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Parental investment by skin feeding in a caecilian amphibian

Nature volume 440, pages 926–929 (2006)Cite this article

Abstract

Although the initial growth and development of most multicellular animals depends on the provision of yolk, there are many varied contrivances by which animals provide additional or alternative investment in their offspring1. Providing offspring with additional nutrition should be favoured by natural selection when the consequent increased fitness of the young offsets any corresponding reduction in fecundity2. Alternative forms of nutrition may allow parents to delay and potentially redirect their investment. Here we report a remarkable form of parental care and mechanism of parent–offspring nutrient transfer in a caecilian amphibian. Boulengerula taitanus is a direct-developing, oviparous caecilian3, the skin of which is transformed in brooding females to provide a rich supply of nutrients for the developing offspring. Young animals are equipped with a specialized dentition, which they use to peel and eat the outer layer of their mother's modified skin. This new form of parental care provides a plausible intermediate stage in the evolution of viviparity in caecilians. At independence, offspring of viviparous and of oviparous dermatotrophic caecilians are relatively large despite being provided with relatively little yolk. The specialized dentition of skin-feeding (dermatophagous) caecilians may constitute a preadaptation to the fetal feeding on the oviduct lining of viviparous caecilians.

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Figure 1: Skin feeding in B. taitanus.
Figure 2: Comparison of the skin of non-brooding and brooding female B. taitanus , showing differences in skin colour, structure and histochemistry.
Figure 3: Dentition of adult and young B. taitanus.

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Acknowledgements

We thank D. Rotich, A. H. Jama and J. Western for arranging collection and export permits; A. Espira, J. Kibirisho and P. W. Kibirisho, J. W. Maghanga, A. Mschimba, D. Mwaghania and B. Mwakina for access to their land and for help in performing fieldwork; A. Ball, E. B. Morello, J. Newberry and B. Williamson for help with the SEM preparations; D. Cooper for preparing some histological sections; T. Vinhas for help with processing video footage; B. Bwong, P. K. Malonza and G. J. Measey for logistic support; and R. Britz, J. J. Day, D. J. Gower, S. Mohun, L. Rüber and E. Valk for improving earlier versions of the manuscript. This work was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico, by the Natural Environment Research Council, and by a Marie Curie Fellowship.

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Authors and Affiliations

  1. Department of Zoology, The Natural History Museum, Cromwell Road, SW7 5BD, London, UK

    Alexander Kupfer, Hendrik Müller & Mark Wilkinson

  2. Institute of Biology, Leiden University, Kaiserstraat 63, 2311 GP, Leiden, The Netherlands

    Hendrik Müller

  3. Laboratório de Biologia Celular, Instituto Butantan, Av. Vital Brasil 1500, 05503-900, São Paulo, Brazil

    Marta M. Antoniazzi & Carlos Jared

  4. Institut für Zoomorphologie und Zellbiologie der Heinrich-Heine-Universität Düsseldorf, Universitätstrasse, D-40225 , Düsseldorf, Germany

    Hartmut Greven

  5. Museum of Zoology and Department of Ecology and Evolutionary Biology, University of Michigan , Michigan, 48109, Ann Arbor, USA

    Ronald A. Nussbaum

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  1. Alexander Kupfer
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Correspondence to Mark Wilkinson.

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Kupfer, A., Müller, H., Antoniazzi, M. et al. Parental investment by skin feeding in a caecilian amphibian. Nature 440, 926–929 (2006). https://doi.org/10.1038/nature04403

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