Exploring the thermal limits of malaria transmission in the western Himalaya.

Environmental temperature is a key driver of malaria transmission dynamics. Using detailed temperature records from four sites: low elevation (1800), mid elevation (2200 m), and high elevation (2600-3200 m) in the western Himalaya, we model how temperature regulates parasite development rate (the inverse of the extrinsic incubation period, EIP) in the wild. Using a Briére parametrization of the EIP, combined with Bayesian parameter inference, we study the thermal limits of transmission for avian (Plasmodium relictum) and human Plasmodium parasites (P. vivax and P. falciparum) as well as for two malaria-like avian parasites, Haemoproteus and Leucocytozoon. We demonstrate that temperature conditions can substantially alter the incubation period of parasites at high elevation sites (2600-3200 m) leading to restricted parasite development or long transmission windows. The thermal limits (optimal temperature) for Plasmodium parasites were 15.62-34.92°C (30.04°C) for P. falciparum, 13.51-34.08°C (29.02°C) for P. vivax, 12.56-34.46°C (29.16°C) for P. relictum and for two malaria-like parasites, 12.01-29.48°C (25.16°C) for Haemoproteus spp. and 11.92-29.95°C (25.51°C) for Leucocytozoon spp. We then compare estimates of EIP based on measures of mean temperature versus hourly temperatures to show that EIP days vary in cold versus warm environments. We found that human Plasmodium parasites experience a limited transmission window at 2600 m. In contrast, for avian Plasmodium transmission was not possible between September and March at 2600 m. In addition, temperature conditions suitable for both Haemoproteus and Leucocytozoon transmission were obtained from June to August and in April, at 2600 m. Finally, we use temperature projections from a suite of climate models to predict that by 2040, high elevation sites (~2600 m) will have a temperature range conducive for malaria transmission, albeit with a limited transmission window. Our study highlights the importance of accounting for fine-scale thermal effects in the expansion of the range of the malaria parasite with global climate change.