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unpublished data).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.