ABSTRACT Environmental challenges early in development can result in complex phenotypic trade-offs and long-term effects on individual physiology, performance and behavior, with implications for disease and predation risk. We examined the effects of simulated pond drying and elevated water temperatures on development, growth, thermal physiology and behavior in a North American amphibian, Rana sphenocephala. Tadpoles were raised in outdoor mesocosms under warming and drying regimes based on projected climatic conditions in 2070. We predicted that amphibians experiencing the rapid pond drying and elevated pond temperatures associated with climate change would accelerate development, be smaller at metamorphosis and demonstrate long-term differences in physiology and exploratory behavior post-metamorphosis. Although both drying and warming accelerated development and reduced survival to metamorphosis, only drying resulted in smaller animals at metamorphosis. Around 1 month post-metamorphosis, animals from the control treatment jumped relatively farther at high temperatures in jumping trials. In addition, across all treatments, frogs with shorter larval periods had lower critical thermal minima and maxima. We also found that developing under warming and drying resulted in a less exploratory behavioral phenotype, and that drying resulted in higher selected temperatures in a thermal gradient. Furthermore, behavior predicted thermal preference, with less exploratory animals selecting higher temperatures. Our results underscore the multi-faceted effects of early developmental environments on behavioral and physiological phenotypes later in life. Thermal preference can influence disease risk through behavioral thermoregulation, and exploratory behavior may increase risk of predation or pathogen encounter. Thus, climatic stressors during development may mediate amphibian exposure and susceptibility to predators and pathogens into later life stages.
more »
« less
This content will become publicly available on February 1, 2026
Post‐metamorphic growth partially compensates for the effects of climate‐driven stressors on juvenile frog performance
Abstract Human‐induced climate change, land use changes, and urbanization are predicted to dramatically impact landscape hydrology, which can have devastating impacts on aquatic organisms. For amphibians that rely on aquatic environments to breed and develop, it is essential to understand how the larval environment impacts development, condition, and performance later in life. Two important predicted impacts of climate change, urbanization, and land use changes are reduced hydroperiod and variable larval density. Here, we explored how larval density and hydroperiod affect development, morphology, physiology, and immune defenses at metamorphosis and 35 days post‐metamorphosis in the frogRana pipiens. We found that high‐density larval conditions had a large negative impact on development and morphology, which resulted in longer larval periods, reduced likelihood of metamorphosis, smaller size at metamorphosis, shorter femur to body length ratio, and reduced microbiome species evenness compared with animals that developed in low‐density conditions. However, animals from the high‐density treatment experienced compensatory growth post‐metamorphosis, demonstrating accelerated growth in body size and relative femur length compared with animals from the low‐density treatments, despite not “catching‐up” in size. We also observed an increase in relative gut length and relative liver size in animals that had developed in the high‐density treatment than those in the low‐density treatment, as well as higher bacterial killing ability, and greater jump distances relative to their leg length across different temperatures. Finally, metabolic rate was higher overall but especially at higher test temperatures for animals that developed under high‐density conditions, indicating that these animals may expend more energy in response to acute temperature changes. While the effects of climate change have direct negative effects on larval development and metamorphosis, animals can increase growth rate post‐metamorphosis; however, that compensatory growth might come at a cost and reduce their ability to cope with further environmental change such as increased temperatures.
more »
« less
- Award ID(s):
- 2120084
- PAR ID:
- 10594487
- Publisher / Repository:
- ESA
- Date Published:
- Journal Name:
- Ecosphere
- Volume:
- 16
- Issue:
- 2
- ISSN:
- 2150-8925
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Development can play a critical role in how organisms respond to changes in the environment. Tolerance to environmental challenges can vary during ontogeny, with individual- and population-level impacts that are associated with the timing of exposure relative to the timing of vulnerability. In addition, the life history consequences of different stressors can vary with the timing of exposure to stress. Salinization of freshwater ecosystems is an emerging environmental concern, and habitat salinity can change rapidly due, for example, to storm surge, runoff of road deicing salts, and rainfall. Elevated salinity can increase the demands of osmoregulation in freshwater organisms, and amphibians are particularly at risk due to their permeable skin and, in many species, semi-aquatic life cycle. In three experiments, we manipulated timing and duration of exposure to elevated salinity during larval development of southern toad (Anaxyrus terrestris) tadpoles and examined effects on survival, larval growth, and timing of and size at metamorphosis. Survival was reduced only for tadpoles exposed to elevated salinity early in development, suggesting an increase in tolerance as development proceeds; however, we found no evidence of acclimation to elevated salinity. Two forms of developmental plasticity may help to ameliorate costs of transient salinity exposure. With early salinity exposure, the return to freshwater was accompanied by a period of rapid compensatory growth, and metamorphosis ultimately occurred at a similar age and size as freshwater controls. By contrast, salinity exposure later in development led to earlier metamorphosis at reduced size, indicating an acceleration of metamorphosis as a mechanism to escape salinity stress. Thus, the consequences of transient salinity exposure were complex and were mediated by developmental state. Salinity stress experienced early in development resulted in acute costs but little long-lasting effect on survivors, while exposures later in development resulted in sublethal effects that could influence success in subsequent life stages. Overall, our results suggest that elevated salinity is more likely to affect southern toad larvae when experienced early during larval development, but even brief sublethal exposure later in development can alter life history in ways that may impact fitness.more » « less
-
<ext-link href='http://Abstract'>Abstract</ext-link> Global climate change is expected to both increase average temperatures as well as temperature variability.Increased average temperatures have led to earlier breeding in many spring‐breeding organisms. However, individuals breeding earlier will also face increased temperature fluctuations, including exposure to potentially harmful cold‐temperature regimes during early developmental stages.Using a model spring‐breeding amphibian, we investigated how embryonic exposure to different cold‐temperature regimes (control, cold‐pulse, and cold‐press) affected (a) compensatory larval development and growth, (b) larval susceptibility to a common contaminant, and (c) larval susceptibility to parasites.We found: (a) no evidence of compensatory development or growth, (b) larvae exposed to the cold‐press treatment were more susceptible to NaCl at 4‐days post‐hatching but recovered by 17‐days post‐hatching, and (c) larvae exposed to both cold treatments were less susceptible to parasites.These results demonstrate that variation in cold‐temperature regimes can lead to unique direct and indirect effects on larval growth, development, and response to stressors. This underscores the importance of considering cold‐temperature variability and not just increased average temperatures when examining the impacts of climate disruption.more » « less
-
Many anuran amphibians (frogs and toads) rely on aquatic habitats during their larval stage. The quality of this environment can significantly impact lifetime fitness and population dynamics. Over 450 studies have been published on environmental impacts on anuran developmental plasticity, yet we lack a synthesis of these effects across different environments. We conducted a meta-analysis and used a comparative approach to understand whether developmental plasticity in response to different larval environments produces predictable changes in metamorphic phenotypes. We analyzed data from 124 studies spanning 80 anuran species and six larval environments and showed that intraspecific variation in mass at metamorphosis and the duration of the larval period is partly explained by the type of environment experienced during the larval period. Changes in larval environments tended to reduce mass at metamorphosis relative to control conditions, with the degree of change depending on the identity and severity of environmental change. Higher temperatures and lower water levels shortened the duration of the larval period, whereas less food and higher densities increased the duration of the larval period. Phylogenetic relationships among species were not associated with interspecific variation in mass at metamorphosis plasticity or duration of the larval period plasticity. Our results provide a foundation for future studies on developmental plasticity, especially in response to global changes. This study provides motivation for additional work that links developmental plasticity with fitness consequences within and across life stages, as well as how the outcomes described here are altered in compounding environments.more » « less
-
ABSTRACT Many songbirds begin active incubation after laying their penultimate egg, resulting in synchronous hatching of the clutch except for a last‐hatched individual (“runt”) that hatches with a size deficit and competitive disadvantage to siblings when begging for food. However, climate change may elevate temperatures and cause environmental incubation as eggs are laid, resulting in asynchronous hatching and larger size hierarchies among siblings. Although previous work demonstrated that asynchronous hatching reduces nestling growth and survival relative to synchrony, the physiological mechanisms underlying these effects are unclear. To test the effects of asynchronous hatching on runt growth, survival, physiology, and compensatory growth‐related tradeoffs, we manipulated incubation temperature in nest boxes of European starlings (Sturnus vulgaris) to increase asynchronous hatching and collected nestling morphological measurements and blood samples to assess physiology and development. Independent of heating treatment, runts from asynchronously hatched nests had lower survival than runts from more synchronous nests. Surviving runts from asynchronous nests were smaller and had reduced stress‐induced corticosterone concentrations and reduced circulating glucose compared with runts from synchronous nests. Despite persistent size and energy deficits, runts from asynchronous nests did not have significant deficits in immunity or telomere length when compared with runts from synchronous nests, suggesting no trade‐off between investment in immune development or telomere maintenance with growth. Overall, these results suggest that increased asynchrony due to climate change could reduce clutch survival for altricial songbirds, especially for the smallest chicks in a clutch, and that the negative effects of asynchrony may be driven by persistent energetic deficits.more » « less
An official website of the United States government
