Localized carry-over effects of pond drying on survival, growth, and pathogen defenses in amphibians

Climate change is increasing variability in precipitation patterns in many
parts of the globe. Unpredictable changes in water availability can be
particularly challenging for organisms that rely on precipitation-fed
water sources for completing their life cycle, such as many amphibian
species. Although developmental plasticity can mitigate the impacts of
changing environments for some species, this strategy can come at a cost
to other fitness-linked traits, such as immune function. We investigated
localized variation in the capacity to respond to pond drying and
evaluated whether developmental responses induced carry-over effects in
disease susceptibility in three leopard frog species
(Rana [Lithobates] pipiens and R.
sphenocephala; two populations each, and one population of R.
chiricahuensis). Using mesocosms located near the site of collection
(<15 km away) in five regions spanning a latitudinal gradient, we
raised tadpoles under simulated fast-drying, slow-drying, or constant
water levels. After metamorphosis, we characterized several aspects of the
skin microbiome, immune function, and response to exposure to the fungal
pathogen Batrachochytrium dendrobatidis (Bd). Note that
for R. chiricahuensis, the only carry-over effect
measured was response to Bd exposure, for which we
observed no effects of pond drying. We found that developmental plasticity
in response to drying was rare, except in the southernmost population
of R. sphenocephala. In this location, tadpoles responded by
accelerating development, and frogs with shorter larval periods developed
more severe infections
following Bd exposure post-metamorphosis,
suggesting a trade-off between surviving pond drying and pathogen defense
investment. In the three other locations, a lack of accelerated
metamorphosis in drying treatments was accompanied by increased mortality,
decreased anti-Bd function of the microbiome, and/or
greater Bd infection after exposure. Overall, results
suggest that faster drying conditions will likely have negative impacts on
amphibians with long larval periods, both directly and indirectly via
carry-over effects. Because effects of drying exposure were not uniform
within a species, our findings suggest local responses may not be
generalizable to other regions of the range. These multifaceted effects of
climate change on pathogen defenses are increasingly relevant as emerging
infectious diseases threaten global biodiversity.