Discussion
Understanding how changing global temperature affects the period during which parasite development can occur is crucial to modelling how the range of viability of the malaria parasite changes with time. We explore these questions using a thermodynamic model that describes the nonlinear relationship between developmental rate and temperature, for five blood-borne parasites and their arthropod hosts. For this we use a parametrization of the EIP proposed by Briére et al . (1999), using Bayesian inference methods to estimate the relevant parameters using prior knowledge assembled using an extensive literature search. For avian haemosporidia – P. relictum , Leucocytozoonspp., Haemoproteus spp. - we are not aware of any prior attempt to obtain the constants defining the EIP as parameterized for the Briére equation. We believe this calculation presents those results for the first time
Using measures of mean temperature versus the diurnal fluctuating temperature in the field, we demonstrated both spatial and temporal variation in malaria transmission risk in the western Himalayan region. Both human malaria and avian malaria prevalence vary with season and intensity across these sites. We showed that for all five vector-borne parasites transmission was most strongly constrained by temperature in high elevation (3200 m) environments throughout the year, and that different models provided largely consistent results for lower elevations.
Whilst the temperature and transmission windows we calculate could fit within the lifespan of Anopheles species in general, it is important to note here that our study was primarily designed for the forested habitat with no records of Anopheles species (FI unpublished data). Malaria incidence has been reported from human dominated hilly areas below 2000 m with high prevalence forAnopheles mosquitoes incriminated as prime malaria vectors (Shukla et al . 2007). Our analysis showed that the temperature conditions are not conducive for malaria transmission in the current scenario and the diurnal temperature fluctuation has no effect on malaria transmission biology. In line with the Government of India’s National Framework for Malaria Elimination in India 2016–2030 Program (NVBDCP 2016), it is crucial now to apply such approaches for identification of hotspots using fine-scale data which can help in addressing the ecological drivers of malaria transmission (Mishraet al . 2016). These temperature estimates have implications on defining the parasite transmission limits across spatio-temporal scales: i) EIP responds in a non-linear fashion to temperature and is sensitive to small changes in temperature which could have significant effects on the parasite transmission window (e.g., Blanford et al . 2013); ii) hourly fluctuations in temperature are experienced in the field by both mosquito and parasite which could provide site-specific insights into parasite transmission range at a small spatial scale. While our data do capture these effects explicitly using mean versus DTR measures, we emphasised that using site-specific data is important for deriving insights into malaria transmission range. Our comparisons of EIP calculated using local meteorological data and WorldClim data showed that relying on weather station data might underestimate the parasite development in a highly seasonal ecosystem with distinct physiographic climatic conditions.
The changing climate has rapidly influenced the rainfall, temperature, and vegetation phenology. These changes are causing shifts in the timing of species activity. For example, a surge in temperature has shifted timing and length of breeding season in birds (Hällfors et al . 2020) leading to mismatch with optimal resource abundance which is vital for reproductive success. For short-lived ectotherms, the spread of mosquito species to new habitats in high elevations, short generation times, high population growth rates and strong temperature-imposed selection could lead to fast adaptation (Couper et al . 2021).
In the western Himalayan context, the thermodynamic model showed that the EIP days do not support transmission of avian haemosporidians parasites at high elevation sites (3200m). However, EIP days have limited transmission windows for Plasmodium , Haemoproteusand Leucocytozoon from 1800-2000 m. This further implies that low to mid elevation sites have optimal conditions and lack thermal constraints for parasite transmission during peak breeding season (April-May). Ishtiaq and Barve (2018) showed that the probability of infection with Plasmodium parasite declines steeply with elevation. In contrast, Leucocytozoon spp. infection risk increases with elevation, however, most of these infections were sub microscopic in high elevation in breeding season (April-May). This contrasts with studies on the ecology of haemosporidia in temperate regions where birds with latent infections return to the breeding grounds and experience a relapse, with increase in parasites visible in the blood stages (Applegate 1970, Becker et al . 2020). In general, parasite intensity showed a significant decline with elevation in the breeding season (April-May) and an increase across mid-elevations in the nonbreeding season. The absence of gametocytes (infective stage) in the blood during spring season or late emergence of vectors due to environmental conditions could lead to the disruption of transmission cycles (migratory mismatch).
Our data support the hypothesis that avian Plasmodium ,Haemoproteus and Leucocytozoon are currently restricted by thermal gradient and provide an ecological explanation for absence of gametocytes in breeding season at high elevation. This further implies that fledgelings might be at the risk of haemosporidian (Haemoproteus ) infections from June-August which coincides with peak emergence of Culicoides spp. in 2000-2600 m sites (Ishtiaq et al. unpublished data). Using a thermodynamic model, we supported thePlasmodium relictum transmission scenario in Hawaiian Islands using Degree-day models with 13°C as minimum temperature and 30° C as maximum temperature threshold to complete sporogonic development (LaPointe et al . 2010).
We used climate models to interrogate how changing temperature from 2021-2040 could potentially lead to an expansion of the temperature range conducive for malaria transmission in high elevation zones. Using mean temperature data, we found low elevation sites (1800m) might experience unsuitable conditions for parasite transmission in the future which suggests that some habitats that are currently too cool to sustain vector populations may become more favourable in the future, whereas others that are drying may become less conducive to vector reproduction. Therefore, the geographic ranges of mosquitoes may expand or be reduced, which may cause parallel changes in the population of malaria pathogens they transmit. Such expansion also increases the time window of malaria transmission resulting in a larger number of generations of parasites per year that can positively affect parasite abundance (Schroderet al . 2008).
One of the limitations of our study is the use of one year data to define these thermal effects at a small spatial scale. To quantify these temperature effects at a fine scale, we need long-term data across multiple sites. Nevertheless, the mean temperature variation using field data and WorldClim records exhibited similar patterns in parasite transmission range. Furthermore, our modelling using mean versus hourly temperatures captures the EIP variation which is corroborated by the prevalence and intensity of parasites characterised in avian hosts. Our data illustrates the contrasting thermal environments that can exist across relatively small spatial scales within a region and can have divergent effects on parasite development.