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Artificial warming increases size at metamorphosis in plateau frogs (Rana kukunoris) in the presence of predators

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Abstract

Global warming may induce significant changes in species life history traits particularly in amphibians, which are characterized by complex and plastic life cycles. Because both warming and predators are often suggested to reduce size at metamorphosis in amphibians, we hypothesized that the size at metamorphosis was further reduced by experimental warming in the presence of predators. We conducted a factorial-designed experiment involving two factors and two levels (warmed vs. ambient, lethal predator absence vs. presence, resulting in four treatments) using Rana kukunoris tadpoles in the eastern Tibetan Plateau, and we examined its behavioral, growth, and developmental responses to warming in the presence and absence of predatory beetles (Agabus sp.) for 13 weeks. During the course of the experiment, a similar level of tadpole mortality due to the diving beetles was found between ambient and warmed treatments, but the warming effect on size at metamorphosis depended on whether the predators were present or absent. In the absence of predators, warming did not significantly increase tadpole growth but advanced the timing of metamorphosis, such that size at metamorphosis of forelimb emergence and tail resorption was much reduced in terms of body fresh weight. In the presence of predators, warming increased tadpole growth rate much more than the development rate (as reflected by duration of the tadpole stage), and therefore the size at metamorphosis was significantly increased. The significant effect of the interaction between predator and warming on the size at metamorphosis could be attributed to the tadpole response in the frequencies of feeding, resting, and swimming to the predator activity level, which was in turn increased by warming. We suggest that warming-induced changes in life history traits should be studied in relation to species interaction so as to accurately predict ecological response of amphibians to the future warmed world.

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Acknowledgments

We thank Ase Xiaohu for assistance and Lee Frelich for English improvement. This study was supported by National Science Foundation of China (31325004), 973 Program (2013CB956302), and the Ministry of Environmental Protection of China (2011ZX08012-005).

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Authors and Affiliations

  1. Department of Biology, Nanjing University, 22 Hankou Rd, Nanjing, 210093, China

    Jiyan Zhao, Yangheshan Yang & Shucun Sun

  2. ECORES Lab, Chengdu Institute of Biology, Chinese Academy of Sciences, 9 Section 4, Renminnan Rd, Chengdu, 610041, China

    Xinqiang Xi & Shucun Sun

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  1. Jiyan Zhao
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Correspondence to Shucun Sun.

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10452_2014_9495_MOESM1_ESM.doc

Online Resource 1 Variation in daily mean temperature during the experiment period. The closed and open symbols stand for warmed and ambient treatments, respectively. (DOC 105 kb)

10452_2014_9495_MOESM2_ESM.doc

Online Resource 2 Tadpole survival during the course of the experiment. W-P-, ambient control; W+P-, warming; W-P+, ambient and predator present; W+P+, warming and predator present. Data are means± 1SE. The difference was significant (P<0.05) between W-P- and W+P- treatments on days 42 and 49 in the absence of predators, as indicated by results of two-way ANOVAs followed by post hoc Tukey’s tests. (DOC 72 kb)

10452_2014_9495_MOESM3_ESM.doc

Online Resource 3 Body fresh weight (a), body length (b) and tail length (c) of surviving tadpoles in four treatments during the course of the experiment. W-P-, ambient control; W+P-, warming; W-P+, ambient and predator-presence; W+P+, warming and predator-presence. The asterisks denote statistically significant differences (*, P<0.05, **, P<0.01, ***, P<0.001) between warmed and ambient treatments in the presence of predators, as derived from a two-way ANOVA followed by post hoc Tukey’s tests on observation days. Data are means±1SE. (DOC 184 kb)

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Zhao, J., Yang, Y., Xi, X. et al. Artificial warming increases size at metamorphosis in plateau frogs (Rana kukunoris) in the presence of predators. Aquat Ecol 48, 423–434 (2014). https://doi.org/10.1007/s10452-014-9495-y

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