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
Developmental environment has lasting effects on amphibian post-metamorphic behavior and thermal physiology
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
- Award ID(s):
- 2120084
- PAR ID:
- 10419680
- Date Published:
- Journal Name:
- Journal of Experimental Biology
- Volume:
- 226
- Issue:
- 9
- ISSN:
- 0022-0949
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
The immune equilibrium model suggests that exposure to microbes during early life primes immune responses for pathogen exposure later in life. While recent studies using a range of gnotobiotic (germ-free) model organisms offer support for this theory, we currently lack a tractable model system for investigating the influence of the microbiome on immune system development. Here, we used an amphibian species ( Xenopus laevis ) to investigate the importance of the microbiome in larval development and susceptibility to infectious disease later in life. We found that experimental reductions of the microbiome during embryonic and larval stages effectively reduced microbial richness, diversity and altered community composition in tadpoles prior to metamorphosis. In addition, our antimicrobial treatments resulted in few negative effects on larval development, body condition, or survival to metamorphosis. However, contrary to our predictions, our antimicrobial treatments did not alter susceptibility to the lethal fungal pathogen Batrachochytrium dendrobatidis ( Bd ) in the adult life stage. While our treatments to reduce the microbiome during early development did not play a critical role in determining susceptibility to disease caused by Bd in X. laevis , they nevertheless indicate that developing a gnotobiotic amphibian model system may be highly useful for future immunological investigations. This article is part of the theme issue ‘Amphibian immunity: stress, disease and ecoimmunology’.more » « less
-
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
-
While both daytime and nighttime temperatures are increasing with climate change, few studies have experimentally investigated their differential effects under field conditions. We conducted a factorial field experiment examining how day‐ and night‐warming impact the growth, survivorship, and behavior of cabbage white caterpillars (Pieris rapae). In this experiment, the night‐warming only treatment showed the highest rates of caterpillar growth, but also showed the highest mortality, the shortest maximum caterpillar lengths, the least accumulated herbivory, and reduced pupation. Caterpillars in the treatments that were not warmed during the day showed daytime‐shifted growth, and caterpillars in the combined day‐ and night‐warming treatment showed strongly night‐shifted herbivory. Both biotic (e.g., predation risk) and abiotic (e.g., thermal) factors could have contributed to these results. Broadly, these results show the importance of temperature‐mediated behavioral changes in diel activity for caterpillar development and survival. These results also support the emerging hypotheses that periods of reduced activity may be important for successful development, that warmer nighttime conditions could limit a temporal thermal refuge for caterpillars, and that increasing temperatures could increase the likelihood of metabolic meltdown. This experiment also illustrates the value of field studies to provide insights into how ectotherms might respond to ongoing climate change.more » « less
-
While both daytime and nighttime temperatures are increasing with climate change, few studies have experimentally investigated their differential effects under field conditions. We conducted a factorial field experiment examining how day- and night-warming impact the growth, survivorship, and behavior of cabbage white caterpillars (Pieris rapae). In this experiment, the night-warming only treatment showed the highest rates of caterpillar growth, but also showed the highest mortality, the shortest maximum caterpillar lengths, the least accumulated herbivory and reduced pupation. Caterpillars in the treatments that were not warmed during the day showed daytime-shifted growth, and caterpillars in the combined day- and night-warming treatment showed strongly night-shifted herbivory. Both biotic (e.g., predation risk) and abiotic (e.g., thermal) factors could have contributed to these results. Broadly, these results show the importance of temperature-mediated behavioral changes in diel activity for caterpillar development and survival. These results also support the emerging hypotheses that periods of reduced activity may be important for successful development, that warmer nighttime conditions could limit a temporal thermal refuge for caterpillars, and that increasing temperatures could increase the likelihood of metabolic meltdown. By documenting organismal responses in the context of more complex microclimates and communities, this experiment also illustrates the value of field studies to provide insights into how ectotherms might respond to ongoing climate change.more » « less
An official website of the United States government

