Award Abstract # 1518681
Effects of temperature on vector-borne disease transmission: integrating theory with empirical data

NSF Org: DEB
Division Of Environmental Biology
Recipient: THE LELAND STANFORD JUNIOR UNIVERSITY
Initial Amendment Date: August 25, 2015
Latest Amendment Date: August 28, 2019
Award Number: 1518681
Award Instrument: Continuing Grant
Program Manager: Samuel Scheiner
DEB
 Division Of Environmental Biology
BIO
 Directorate for Biological Sciences
Start Date: September 1, 2015
End Date: August 31, 2021 (Estimated)
Total Intended Award Amount: $2,190,450.00
Total Awarded Amount to Date: $2,402,276.00
Funds Obligated to Date: FY 2015 = $1,846,842.00
FY 2016 = $20,500.00

FY 2017 = $511,158.00

FY 2019 = $23,776.00
History of Investigator:
  • Erin Mordecai (Principal Investigator)
    emordeca@stanford.edu
Recipient Sponsored Research Office: Stanford University
450 JANE STANFORD WAY
STANFORD
CA  US  94305-2004
(650)723-2300
Sponsor Congressional District: 16
Primary Place of Performance: Stanford University
Department of Biology
Stanford
CA  US  94305-5020
Primary Place of Performance
Congressional District:
16
Unique Entity Identifier (UEI): HJD6G4D6TJY5
Parent UEI:
NSF Program(s): Ecology of Infectious Diseases
Primary Program Source: 01001516DB NSF RESEARCH & RELATED ACTIVIT
01001516RB NSF RESEARCH & RELATED ACTIVIT

01001617DB NSF RESEARCH & RELATED ACTIVIT

01001718DB NSF RESEARCH & RELATED ACTIVIT

01001819DB NSF RESEARCH & RELATED ACTIVIT

01001920DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s): 7242, 9169, 9178, 9251, CL10, EGCH
Program Element Code(s): 724200
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.074

ABSTRACT

Understanding how temperature affects disease-causing organisms and the mosquitoes that carry them is critical for predicting and responding to future changes in disease risk. Many of the world's most devastating and neglected infectious diseases require mosquitoes and other insects for transmission between people. Malaria kills over 650,000 people each year, mostly children in sub-Saharan Africa, and pathogens like West Nile virus, dengue virus, and chikungunya virus are on the rise in both North America and the tropics. Mosquitoes and the pathogens they carry are sensitive to the environment, so changes in climate, particularly temperature, affect disease risk both in the tropics and in temperate areas. This award supports research to measure the effect of temperature on 13 different pathogens that use mosquitoes and flies for transmission, and the capacity for two common mosquitoes in the Americas to adapt to different temperature conditions. In addition, this work will support STEM education through training in science and math with a focus on under-represented groups, and will contribute publicly available data that can be used by other researchers and public health professionals.

The goal of this project is to develop a general framework for predicting the temperature sensitivity of vector transmission. This work addresses three main questions: (1) How does vector-borne pathogen transmission respond to temperature? (2) How important is the influence of temperature, relative to other factors, on transmission in the field? (3) Can such transmission adapt to local temperature regimes? The research will develop temperature-sensitive transmission models and fit them with data from the existing literature for 13 vector-borne diseases: vivax malaria, trypanosomiasis, dengue, chikungunya, yellow fever, West Nile, Eastern equine encephalitis, Western equine encephalitis, St. Louis encephalitis, Rift Valley fever, Ockelbo (Sindbis) disease, Ross River fever, and bluetongue. Laboratory experiments will measure local thermal adaptation of Aedes aegypti and Ae. albopictus mosquitoes, which transmit dengue and other viruses, from across their geographic and temperature ranges. In tandem, the research will develop and test theory on how vectors and parasites respond to temperature based on theory from physiological ecology. New local-scale data collected in Ecuador on transmission risk, dengue cases, climate, and other social and economic factors will be used to validate the model predictions. Complementing these local-scale data, the research will develop a global database on field transmission from the existing literature, along with climatic and socioeconomic information. Together, these field data will test the accuracy of the transmission models and assess the relative importance of temperature for transmission at scales from neighborhood to continent.

PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH

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Ali, S., O. Gugliemini, S. Harber, S. Harrison, L. Houle, J. Ivory, S. Kersten, R. Khan, J. Kim, C. LeBoa, E. Nez-Whitfield, J. O?Marr, E. Rothenberg, R. M. Segnitz, S. Sila, A. Verwillow, M. Vogt, A. Yang, and E. A. Mordecai "Environmental and Social Change Drive the Explosive Emergence of Zika Virus in the Americas" PLoS Neglected Tropical Diseases , 2017
Anna M. Stewart-Ibarra, Aileen Kenneson, Christine A. King, Mark Abbott, Arturo Barbachano-Guerrero, Efrain Beltran-Ayala, Mercy J. Borbor-Cordova, Washington B. Cardenas, Cinthya Cueva, Julia L. Finkelstein, Christina D. Lupone, Richard G. Jarman, Irina "The Burden of Dengue Fever and Chikungunya in Southern Coastal Ecuador: Epidemiology, Clinical Presentation, and Phylogenetics from the First Two Years of a Prospective Study" American Journal of Tropical Medicine and Hygiene , v.98 , 2018 , p.1444 10.4269/ajtmh.17-0762
Athni, T.S., Shocket, M.S., Couper, L.I., Nova, N., Caldwell, I.R., Caldwell, J.M., Childress, J.N., Childs, M.L., De Leo, G.A., Kirk, D., MacDonald, A.J., Olivarius, K., Pickel, D.G., Roberts, S.O., Winokur, O.C., Young, H.S., Cheng, J., Grant, E.A., Kur "The influence of vector-borne disease on human history: socio-ecological mechanisms" Ecology Letters , v.24 , 2021 , p.829
Bradley, P.W., Brawner, M.D., Raffel, T.R., Rohr, J.R., Olson, D.H., Blaustein, A.R. "Shifts in temperature influence how an emerging infectious fungus infects amphibian larvae" PLoS One , 2019 10.1101/165985
Caldwell, J.M., LaBeaud, A.D., Lambin, E.F., Stewart-Ibarra, A.M., Ndenga, B. A., Mutuku, F.M, Krystosik, A.R., Beltran Ayala, E., Anyamba, A., Borbor-Cordova, M., Damoah, R., Grossi-Soyster, E.N., Heras, F., Ngugi, H. N., Ryan, S.J., Shah, M. M., Sippy, "Climate explains geographic and temporal variation in mosquito-borne disease dynamics on two continents" Nature Communications , 2021
Carlson, C.J., Dougherty, E., Boots, M., Getz, W.M., Ryan, S.J. "Consensus and conflict among ecological forecasts of Zika virus outbreaks in the United States" Scientific Reports , v.8 , 2018 , p.4921
Cator, L.J., Johnson, L.R., Mordecai, E.A., El Moustaid, F., Smallwood, T.R.C., LaDeau, S.L., Johansson, M.A., Hudson, P.J., Boots, M., Thomas, M.B., Power, A.G., Pawar, S. "The role of vector trait variation in vector-borne disease dynamics" Frontiers in Ecology and Evolution , v.8 , 2020 10.3389/fevo.2020.00189
Childs, M.L., Kain, M.P. , Harris, M.J., Becker, A.D., Kirk, D.G., Couper, L.I., Nova, N., Delwel, I.O., Ritchie, J., Mordecai, E.A. "The impact of long-term non-pharmaceutical interventions on COVID-19 epidemic dynamics and control" Proceedings of the Royal Society B , v.288 , 2021 , p.20210811
Childs, M., Nova, N., Colvin, J., Mordecai, E.A. "Mosquito and primate ecology predict human risk of yellow fever virus spillover in Brazil" Philosophical Transactions of the Royal Society B: Biological Sciences , v.374 , 2019 , p.rstb.2018 10.1098/rstb.2018.0335
Cohen, J., Civitello, D.J., Brace, A.J., Feichtinger, E, Ortega, N., Richardson, J.C., Sauer, E.L., Liu, X., Rohr, J.R. "Spatial scale modulates the strength of ecological processes driving disease distributions" Proceedings of the National Academy of Sciences , v.113 , 2016 , p.E3359
Cohen, J.M., Civitello, D.J., Venesky, M.D., McMahon, T.A., Rohr, J.R. "An interaction between climate change and infectious disease drove widespread amphibian declines" Global Change Biology , v.25 , 2019 , p.927 10.1111/gcb.14489
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PROJECT OUTCOMES REPORT

Disclaimer

This Project Outcomes Report for the General Public is displayed verbatim as submitted by the Principal Investigator (PI) for this award. Any opinions, findings, and conclusions or recommendations expressed in this Report are those of the PI and do not necessarily reflect the views of the National Science Foundation; NSF has not approved or endorsed its content.

This research investigated the impacts of climate and climate change on infectious diseases. We made several significant discoveries. First, we found that vector-borne diseases, which are transmitted by biting mosquitoes, flies, ticks, fleas, and other arthropods, are highly sensitive to temperature and transmission peaks at intermediate temperatures (between 23-29 degrees C or 73-84 degrees F), depending on the disease and vector. These peak temperatures are increasingly occurring in temperate and highland regions where diseases like malaria, West Nile, dengue, and Lyme disease have historically been absent or eliminated. We found that some regions may see shifts in which diseases and mosquito and tick species present the greatest threat. For example, as the temperature warms in sub-Saharan Africa, much of the region that is currently malaria-endemic may see temperatures so warm that malaria (which has peak transmission at 25 degrees C or 77 degrees F) begins to decline, while dengue and its mosquito vector, which thrive at warmer temperatures (peaking at 29 degrees C or 84 degrees F), becomes more common. Mountainous and temperate areas in Africa, Asia, and Latin America are becoming more suitable for malaria, dengue, and other mosquito-borne diseases as the climate warms. Recent warmer winters are driving an expansion of Lyme disease in the northeastern part of the United States, and future warmer winters are likely to further increase the number of Lyme disease cases in the Northeast and Midwest.

 

We also developed and tested theory that predicts how diseases will spread under warming climates. Across hundreds of different wild animal species, we found support for the "thermal mismatch hypothesis", which predicts that the burden of diseases is highest at temperatures to which a species is poorly adapted. Thermal mismatches are part of the reason that the emerging chytrid fungus disease (Bd) now threatens many cold-adapted frog and salamander species with extinction as the climate warms. We found that how animal metabolisms respond to temperature can predict the effects of climate on mosquito-borne disease transmission, providing an opportunity to understand the effects of climate on newly emerging diseases. Finally, we found that mosquitoes that transmit diseases have potential to evolve to tolerate warmer temperatures as the climate warms, due to their large population sizes, short life cycles, and ecological flexibility in adapting to new habitats. Our work concludes that climate change has the potential to greatly expand the transmission of many devastating diseases, including malaria, dengue, Zika, West Nile, and Lyme disease, into new regions, and to drive unexpected changes in disease that can cause public health crises. In concert with deforestation and other types of land use change, human impacts on the environment are creating major threats to human health.

 

Finally, we conducted controlled experiments in the laboratory and mosquito trapping in the field to discover how the capacity for mosquitoes to transmit malaria, dengue, chikungunya, and Zika varies with weather and climate in the real world. Comparing sites across both Ecuador and Kenya, we found that measurements of the local weather, combined with a mathematical model, can predict when people get bitten by mosquitoes and get infected with dengue, chikungunya, and Zika viruses, but that the ages of household members, access to piped water, and the construction materials of the home all affected these risks. Based on observations that in regions of Africa where people regularly use bed nets, malaria-transmitting mosquitoes begin to bite earlier in the evening or in the early morning, we tested how these shifts in biting behavior affect mosquito capacity to transmit malaria. We found that while early evening biting increases malaria transmission compared to late night biting, morning biting reduces malaria transmission by exposing mosquitoes to warm temperatures that inhibit parasite development. Together, this research shows that temperature, rainfall, and humidity have powerful influences on mosquito and disease dynamics that are likely to change with climate change, but can be predicted using experiments and mathematical models in order to prevent the worst outcomes of climate change for disease.

 

This research provided training opportunities for 66 graduate, undergraduate, high school, and postdoctoral students. Our work was covered in major national and international news outlets, in public seminars in Ecuador, Kenya, Australia, and elsewhere, and in classrooms at Stanford University, UCLA, Penn State University, the University of Florida, the University of South Florida, Virginia Tech, and Notre Dame University. We worked with vector control and Ministry of Health officials and community members in Kenya and Ecuador to develop sustainable strategies for reducing mosquito and disease exposure. We presented our work at the White House Office of Science Technology and Policy and participated in analyses of the impacts of climate change on human health for the Intergovernmental Panel on Climate Change Sixth Assessment Report (IPCC AR6) and social costs of carbon estimates to be used in the Biden administration environmental policy.

 


Last Modified: 09/16/2021
Modified by: Erin Mordecai

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