Discussion
We analyzed a wide range of species and environmental reservoirs across
different seasons to evaluate the infection patterns of Bsal in
relation to geographic and environmental factors in Guangxi region. We
did not detect Bsal in any of the samples from wild and captive
animals or sampled water bodies. Our species distribution model
estimated a small fraction of suitable habitats in this region under the
current climatic conditions, but with patchy distributions. These
results suggest that climate is a potential barrier, limitingBsal spread into the surveyed sites. However, there is a
possibility that it could be present at undetectable levels, or occur in
specific microhabitats that were not sampled in our study.
Our niche model predicted that climatically suitable areas forBsal in the Guangxi region are less and fragmented, generally low
suitability. The model identified mean diurnal range as the most crucial
variable in our models. This corroborates the findings from previousBsal distribution models in its native Asian range (Moubarak et
al., 2022). The relatively high variations in mean diurnal range within
the study area seem to limit the potential distribution of Bsal ,
emphasizing that environmental temperature is a primary factor
influencing Bsal occurrences (Martel et al., 2013).
Bsal prefer lower thermal conditions for their existence, the
temperatures above 22°C
adversely
affects its growth and diminish its pathogenicity to hosts (Carter et
al., 2021; Martel et al., 2013). Previous studies have proposed that
temperature is a key factor behind the low prevalence of Bsal in
Asian amphibians, as the environmental as well as the water temperatures
in these regions are generally considered suboptimal (≥ 15°C) forBsal ’s survival and growth (Laking et al., 2017; Martel et al.,
2013; Yuan et al., 2018). It has also been documented that warmer
temperatures can potentially reduce intraspecific transmission rates,
especially when temperatures surpass 25°C (Blooi et al., 2015) .
Furthermore,
the
precipitation of the coldest quarter plays a contributory role in
modeling predictions for Bsal occurrences in Asia which shows the
same pattern as of European Bsal presence which requires moist,
relatively cool and stable conditions (Beukema et al., 2021), the high
fluctuations of precipitation in cool periods weaken its occurrences.
The absence of Bsal in northern sites in our study might partly
result from competition with other pathogens that share a similar
climatic niche, such as Bd . It was identified at ten of the
surveyed sites (Fig. 1B), displaying a high prevalence in the northern
locales of the Guangxi region (Sun et al., 2023). One of 38 species we
examined, A. davidianus (positive to Bd in our subsequent
detections), have been reported as Bsal -positive species (Fig.1;
Laking et al., 2017; Yuan et al., 2018), but it was negative toBsal infection in our present study. These patterns suggest that
Asian Bd lineages might outcompete Bsal when site-specific
conditions and species susceptibility enhance the pathogenic performance
of Bd lineages as pathogenicity of both pathogens varies with
species and environmental conditions (Fisher & Garner, 2020; Martel et
al., 2014). This competition could occur because Bd infection can
negatively impact Bsal infection under certain circumstances
(Direnzo et al., 2021).
Considering the possibility that Bsal has not yet been
transmitted to the current sampling sites, particularly in highly
suitable habitats (e.g., southwestern sites) where Bd is present
(Fig. 1), the coexistence of Bd and Bsal in the same
microhabitats could result in severe coinfections or reinfections and
potentially generate new, highly virulent genotypes within the same host
once the pathogen is introduced to these sites (Greenspan et al., 2018).
Among the 38 amphibian species tested for Bsal , none were found
to be infected. However, 16 of these species tested positive forBd infection (Table 1), highlighting the need for further
investigation into the potential co-occurrence of these fungal
pathogens. Specifically, we recommend investigating predicted suitable
areas for Bsal where Bd is present, in order to better
understand the ecological interactions between these pathogens and their
impact on amphibian species.
Geographic barriers such as drier plains which prevents the migration of
susceptible species could be another potential reasons for absence ofBsal (restricted slowly dispersal) in the region. This may
inhibit the host-dependent intraspecific and interspecific as well as
human-mediated transmissions of this pathogen within landscapes (Malagon
et al., 2020; Spitzen-Van Der Sluijs et al., 2018; Tompros et al.,
2021). In addition, the negative result of Bsal is consistent
with previous studies of this pathogen in Asia that primarily detected
the fungus in anuran species (Wang et al. 2017; Zhu et al. 2014), which
was thought to lead to transient persistence for Bsal and
decreased transmission rates due to low galactose proportions in host
skin (Stegen et al., 2017; Wang et al., 2021). However, it is possible
that Bsal could be present sub clinically at low prevalence in
these studied amphibians, with fungal loads below the thresholds of
detection. As growth of Bsal could also depend on relevant plant
materials in water (Kelly et al., 2021), extending the range of sampling
efforts in environmental reservoirs can improve our understanding the
existence of Bsal in the region.
Seasonality mainly explained by variations in temperature and
precipitation, may influence Bsal occurrences and host
susceptibility (Bozzuto & Canessa, 2019; Carter et al., 2021). Our
study primarily surveyed amphibians that are reproductively active
during spring and summer, with a limited number of individuals sampled
in autumn. We were unable to conduct any sampling of wild host species
during winter, which limits our understanding of Bsal infection
across seasons. Notably, autumn and winter conditions in this
subtropical region might be more conducive for Bsal prevalence.
It is important to understand the resource partitioning and natural
behaviors of amphibians across seasons. One such factor would be
overwintering and potential attenuation of defensive mechanisms such as
reduced skin bacterial diversity during hibernation (Tong et al., 2019).
This would lead the pathogen to cause sub-lethal infections in
susceptible amphibians during autumn and winter. Hence, we recommend
integrating experimental and field studies in both summer and winter, to
enhance our understanding of the effects of Bsal infection on
amphibians in specific ecological contexts.
In conclusion, the absence of Bsal in our study should not
undermine the importance of proactive management and conservation
strategies aimed at minimizing the risk of Bsal transmission in
the region. This is due to the limited presence of climatically suitable
areas for Bsal in this region and the isolated suitable sites
within mountains could provide an important refuge for Bsal(Beukema et al., 2021; Lötters et al., 2020). Implementing stringent
biosecurity measures, such as regulating the trade of amphibians can
help reduce the chances of pathogen introduction. Regular monitoring and
surveillance programs are crucial for early detection of Bsal ,
which could allow for timely interventions to prevent severe declines in
amphibian populations (Thomas et al., 2019). In addition, further
research into the ecology, transmission dynamics, and host-pathogen
interactions of Bsal is essential to generate knowledge that will
inform targeted conservation.