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.
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Consequences of life history switch point plasticity for juvenile morphology and locomotion in the Túngara frog
Many animals with complex life cycles can cope with environmental uncertainty by altering the timing of life history switch points through plasticity. Pond hydroperiod has important consequences for the fitness of aquatic organisms and many taxa alter the timing of life history switch points in response to habitat desiccation. For example, larval amphibians can metamorphose early to escape drying ponds. Such plasticity may induce variation in size and morphology of juveniles which can result in carry-over effects on jumping performance. To investigate the carry-over effects of metamorphic plasticity to pond drying, we studied the Túngara frog,
- NSF-PAR ID:
- 10012762
- Publisher / Repository:
- PeerJ
- Date Published:
- Journal Name:
- PeerJ
- Volume:
- 3
- ISSN:
- 2167-8359
- Page Range / eLocation ID:
- e1268
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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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
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Abstract The many and varied effects of human‐induced environmental change have the potential to threaten animal biodiversity and species abundance. Importantly, human land use and global climate change are predicted to reduce water availability, which might have negative consequences for freshwater organisms.
In this study, we tested for an effect of a shortened hydroperiod on larval growth and development, and post‐metamorphic survival and immune function in a temperate frog,
Rana pipiens .Animals developing under pond drying conditions metamorphosed at a smaller size and had lower survival after metamorphosis. We found sex‐specific differences in larval period in our fastest drying treatment, with males metamorphosing more quickly than females. Individuals that developed under drying conditions also showed reduced skin swelling after phytohaemagglutinin injection, indicating a compromised immune response. We found support for trade‐offs between growth, development and post‐metamorphic immune function across hydroperiod treatments. Whole blood from animals with shorter larval periods had lower bacterial killing ability, and small‐bodied juveniles had lower antibody titres.
Overall, our results indicate that a shortened hydroperiod can affect the rate of larval amphibian growth and development, and might negatively impact the condition of species that rely on freshwater for development. Our work improves understanding of the complex impacts that environmental stressors might have on the health of animal populations.
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Plain Language Summary can be found within the Supporting Information of this article. -
On a changing planet, amphibians must respond to weather events shifting in frequency and magnitude, and to how those temperature and precipitation changes interact with other anthropogenic disturbances that modify amphibian habitat. To understand how drastic changes in environmental conditions affect wood frog tadpoles, we tested five temperature manipulations, including Ambient (water temperatures tracking daily air temperatures), Elevated (+ 3 °C above ambient), Nightly (removal of nightly lows), Spike (+ 6 °C above ambient every third week), and Flux (alternating ambient and + 3 °C weekly) crossed with Low Salt (specific conductivity: 109–207 μS-cm) and High Salt (1900–2000 μS-cm). We replicated each of the ten resulting treatments four times. High-salinity conditions produced larger metamorphs than low-salinity conditions. Tadpole survival was reduced only by the Spike treatment (P = 0.017). Elevated temperatures did not shorten larval periods; time to metamorphosis did not differ among temperature treatments (P = 0.328). We retained 135 recently metamorphosed frogs in outdoor terrestrial enclosures for 10 months to investigate larval environment carryover effects. Juvenile frogs grew larger in low-density terrestrial enclosures than high density (P = 0.015) and frogs from Ambient Low Salt larval conditions grew and survived better than frogs from manipulated larval conditions. Frogs from High Salt larval conditions had lower survival than frogs from Low Salt conditions. Our results suggest that anthropogenic disturbances to larval environmental conditions can affect both larval and post-metamorphic individuals, with detrimental carryover effects of high-salinity larval conditions not emerging until the juvenile life stage.more » « less
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