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Dietary protein restriction impairs growth, immunity, and disease resistance in southern leopard frog tadpoles

  • Physiological ecology - Original Paper
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Abstract

The immune system is a necessary, but potentially costly, defense against infectious diseases. When nutrition is limited, immune activity may consume a significant amount of an organism’s energy budget. Levels of dietary protein affect immune system function; high levels can enhance disease resistance. We exposed southern leopard frog [Lithobates sphenocephalus (=Rana sphenocephala)] tadpoles to high and low protein diets crossed with the presence or absence of the pathogenic amphibian chytrid fungus (Batrachochytrium dendrobatidis; Bd) and quantified: (1) tadpole resistance to Bd; (2) tadpole skin-swelling in response to phytohaemagglutinin (PHA) injection (a measure of the T cell-mediated response of the immune system); (3) bacterial killing ability (BKA) of tadpole blood (a measure of the complement-mediated cytotoxicity of the innate immune system); and (4) tadpole growth and development. Tadpoles raised on a low-protein diet were smaller and less developed than tadpoles on a high-protein diet. When controlled for developmental stage, tadpoles raised on a low-protein diet had reduced PHA and BKA responses relative to tadpoles on a high-protein diet, but these immune responses were independent of Bd exposure. High dietary protein significantly increased resistance to Bd. Our results support the general hypothesis that host condition can strongly affect disease resistance; in particular, fluctuations in dietary protein availability may change how diseases affect populations in the field.

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Acknowledgments

We thank F. Brem for assistance collecting anuran eggs. The Rohr Lab at The University of South Florida provided helpful comments on an earlier draft of this manuscript. We also thank R. Alford for providing extensive editorial comments on an earlier draft of this manuscript. Collection permits from Tennessee were obtained prior to collecting the animals used in these experiments and all experimental procedures were approved by the University of Memphis IACUC. The experiments comply with the current laws of the USA. This publication was developed, in part, under a GRO Research Assistance Agreement No. MA-916980 awarded by the U.S. Environmental Protection Agency to M. Venesky. It has not been formally reviewed by the EPA. The views expressed in this document are solely those of the authors and the EPA does not endorse any products or commercial services mentioned in this publication. T. Wilcoxen was supported by a NSF Doctoral Dissertation Improvement Grant (IOS-0909620). L. Rollins-Smith was supported by NSF grants IOS-0619536 and IOS-0843207. Bd qPCR analysis was performed on instrumentation provided by NSF (MRI-0923419) to J. Kerby.

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Author notes

  1. Matthew D. Venesky

    Present address: Department of Integrative Biology, The University of South Florida, Tampa, FL, 33647, USA

  2. Travis E. Wilcoxen

    Present address: Department of Biology, Milikin University, Decatur, IL, 62522, USA

  3. Michelle A. Rensel

    Present address: Department of Integrative Biology and Physiology, University of California, Los Angeles, Los Angeles, CA, 90095, USA

Authors and Affiliations

  1. Department of Biological Sciences, The University of Memphis, Memphis, TN, 38152, USA

    Matthew D. Venesky, Travis E. Wilcoxen, Michelle A. Rensel & Matthew J. Parris

  2. Departments of Microbiology and Immunology, Pediatrics, and Biological Sciences, Vanderbilt University Medical Center, Nashville, TN, 37232, USA

    Louise Rollins-Smith

  3. Department of Biology, University of South Dakota, Vermillion, SD, 57069, USA

    Jacob L. Kerby

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  1. Matthew D. Venesky
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Correspondence to Matthew D. Venesky.

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Communicated by Ross Alford.

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Venesky, M.D., Wilcoxen, T.E., Rensel, M.A. et al. Dietary protein restriction impairs growth, immunity, and disease resistance in southern leopard frog tadpoles. Oecologia 169, 23–31 (2012). https://doi.org/10.1007/s00442-011-2171-1

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  • DOI: https://doi.org/10.1007/s00442-011-2171-1

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