Post-epizootic microbiome associations across communities of neotropical amphibians.

Microbiome-pathogen interactions are increasingly recognized as an important element of host immunity. While these host-level interactions will have consequences for community disease dynamics, the factors which influence host microbiomes at larger scales are poorly understood. We here describe landscape-scale pathogen-microbiome associations within the context of post-epizootic amphibian chytridiomycosis, a disease caused by the panzootic chytrid fungus Batrachochytrium dendrobatidis. We undertook a survey of Neotropical amphibians across altitudinal gradients in Ecuador ~30 years following the observed amphibian declines and collected skin swab-samples which were metabarcoded using both fungal (ITS-2) and bacterial (r16S) amplicons. The data revealed marked variation in patterns of both B. dendrobatidis infection and microbiome structure that are associated with host life history. Stream breeding amphibians were most likely to be infected with B. dendrobatidis. This increased probability of infection was further associated with increased abundance and diversity of non-Batrachochytrium chytrid fungi in the skin and environmental microbiome. We also show that increased alpha diversity and the relative abundance of fungi are lower in the skin microbiome of adult stream amphibians compared to adult pond-breeding amphibians, an association not seen for bacteria. Finally, stream tadpoles exhibit lower proportions of predicted protective microbial taxa than pond tadpoles, suggesting reduced biotic resistance. Our analyses show that host breeding ecology strongly shapes pathogen-microbiome associations at a landscape scale, a trait that may influence resilience in the face of emerging infectious diseases.

Predators like it hot: Thermal mismatch in a predator-prey system across an elevational tropical gradient.

Climate change may have dramatic consequences for communities through both direct effects of peak temperatures upon individual species and through interspecific mismatches in thermal sensitivities of interacting organisms which mediate changes in interspecific interactions (i.e. predation). Despite this, there is a paucity of information on the patterns of spatial physiological sensitivity of interacting species (at both landscape and local scales) which could ultimately influence geographical variation in the effects of climate change on community processes. In order to assess where these impacts may occur, we first need to evaluate the spatial heterogeneity in the degree of mismatch in thermal tolerances between interacting organisms. We quantify the magnitude of interspecific mismatch in maximum (CTmax ) and minimum (CTmin ) thermal tolerances among a predator-prey system of dragonfly and anuran larvae in tropical montane (242-3,631 m) and habitat (ponds and streams) gradients. To compare thermal mismatches between predator and prey, we coined the parameters maximum and minimum predatory tolerance margins (PTMmax and PTMmin ), or difference in CTmax and CTmin of interacting organisms sampled across elevational and habitat gradients. Our analyses revealed that: (a) predators exhibit higher heat tolerances than prey (~4°C), a trend which remained stable across habitats and elevations. In contrast, we found no differences in minimum thermal tolerances between these groups. (b) Maximum and minimum thermal tolerances of both predators and prey decreased with elevation, but only maximum thermal tolerance varied across habitats, with pond species exhibiting higher heat tolerance than stream species. (c) Pond-dwelling organisms from low elevations (0-1,500 m a.s.l.) may be more susceptible to direct effects of warming than their highland counterparts because their maximum thermal tolerances are only slightly higher than their exposed maximum environmental temperatures. The greater relative thermal tolerance of dragonfly naiad predators may further increase the vulnerability of lowland tadpoles to warming due to potentially enhanced indirect effects of higher predation rates by more heat-tolerant dragonfly predators. However, further experimental work is required to establish the individual and population-level consequences of this thermal tolerance mismatch upon biotic interactions such as predator-prey. ​.

El cambio climático puede acarrear consecuencias dramáticas en las comunidades, ya sea mediante los efectos directos de las temperaturas extremas sobre cada especie particular, o por los efectos indirectos en las interacciones entre especies (p.ej. depredación). Sin embargo, no existe actualmente información a escala local o regional sobre los patrones geográficos de la sensibilidad térmica de especies que interaccionan, que en última instancia puede afectar a los procesos de las comunidades. Es por ello que para estimar dónde se van a producir los impactos del calentamiento, necesitamos primero tener un conocimiento de los niveles de desajustes espaciales que puedan presentar las interacciones biológicas. En este estudio hemos cuantificado los desajustes interespecíficos en las tolerancias térmicas extremas al calor (CTmax ) y al frío (CTmin ) en un sistema de depredador-presa, de larvas de libélulas y anfibios, en un gradientes de altitud tropical (242-3,631 m) y entre hábitats (charcas y arroyos). Para comparar los desajustes entre depredador y presa, definimos dos parámetros: margen máximo y mínimo de tolerancia a la depredación (PTMmax y PTMmin ) que se definiría como la diferencia respectiva entre CTmax y CTmin entre los organimos que interaccionan. Nuestros resultados muestran: (1) los depredadores muestran mayor tolerancia al calor que las presas (~4°C), diferencia que se mantiene invariable entre hábitats y altitudes. Por el contrario, no encontramos diferencias en las tolerancias térmicas mínimas entre estos grupos. (2) Las tolerancias térmicas máximas y mínimas, tanto en depredadores como en presas, disminuyen con la elevación pero sólo la tolerancia al calor varía entre hábitats, siendo más resistentes las especies de charcas frente a las de arroyos. (3) Las especies que habitan charcas de baja altitud (0-1,500 m) son más susceptibles a recibir impactos directos del calentamiento que las de alta montaña, ya que sus tolerancias térmicas máximas son sólo ligeramente superiores a las temperaturas extremas que se registran en la actualidad. La mayor tolerancia térmica relativa que presentan las larvas depredadoras de libélulas, puede incrementar la vulnerabilidad al calentamiento de los renacuajos de baja altitud, por los efectos indirectos que pueden infringir sobre ellos las libélulas depredadoras, más tolerantes al calor. Sin embargo, es necesario realizar más investigaciones experimentales, para establecer las consecuencias individuales y poblacionales de este desajuste en las tolerancias térmicas en las interacciones bióticas, como las de depredador-presa. ​.

Ontogenetic reduction in thermal tolerance is not alleviated by earlier developmental acclimation in Rana temporaria.

Complex life-histories may promote the evolution of different strategies to allow optimal matching to the environmental conditions that organisms can encounter in contrasting environments. For ectothermic animals, we need to disentangle the role of stage-specific thermal tolerances and developmental acclimation to predict the effects of climate change on spatial distributions. However, the interplay between these mechanisms has been poorly explored. Here we study whether developmental larval acclimation to rearing temperatures affects the thermal tolerance of subsequent terrestrial stages (metamorphs and juveniles) in common frogs (Rana temporaria). Our results show that larval acclimation to warm temperatures enhances larval heat tolerance, but not thermal tolerance in later metamorphic and juvenile stages, which does not support the developmental acclimation hypothesis. Further, metamorphic and juvenile individuals exhibit a decline in thermal tolerance, which would confer higher sensitivity to extreme temperatures. Because thermal tolerance is not enhanced by larval developmental acclimation, these 'risky' stages may be forced to compensate through behavioural thermoregulation and short-term acclimation to face eventual heat peaks in the coming decades.

Phenology and plasticity can prevent adaptive clines in thermal tolerance across temperate mountains: The importance of the elevation-time axis.

Critical thermal limits (CTmax and CTmin) decrease with elevation, with greater change in CTmin, and the risk to suffer heat and cold stress increasing at the gradient ends. A central prediction is that populations will adapt to the prevailing climatic conditions. Yet, reliable support for such expectation is scant because of the complexity of integrating phenotypic, molecular divergence and organism exposure. We examined intraspecific variation of CTmax and CTmin, neutral variation for 11 microsatellite loci, and micro- and macro-temperatures in larvae from 11 populations of the Galician common frog (Rana parvipalmata) across an elevational gradient, to assess (1) the existence of local adaptation through a PST-FST comparison, (2) the acclimation scope in both thermal limits, and (3) the vulnerability to suffer acute heat and cold thermal stress, measured at both macro- and microclimatic scales. Our study revealed significant microgeographic variation in CTmax and CTmin, and unexpected elevation gradients in pond temperatures. However, variation in CTmax and CTmin could not be attributed to selection because critical thermal limits were not correlated to elevation or temperatures. Differences in breeding phenology among populations resulted in exposure to higher and more variable temperatures at mid and high elevations. Accordingly, mid- and high-elevation populations had higher CTmax and CTmin plasticities than lowland populations, but not more extreme CTmax and CTmin. Thus, our results support the prediction that plasticity and phenological shifts may hinder local adaptation, promoting thermal niche conservatism. This may simply be a consequence of a coupled variation of reproductive timing with elevation (the "elevation-time axis" for temperature variation). Mid and high mountain populations of R. parvipalmata are more vulnerable to heat and cool impacts than lowland populations during the aquatic phase. All of this contradicts some of the existing predictions on adaptive thermal clines and vulnerability to climate change in elevational gradients.