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Open Access Research article

Daily temperature fluctuations unpredictably influence developmental rate and morphology at a critical early larval stage in a frog

Juliana M Arrighi12, Ezra S Lencer13, Advait Jukar14, Daesik Park5, Patrick C Phillips6 and Robert H Kaplan1*

Author Affiliations

1 Department of Biology, Reed College, 3203 SE Woodstock Blvd, Portland, OR 97202, USA

2 Systems Science, Portland State University, Portland, OR, USA

3 Ecology and Evolutionary Biology, Cornell University, Ithaca, NY, USA

4 Environmental Science and Policy, George Mason University, Fairfax, VA, USA

5 Division of Science Education, Kangwon National University, Chuncheon, Kangwon, 200-701, South Korea

6 Institute of Ecology and Evolution, University of Oregon, Eugene, OR, 97403, USA

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BMC Ecology 2013, 13:18  doi:10.1186/1472-6785-13-18

Published: 4 May 2013

Abstract

Background

Environmental temperature has profound consequences for early amphibian development and many field and laboratory studies have examined this. Most laboratory studies that have characterized the influence of temperature on development in amphibians have failed to incorporate the realities of diel temperature fluctuations (DTF), which can be considerable for pond-breeding amphibians.

Results

We evaluated the effects of different ecologically relevant ranges of DTF compared with effects of constant temperatures on development of embryos and larvae of the Korean fire-bellied toad (Bombina orientalis). We constructed thermal reaction norms for developmental stage, snout- vent length, and tail length by fitting a Gompertz-Gaussian function to measurements taken from embryos after 66 hours of development in 12 different constant temperature environments between 14°C and 36°C. We used these reaction norms as null models to test the hypothesis that developmental effects of DTF are more than the sum of average constant temperature effects over the distribution of temperatures experienced. We predicted from these models that growth and differentiation would be positively correlated with average temperature at low levels of DTF but not at higher levels of DTF. We tested our prediction in the laboratory by rearing B. orientalis embryos at three average temperatures (20°C, 24°C, and 28°C) and four levels of thermal variation (0°C, 6°C, 13°C, and 20°C). Several of the observed responses to DTF were significantly different from both predictions of the model and from responses in constant temperature treatments at the same average temperatures. At an average temperature of 24°C, only the highest level of DTF affected differentiation and growth rates, but at both cooler and warmer average temperatures, moderate DTF was enough to slow developmental and tail growth rates.

Conclusions

These results demonstrate that both the magnitude of DTF range and thermal averages need to be considered simultaneously when parsing the effects of changing thermal environments on complex developmental responses, particularly when they have potential functional and adaptive significance.

Keywords:
Bombina orientalis; Amphibian; Diel temperature fluctuation (DTF); Developmental plasticity; Thermal performance curve; Reaction norm