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Maximal thermogenic capacity and non-shivering thermogenesis in the South American subterranean rodent Ctenomys talarum

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Abstract

Subterranean rodents inhabit closed tunnel systems that are hypoxic and hypercapnic and buffer aboveground ambient temperature. In contrast to other strictly subterranean rodents, Ctenomys talarum exhibits activity on the surface during foraging and dispersion and hence, is exposed also to the aboveground environment. In this context, this species is a valuable model to explore how the interplay between underground and aboveground use affects the relationship among basal metabolic rate (BMR), cold-induced maximum metabolic rate (MMR), shivering (ST), and non-shivering thermogenesis (NST). In this work, we provide the first evidence of the presence of NST, including the expression of uncoupling proteins in brown adipose tissue (BAT), and shivering thermogenesis in Ctenomys talarum, a species belonging to the most numerous subterranean genus, endemic to South America. Our results show no differences in BMR, cold-induced MMR, and NST between cold- (15 °C) and warm- (25 °C) acclimated individuals. Furthermore, thermal acclimation had no effect on the expression of mitochondrial uncoupling protein 1 (UCP1) in BAT. Only cytochrome c oxidase (COX) content and activity increased during cold acclimation. When interscapular BAT was removed, NST decreased more than 30 %, whereas cold-induced MMR remained unchanged. All together, these data suggest that cold-induced MMR reaches a maximum in warm-acclimated individuals and so a probable ceiling in NST and UCP1 expression in BAT. Possible thermogenic mechanisms explaining the increase in the oxidative capacity, mediated by COX in BAT of cold-acclimated individuals and the role of ST in subterranean life habits are proposed.

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Acknowledgments

We thank R.R. Zenuto, M. S. Fanjul, and F. Luchessi for helping with individuals in the lab and during surgery procedures. We also thank J. Sastre for assisting us during molecular laboratory work. We appreciate the comments provided by reviewers that improved an earlier version of this manuscript. Special thanks are due to F. Vera for English linguistic revision of the manuscript. FL was supported by CONICET Partial Travel Support. This work was supported by CONICET (PIP 2787 to CDA), and by ANPCyT (PICT 2102 to CDA, and PICT 1816 to FL).

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  1. Laboratorio de Ecología Fisiológica y del Comportamiento, Instituto de Investigaciones Marinas y Costeras (IIMyC), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Universidad Nacional de Mar del Plata, Mar del Plata, Argentina

    Facundo Luna & C. Daniel Antenucci

  2. Grupo Multidisciplinar de Oncología Traslacional, Institut Universitari d’Investigació en Ciències de la Salut (IUNICS), Palma de Mallorca, Illes Balears, Spain

    Pilar Roca & Jordi Oliver

  3. Laboratorio de Ecología Fisiológica y del Comportamiento, Universidad Nacional de Mar del Plata, CC1245, Mar del Plata, Argentina

    Facundo Luna

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  1. Facundo Luna
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  2. Pilar Roca
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  4. C. Daniel Antenucci
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Correspondence to Facundo Luna.

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Communicated by I.D. Hume.

C.D. Antenucci was formerly C.D. Antinuchi.

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Luna, F., Roca, P., Oliver, J. et al. Maximal thermogenic capacity and non-shivering thermogenesis in the South American subterranean rodent Ctenomys talarum . J Comp Physiol B 182, 971–983 (2012). https://doi.org/10.1007/s00360-012-0675-6

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