Abstract Extrinsic environmental factors influence the spatiotemporal dynamics of many organisms, including insects that transmit the pathogens responsible for vector‐borne diseases (VBDs). Temperature is an especially important constraint on the fitness of a wide variety of ectothermic insects. A mechanistic understanding of how temperature impacts traits of ectotherms, and thus the distribution of ectotherms and vector‐borne infections, is key to predicting the consequences of climate change on transmission of VBDs like malaria. However, the response of transmission to temperature and other drivers is complex, as thermal traits of ectotherms are typically nonlinear, and they interact to determine transmission constraints. In this study, we assess and compare the effect of temperature on the transmission of two malaria parasites,Plasmodium falciparumandPlasmodium vivax, by two malaria vector species,Anopheles gambiaeandAnopheles stephensi. We model the nonlinear responses of temperature dependent mosquito and parasite traits (mosquito development rate, bite rate, fecundity, proportion of eggs surviving to adulthood, vector competence, mortality rate, and parasite development rate) and incorporate these traits into a suitability metric based on a model for the basic reproductive number across temperatures. Our model predicts that the optimum temperature for transmission suitability is similar for the four mosquito–parasite combinations assessed in this study, but may differ at the thermal limits. More specifically, we found significant differences in the upper thermal limit between parasites spread by the same mosquito (A. stephensi) and between mosquitoes carryingP. falciparum. In contrast, at the lower thermal limit the significant differences were primarily between the mosquito species that both carried the same pathogen (e.g.,A. stephensiandA. gambiaeboth withP. falciparum). Using prevalence data, we show that the transmission suitability metric calculated from our mechanistic model is consistent with observedP. falciparumprevalence in Africa and Asia but is equivocal forP. vivaxprevalence in Asia, and inconsistent withP. vivaxprevalence in Africa. We mapped risk to illustrate the number of months various areas in Africa and Asia predicted to be suitable for malaria transmission based on this suitability metric. This mapping provides spatially explicit predictions for suitability and transmission risk.
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Impacts of host availability and temperature on mosquito‐borne parasite transmission
Abstract Global climate change is predicted to cause range shifts in the mosquito species that transmit pathogens to humans and wildlife. Recent modeling studies have sought to improve our understanding of the relationship between temperature and the transmission potential of mosquito‐borne pathogens. However, the role of the vertebrate host population, including the importance of host behavioral defenses on mosquito feeding success, remains poorly understood despite ample empirical evidence of its significance to pathogen transmission. Here, we derived thermal performance curves for mosquito and parasite traits and integrated them into two models of vector–host contact to investigate how vertebrate host traits and behaviors affect two key thermal properties of mosquito‐borne parasite transmission: the thermal optimum for transmission and the thermal niche of the parasite population. We parameterized these models for five mosquito‐borne parasite transmission systems, leading to two main conclusions. First, vertebrate host availability may induce a shift in the thermal optimum of transmission. When the tolerance of the vertebrate host to biting from mosquitoes is limited, the thermal optimum of transmission may be altered by as much as 5°C, a magnitude of applied significance. Second, thresholds for sustained transmission depend nonlinearly on both vertebrate host availability and temperature. At any temperature, sustained transmission is impossible when vertebrate hosts are extremely abundant because the probability of encountering an infected individual is negligible. But when host biting tolerance is limited, sustained transmission will also not occur at low host population densities. Furthermore, our model indicates that biting tolerance should interact with vertebrate host population density to adjust the parasite population thermal niche. Together, these results suggest that vertebrate host traits and behaviors play essential roles in the thermal properties of mosquito‐borne parasite transmission. Increasing our understanding of this relationship should lead us to improved predictions about shifting global patterns of mosquito‐borne disease.
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- Award ID(s):
- 1717282
- PAR ID:
- 10529514
- Publisher / Repository:
- Ecological Monographs
- Date Published:
- Journal Name:
- Ecological Monographs
- Volume:
- 94
- Issue:
- 2
- ISSN:
- 0012-9615
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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