Introduction
Changes in climate are shifting the geographic ranges of species (e.g., birds; Chen et al . 2011, Freeman et al . 2018). These have a significant influence on parasite transmission dynamics, either by exposing immunologically naïve hosts to longer transmission seasons or bridging novel host-parasite interactions (Patz et al . 2001). Among vector-borne pathogens, malaria parasites have remained the most virulent group, with high sensitivity to climatic factors which continue to threaten both human and many wild animal populations (van Riperet al . 1999).
Temperature is the key environmental driver influencing the transmission dynamics and distribution of malaria parasites. The rate of malaria parasite transmission and intensity of infection is strongly determined by the extrinsic incubation period (EIP: also known as the duration of sporogony), the time it takes for a parasite to develop within a mosquito and become transmissible (Ohm et al . 2018). Therefore, the EIP determines the parasite development rate in the midgut after many replication cycles before it migrates as a sporozoite (infective stage) in the salivary glands of an arthropod vector. The development rate of a parasite depends on host, parasite, and environmental conditions. These conditions must be conducive for transmission of the parasite. For example, the EIP of human Plasmodium is dependent on temperature and the parasite generally takes 8–14 days to develop, so if adult Anopheles mosquitoes die before or within a 12-day period, they are unlikely to contribute to parasite transmission (Killeen et al . 2000, Paijmans et al . 2009, Ohm et al . 2018). In addition, temperature plays a central role in regulating mosquito population dynamics, age-structure in a population, life-history traits, fitness and phenology of vectors and parasites, leading to complex spatial and temporal patterns of distribution (Beck-Johnson et al . 2013).
Most mechanistic models of human Plasmodium transmission are based on the degree-day model of Detinova (Detinova 1962). The Detinova model assumes a linear relationship between ambient temperature (T ) and the parasite development rate (PDR). For example, forPlasmodium falciparum the following relationship is assumed to hold: EIP (in days) =111/(T -16), where 111 is the cumulative number of degree-days required for the parasite to complete development,T is the average ambient environmental temperature, and the relationship assumes that the temperature threshold below which development cannot occur is 16°C. However, although this equation is used in many studies, it fails to capture daily temperature fluctuations which could potentially alter the rate of parasite development and malaria transmission in a population. Other thermodynamic models propose a nonlinear relationship between temperature and growth or development (Paaijmans et al . 2009). These models can be generalised to consider temperature fluctuations which alter the length of parasite incubation period and malaria transmission rates. Therefore, epidemiological models should benefit from combining local meteorological data and diurnal temperature fluctuations to understand the biological significance of temperature in shaping parasite transmission dynamics.
Temperature is considered as the main driver for mosquito emergence and spring phenology (e.g., budburst, leaf-out, and flowering) in temperate regions (e.g., Hӓllfors et al . 2020). In the context of epidemiology of avian malaria, the overlap in seasonal emergence of vectors produces spring relapses in chronic infections (parasite phenology) and new infections in breeding host populations (Applegate 1970, Beaudoin et al . 1971). However, the implications of temperature variation for avian malaria parasite development across temperate regions are less understood.
The western Himalayas are a species-rich and highly seasonal ecosystem with distinct physiographic climatic conditions which drives bird migration, spring phenology and vector emergence (Barve et al.2016, Ishtiaq and Barve 2018). In general, birds harbour a huge diversity of three genera of haemosporidian parasites −Plasmodium, Haemoproteus and Leucocytozoon, which are more ubiquitous and cosmopolitan (except Antarctica) (Valkinũas 2005). These parasites are transmitted by dipteran insects, e.g., mosquitoes (Plasmodium ), biting midges (Haemoproteus ) and black flies (Leucocytozoon ) and have significant negative effects on the host survival and longevity (Asghar et al . 2015), reproductive success and body condition (Marzal et al . 2005). In this montane system, birds exhibit two migration strategies; species are either year-round high elevation residents (sedentary) or seasonal elevational migrants. Elevational migrants winter at low elevations or in the plains (≤ 1500 m above sea level; a.s.l.) and move to breeding grounds at higher elevations (2600–4000 m a.s.l. or even higher) during the summer season (Dixit et al . 2016). The elevational migrants are exposed to a large suite of parasites and vector fauna, especially in low elevations and move to high elevation breeding grounds only during the summer season (“migratory escape”, Loehle 1995). By contrast, sedentary counterparts potentially experience little or no exposure to parasites at high elevations in winters. Given that a competent vector and optimal thermal conditions are present, elevational migrants could act as ‘bridge hosts’ of parasite species and potentially increase transmission risk between wintering and breeding areas. This potentially increases the risk of infection to naïve resident birds at high elevations which might not have evolved to cope with parasite infection. In addition, the emergence of insect vectors (e.g., Culicoides ) is driven by temperature and does not coincide with peak bird breeding season (April-May) in a high elevation environment suggesting a mismatch in phenology of vectors and avian hosts (Ishtiaq et al. unpubl., e.g., Gethigs et al . 2015). This mismatch potentially alters the degree of interaction between host and vector species, thereby influencing parasite transmission dynamics. Only if the arrival of infected birds (with infective stages in the bloodstream) coincides with the peak of vector abundance, can transmission of pathogens from migratory birds to vectors be facilitated. There are currently no studies undertaken to understand the influence of environmental factors on vector phenology and what changes in parasites’ distribution ranges are expected with climate change.
In this study we model the change in temperature and parasite transmission dynamics in four western Himalayan sites across an elevational gradient. Using fine-scale meteorological data, we explore limits of parasite transmission as a function of temperature in the western Himalayan landscape. Specifically, we ask the following questions:
(i) Is parasite transmission restricted by temperature in high elevation environments?
(ii) Is there spatial and temporal variation in parasite transmission dynamics?
(iii) How will climate change affect the distribution of malaria and the parasite transmission window?