density-dependent factors). Since then, population ecology has recognized the importance of the interplay between external environmental forcing and intrinsic nonlinearities in determining population dynamics. With some delay, the same polarization appeared, and is still present, in debates on the role of climate in the dynamics of infectious diseases at different temporal scales, from interannual fluctuations to longer trends. Although opposite views serve to organize our thinking and the testing of hypotheses, taken to extremes such polarization is unproductive, and delays understanding. From this perspective, Lafferty’s (2009) review is a welcome addition to the existing literature on the importance of considering climate in the context of other aspects of change (e.g., Lindblade et al. 2000, Chaves et al. 2008). However, Lafferty’s description of the state of the science as a ‘‘crisis discipline, reminiscent of the early phases of conservation biology’’ is already outdated, applying for example to the earlier scenarios for the global resurgence of malaria. An earlier reaction to such a ‘‘crisis discipline’’ has contributed to a polarization of the field and it would be unfortunate if conclusions in this review, on the lack of a net effect of climate change on the geographic range of infectious diseases at large spatial scales, were mistakenly taken as further support for the view that climate does not matter. Lafferty argues that climate driven range shifts are more likely than range expansions (with no net positive change) in vector-transmitted diseases such as malaria. We focus first on this point to emphasize that range shifts will matter and should be better understood, regardless of net effects at the large scales of continents or the globe. Importantly, assessments of net effects at too large a spatial scale miss fundamental considerations, as emphasized here with a focus on epidemic malaria in tropical regions. Furthermore, assessments based on current indices of climate suitability are problematic given the limitations of the current indices themselves. Similarly problematic are extrapolations from the history of malaria in Europe to epidemic regions that are climate sensitive. At shorter temporal scales, the relevance of climate has been addressed with seasonal and interannual patterns. Whether and how climate variability drives seasonality and cycles of longer period is important for the mechanisms by which infectious diseases will respond to climate change, for example in the length and timing of the seasons and in the amplitude of phenomena such as the El Nino Southern Oscillation (ENSO). The second part of our commentary concerns Lafferty’s review of interannual climate effects. We argue that the conclusions of the re-analysis of historical yellow fever and ENSO in the US do not extrapolate to yellow fever in general, and that more recent results on epidemic malaria in African highlands support a role of climate variability. With the case study of cholera on the evidence for a role of ENSO, we illustrate current approaches that consider climate drivers in the context of nonlinear disease dynamics. The challenge of considering climate in the context of other aspects of change goes beyond socioeconomic factors and includes pathogen evolution. Importantly, however, this is not an argument against the importance of climate itself, as we illustrate with the open question of the possible synergy of climate and drug resistance.

[1]  Jeff Miller,et al.  Coral bleaching and disease combine to cause extensive mortality on reefs in US Virgin Islands , 2006, Coral Reefs.

[2]  W. Wernsdorfer,et al.  The epidemiology of human malaria as an explanation of its distribution, including some implications for its control. , 1988 .

[3]  M. Bouma,et al.  Epidemic malaria in India's Thar desert , 1995, The Lancet.

[4]  D. Kwiatkowski,et al.  Parasite virulence and disease patterns in Plasmodium falciparum malaria. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[5]  Kevin D Lafferty,et al.  The ecology of climate change and infectious diseases. , 2010, Ecology.

[6]  S. Randolph,et al.  Ticks are not Insects: Consequences of Contrasting Vector Biology for Transmission Potential. , 1998, Parasitology today.

[7]  C. Friedman,et al.  Withering Syndrome in Farmed Red Abalone Haliotis rufescens: Thermal Induction and Association with a Gastrointestinal Rickettsiales-like Prokaryote. , 2000, Journal of aquatic animal health.

[8]  Fält Johan,et al.  Tick-borne encephalitis (TBE) in Skåne, southern Sweden: A new TBE endemic region? , 2006, Scandinavian journal of infectious diseases.

[9]  S. Randolph,et al.  Behavioural responses to perceived risk of tick-borne encephalitis: vaccination and avoidance in the Baltics and Slovenia. , 2008, Vaccine.

[10]  P. Martens,et al.  Climate change and human health in Europe , 1999, BMJ.

[11]  C. Turner Antigenic variation in Trypanosoma brucei infections: an holistic view. , 1999, Journal of cell science.

[12]  D. Rogers,et al.  The Global Spread of Malaria in a Future , Warmer World , 2022 .

[13]  W. Martens Health and Climate Change: Modelling the Impacts of Global Warming and Ozone Depletion , 1998 .

[14]  P Reiter,et al.  Climate change and mosquito-borne disease. , 2001, Environmental health perspectives.

[15]  E. Lindgren,et al.  Tick-borne encephalitis in Sweden and climate change , 2001, The Lancet.

[16]  S. Randolph Ticks and tick-borne disease systems in space and from space. , 2000, Advances in parasitology.

[17]  J. Mendelson,et al.  Riding the Wave: Reconciling the Roles of Disease and Climate Change in Amphibian Declines , 2008, PLoS biology.

[18]  B. Young,et al.  Widespread amphibian extinctions from epidemic disease driven by global warming , 2006, Nature.

[19]  R. Ostfeld,et al.  BIODIVERSITY AND THE DILUTION EFFECT IN DISEASE ECOLOGY , 2001 .

[20]  E. Gould,et al.  Persistence and transmission of tick-borne viruses: Ixodes ricinus and louping-ill virus in red grouse populations , 1995, Parasitology.

[21]  A. Dobson,et al.  Emerging infectious pathogens of wildlife. , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[22]  L. F. Chaves,et al.  Social Exclusion Modifies Climate and Deforestation Impacts on a Vector-Borne Disease , 2008, PLoS neglected tropical diseases.

[23]  W. Hawley,et al.  Aedes albopictus in North America: probable introduction in used tires from northern Asia. , 1987, Science.

[24]  S I Hay,et al.  Etiology of interepidemic periods of mosquito-borne disease. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[25]  Mercedes Pascual,et al.  Disentangling Extrinsic from Intrinsic Factors in Disease Dynamics: A Nonlinear Time Series Approach with an Application to Cholera , 2004, The American Naturalist.

[26]  A. Peterson,et al.  Modeling current and future potential wintering distributions of eastern North American monarch butterflies , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[27]  Felicia Keesing,et al.  Sacred Cows and Sympathetic Squirrels: The Importance of Biological Diversity to Human Health , 2006, PLoS medicine.

[28]  Craig Loehle,et al.  Social barriers to pathogen transmission in wild animal populations , 1995 .

[29]  Mercedes Pascual,et al.  Detecting nonlinear dynamics in spatio-temporal systems, examples from ecological models , 1996 .

[30]  R. Ostfeld,et al.  Biodiversity and Disease Risk: the Case of Lyme Disease , 2000 .

[31]  K. Lindblade,et al.  Land use change alters malaria transmission parameters by modifying temperature in a highland area of Uganda , 2000, Tropical medicine & international health : TM & IH.

[32]  E L Ionides,et al.  Inference for nonlinear dynamical systems , 2006, Proceedings of the National Academy of Sciences.

[33]  A. Simmons,et al.  Dispersal and Seasonal Occurrence of Noctuidonema guyanense, an Ectoparasitic Nematode of Adult Fall Armyworm (Lepidoptera: Noctuidae), in the United States2 , 1991 .

[34]  A. Dobson,et al.  Parasites dominate food web links. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[35]  C. Huntingford,et al.  Impact of climate change on health: what is required of climate modellers? , 2007, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[36]  E. Hoberg,et al.  Global warming is changing the dynamics of Arctic host–parasite systems , 2005, Proceedings of the Royal Society B: Biological Sciences.

[37]  Michael Taylor Diversity of life , 1994, Nature.

[38]  Andrew J Tatem,et al.  Global traffic and disease vector dispersal. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[39]  Felicia Keesing,et al.  The ecology of infectious disease: Effects of host diversity and community composition on Lyme disease risk , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[40]  D. Argaw,et al.  Malaria epidemics in the highlands of Ethiopia. , 2005, East African medical journal.

[41]  P. Epstein,et al.  Climate change and human health. , 1996, The New England journal of medicine.

[42]  J. Reynolds,et al.  Climate Change and Distribution Shifts in Marine Fishes , 2005, Science.

[43]  Roy M. Anderson,et al.  Vaccination and herd immunity to infectious diseases , 1985, Nature.

[44]  J Rotmans,et al.  Potential impact of global climate change on malaria risk. , 1995, Environmental health perspectives.

[45]  David L. Smith,et al.  Ecological theory to enhance infectious disease control and public health policy. , 2005, Frontiers in ecology and the environment.

[46]  A. Dobson,et al.  Projected Impacts of Climate and Land-Use Change on the Global Diversity of Birds , 2007, PLoS biology.

[47]  L. F. Chaves,et al.  Shifting patterns: malaria dynamics and rainfall variability in an African highland , 2008, Proceedings of the Royal Society B: Biological Sciences.

[48]  C. Dye,et al.  Population dynamics of mosquito-borne disease: persistence in a completely heterogeneous environment. , 1988, Theoretical population biology.

[49]  C. Saegerman,et al.  Bluetongue Epidemiology in the European Union , 2008, Emerging infectious diseases.

[50]  F. Jongejan,et al.  Modeling the spatial distribution of crimean-congo hemorrhagic fever outbreaks in Turkey. , 2007, Vector borne and zoonotic diseases.

[51]  J. Patz,et al.  Malaria risk and temperature: influences from global climate change and local land use practices. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[52]  S. Hay,et al.  Satellite imagery in the study and forecast of malaria , 2002, Nature.

[53]  Francesco Checchi,et al.  Malaria Epidemics and Interventions, Kenya, Burundi, Southern Sudan, and Ethiopia, 1999–2004 , 2006, Emerging infectious diseases.

[54]  M. Pascual,et al.  Inapparent infections and cholera dynamics , 2008, Nature.

[55]  Sarah E. Randolph,et al.  Tsetse Flies in Africa: Bane or Boon? , 1988 .

[56]  A. Tulu Determinants of malaria transmission in the highlands of Ethiopia : the impact of global warming on morbidity and mortality ascribed to malaria. , 1996 .

[57]  A. Dicko,et al.  Malaria incidence in relation to rice cultivation in the irrigated Sahel of Mali. , 2004, Acta tropica.

[58]  Monica F. Myers,et al.  Climate change and the resurgence of malaria in the East African highlands , 2002, Nature.

[59]  H. Landsberg Trends in Climatology: The investigation of climates is moving from a descriptive science to a science grounded in physics , 1958 .

[60]  Jane-Ling Wang,et al.  Mosquitoes do senesce: departure from the paradigm of constant mortality. , 2007, The American journal of tropical medicine and hygiene.

[61]  Parviez R. Hosseini,et al.  Seasonality and wildlife disease: how seasonal birth, aggregation and variation in immunity affect the dynamics of Mycoplasma gallisepticum in house finches , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[62]  L. Hannah,et al.  Climate change and biodiversity : synergistic impacts , 2003 .

[63]  R M May,et al.  Coevolution of hosts and parasites , 1982, Parasitology.

[64]  J. Simon,et al.  Extinction rates. , 1996, Science.

[65]  J. Cox,et al.  Early effects of climate change: do they include changes in vector-borne disease? , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[66]  T. Solomon,et al.  Pathogenic flaviviruses , 2008, The Lancet.

[67]  P. Garnham The incidence of malaria at high altitudes. , 1948, Journal. National Malaria Society.

[68]  P. Kaye Infectious diseases of humans: Dynamics and control , 1993 .

[69]  A. Osterhaus,et al.  Identification of virus causing recent seal deaths , 1988, Nature.

[70]  S. Hay,et al.  The decline in paediatric malaria admissions on the coast of Kenya , 2007, Malaria Journal.

[71]  M. Pascual,et al.  Refractory periods and climate forcing in cholera dynamics , 2005, Nature.

[72]  S. Carpenter,et al.  Global Consequences of Land Use , 2005, Science.

[73]  P. Reiter,et al.  The used tire trade: a mechanism for the worldwide dispersal of container breeding mosquitoes. , 1987, Journal of the American Mosquito Control Association.

[74]  C. Kunz Tick-borne encephalitis in Europe. , 1992, Acta Leidensia.

[75]  D. Earn,et al.  A simple model for complex dynamical transitions in epidemics. , 2000, Science.

[76]  L. F. Chaves,et al.  Sources and sinks: revisiting the criteria for identifying reservoirs for American cutaneous leishmaniasis. , 2007, Trends in parasitology.

[77]  C. Rogers,et al.  Bleaching increases likelihood of disease on Acropora palmata (Lamarck) in Hawksnest Bay, St John, US Virgin Islands , 2008, Coral Reefs.

[78]  A. El Gaddal,et al.  Malaria control in the Gezira-Managil Irrigated Scheme of the Sudan. , 1985, The Journal of tropical medicine and hygiene.

[79]  Michael W. Parker,et al.  Origin of the West Nile virus responsible for an outbreak of encephalitis in the northeastern United States. , 1999, Science.

[80]  P E Fine,et al.  Herd immunity: history, theory, practice. , 1993, Epidemiologic reviews.

[81]  D. Lusseau,et al.  Parallel influence of climate on the behaviour of Pacific killer whales and Atlantic bottlenose dolphins , 2004 .

[82]  M. Bouma,et al.  Falciparum malaria and climate change in the northwest frontier province of Pakistan. , 1996, The American journal of tropical medicine and hygiene.

[83]  Grenfell,et al.  Cities and villages: infection hierarchies in a measles metapopulation , 1998 .

[84]  S. Frank A model for the sequential dominance of antigenic variants in African trypanosome infections , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[85]  L. Mydlarz,et al.  Cellular Responses in Sea Fan Corals: Granular Amoebocytes React to Pathogen and Climate Stressors , 2008, PloS one.

[86]  G. Medley,et al.  Ruminating on complexity: macroparasites of wildlife and livestock. , 2004, Trends in ecology & evolution.

[87]  O. Diekmann,et al.  On the definition and the computation of the basic reproduction ratio R0 in models for infectious diseases in heterogeneous populations , 1990, Journal of mathematical biology.

[88]  J. Jones,et al.  Climate change and human health. , 1997, South African medical journal = Suid-Afrikaanse tydskrif vir geneeskunde.

[89]  H. Hoogstraal The epidemiology of tick-borne Crimean-Congo hemorrhagic fever in Asia, Europe, and Africa. , 1979, Journal of medical entomology.

[90]  M. Bouma Methodological problems and amendments to demonstrate effects of temperature on the epidemiology of malaria. A new perspective on the highland epidemics in Madagascar, 1972-89. , 2003, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[91]  M. Bouma,et al.  The EI Niño Southern Oscillation and the historic malaria epidemics on the Indian subcontinent and Sri Lanka: an early warning system for future epidemics? , 1996, Tropical medicine & international health : TM & IH.

[92]  Simon I Hay,et al.  Hot topic or hot air? Climate change and malaria resurgence in East African highlands. , 2002, Trends in parasitology.

[93]  S. Hay,et al.  Malaria in Kenya's Western Highlands , 2005, Emerging infectious diseases.

[94]  D. Campbell-Lendrum,et al.  How much disease could climate change cause , 2003 .

[95]  L. F. Chaves,et al.  Predicting endemic cholera: the role of climate variability and disease dynamics , 2008 .

[96]  R. Alford,et al.  Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[97]  S. P. Ellner,et al.  Measles as a case study in nonlinear forecasting and chaos , 1994, Philosophical Transactions of the Royal Society of London. Series A: Physical and Engineering Sciences.

[98]  D. Henderson,et al.  Cholera Dynamics and El Niño – Southern Oscillation , 2010 .

[99]  G. Yohe,et al.  A globally coherent fingerprint of climate change impacts across natural systems , 2003, Nature.

[100]  B. Sharp,et al.  Potential effect of climate change on malaria transmission in Africa , 2003, The Lancet.

[101]  Marcel Tanner,et al.  Effect of irrigation and large dams on the burden of malaria on a global and regional scale. , 2005, The American journal of tropical medicine and hygiene.

[102]  M. Pascual,et al.  Stochastic amplification in epidemics , 2007, Journal of The Royal Society Interface.

[103]  O. Bjørnstad,et al.  The dynamics of measles in sub-Saharan Africa , 2008, Nature.

[104]  M. Loevinsohn,et al.  Climatic warming and increased malaria incidence in Rwanda , 1994, The Lancet.

[105]  P. Epstein Is global warming harmful to health? , 2000, Scientific American.

[106]  P. Reiter,et al.  From Shakespeare to Defoe: malaria in England in the Little Ice Age. , 2000, Emerging infectious diseases.

[107]  S. Randolph,et al.  Climate Change Cannot Explain the Upsurge of Tick-Borne Encephalitis in the Baltics , 2007, PloS one.

[108]  P. Atkinson,et al.  Reflection & Reaction Global warming and malaria: a call for accuracy , 2004 .

[109]  P. Hudson,et al.  Negative effects of changing temperature on amphibian immunity under field conditions , 2006 .

[110]  P. Pockley Bushfires leave ecologists hot under the collar , 2002, Nature.

[111]  A. Onapa,et al.  Evolution of malaria in Africa for the past 40 years: impact of climatic and human factors. , 1998, Journal of the American Mosquito Control Association.

[112]  S. Randolph,et al.  Socio‐economic factors in the differential upsurge of tick‐borne encephalitis in central and Eastern Europe , 2008, Reviews in medical virology.

[113]  D. Rogers,et al.  Fragile transmission cycles of tick-borne encephalitis virus may be disrupted by predicted climate change , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[114]  R. Ostfeld,et al.  Effects of species diversity on disease risk. , 2006, Ecology letters.

[115]  Mercedes Pascual,et al.  ENSO and cholera: A nonstationary link related to climate change? , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[116]  L. F. Chaves,et al.  Malaria resurgence in the East African highlands: temperature trends revisited. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[117]  N. L. Kalra,et al.  Epidemic of malaria in Barmer district (Thar desert) of Rajasthan during 1990. , 1992, Indian journal of malariology.

[118]  Andrew P. Morse,et al.  Malaria early warnings based on seasonal climate forecasts from multi-model ensembles , 2006, Nature.

[119]  J. Cox,et al.  Altitude-dependent and -independent variations in Plasmodium falciparum prevalence in northeastern Tanzania. , 2005, The Journal of infectious diseases.