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?