Abstract

Phenological shifts are primary responses of species to recent climate change. Such changes might lead to temporal mismatches in food webs and exacerbate species vulnerability. Yet insights into this phenomenon through experimental approaches are still scarce, especially in amphibians, which are particularly sensitive to changing thermal environments. Here, under controlled warming conditions, we report a critical, but poorly studied, life-cycle stage (i.e., hibernation) in frogs inhabiting subtropical latitudes. Using outdoor mesocosm experiments, we examined the effects of temperature (ambient vs. + ~2.2/2.4 °C of pre-/post-hibernation warming) and food availability (normal vs. 1/3 food) on the date of entrance into/emergence from hibernation in Pelophylax nigromaculatus. We found temperature was the major factor determining the hibernation period, which showed a significant shortening under experimental warming (6–8 days), with delays in autumn and advances in spring. Moreover, the timing of hibernation was not affected by food availability, whereas sex and, particularly, age were key factors in the species’ phenological responses. Specifically, male individuals emerged from hibernation earlier, while older individuals also entered and emerged from hibernation earlier. We believe that this study provides some of the first experimental evidence for the effect of climate warming on the timing of amphibian hibernation.

Highlights

  • Earlier metamorphosis in anuran larvae was reported under artificially warmed and dried environments, which allowed for an independent assessment of the factors involved[10]

  • It is expected that an uncertainty in food availability favors more complex and less predictable responses of amphibians to climate change, such as the ones already observed in amphibian larvae showing differences in defensive strategies and growth patterns under warming conditions[10,29,30], and further synergic processes related to phenological changes might emerge

  • We addressed the following questions: (i) Do frogs shift hibernation phenology when exposed to climate warming at rates consistent with projected climate-change scenarios? (ii) Is pre- and post-hibernation warming leading to similar shifting patterns? (iii) Does food deprivation cause synergic effects on species response to climate warming? and (iv) Do these responses differ across individual traits, such as sex or age? Using meso-scale experimentation with greenhouse units, we were able to test independent and interaction effects under controlled conditions, excluding other factors such as precipitation, population density, competitors, and predation pressure

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Summary

Introduction

Earlier metamorphosis in anuran larvae was reported under artificially warmed and dried environments, which allowed for an independent assessment of the factors involved[10]. We believe that our study is one of the first that experimentally examines the effect of climate warming on the timing of amphibian hibernation. Temperature-induced changes in phenology have led birds and other animals to mismatch peaks of breeding activity and food abundance[26,27,28], which directly impacts their individual fitness and population dynamics. It is expected that an uncertainty in food availability favors more complex and less predictable responses of amphibians to climate change, such as the ones already observed in amphibian larvae showing differences in defensive strategies and growth patterns under warming conditions[10,29,30], and further synergic processes related to phenological changes might emerge. We experimentally examined the effects of temperature and food availability on the hibernation behavior of post-metamorphic black-spotted pond frogs (Pelophylax nigromaculatus) through outdoor mesocosm experiments. We addressed the following questions: (i) Do frogs shift hibernation phenology when exposed to climate warming at rates consistent with projected climate-change scenarios? (ii) Is pre- and post-hibernation warming leading to similar shifting patterns? (iii) Does food deprivation cause synergic effects on species response to climate warming? and (iv) Do these responses differ across individual traits, such as sex or age? Using meso-scale experimentation with greenhouse units, we were able to test independent and interaction effects under controlled conditions, excluding other factors such as precipitation, population density, competitors, and predation pressure

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