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The energy cost of embryonic development in fishes and amphibians, with emphasis on new data from the Australian lungfish, Neoceratodus forsteri

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Abstract

The rate of oxygen consumption throughout embryonic development is used to indirectly determine the ‘cost’ of development, which includes both differentiation and growth. This cost is affected by temperature and the duration of incubation in anamniote fish and amphibian embryos. The influences of temperature on embryonic development rate, respiration rate and energetics were investigated in the Australian lungfish, Neoceratodus forsteri, and compared with published data. Developmental stage and oxygen consumption rate were measured until hatching, upon which wet and dry gut-free masses were determined. A measure of the cost of development, the total oxygen required to produce 1 mg of embryonic dry tissue, increased as temperature decreased. The relationship between the oxygen cost of development (C, ml mg−1) and dry hatchling mass (M, mg) in fishes and amphibians is described by C = 0.30 M0.22 ± 0.13 (95% CI), r 2 = 0.52. The scaling exponent indicates that the cost of embryonic development increases disproportionally with increasing hatchling mass. At 15 and 20°C, N. forsteri cost of development is significantly lower than the regression mean for all species, and at 25°C is lower than the allometrically scaled data set. Unexpectedly, incubation of N. forsteri is long, despite natural development under relatively warm conditions, and may be related to a large genome size. The low cost of development may be associated with construction of a rather sluggish fish with a low capacity for aerobic metabolism. The metabolic rate is lower in N. forsteri hatchlings than in any other fishes or amphibians at the same temperature, which matches the extremely low aerobic metabolic scope of the juveniles.

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Acknowledgments

We thank Rolf Ericsson from the Australian lungfish laboratory, Macquarie University for his expertise and provision of eggs and two anonymous reviewers for helpful comments on the manuscript. We acknowledge funding from the University of Adelaide and the Australian Geographic Society.

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Authors and Affiliations

  1. Ecology and Evolutionary Biology, University of Adelaide, Adelaide, SA, 5005, Australia

    Casey A. Mueller & Roger S. Seymour

  2. Biological Sciences, Macquarie University, Sydney, NSW, 2109, Australia

    Jean M. P. Joss

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  1. Casey A. Mueller
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Correspondence to Casey A. Mueller.

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Communicated by I. D. Hume.

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Mueller, C.A., Joss, J.M.P. & Seymour, R.S. The energy cost of embryonic development in fishes and amphibians, with emphasis on new data from the Australian lungfish, Neoceratodus forsteri . J Comp Physiol B 181, 43–52 (2011). https://doi.org/10.1007/s00360-010-0501-y

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