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Parasitic castration in slipper limpets infested by the symbiotic crab Calyptraeotheres garthi

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Abstract

Two ill-explored hypotheses might explain host castration by parasitic pea crabs. The ‘energy drain’ hypothesis states that castration is caused by host-derived nutrient consumption of parasites that ultimately diminishes host-energy intake. The ‘steric interference’ hypothesis states that castration occurs when parasites physically inhibit host reproduction. This study evaluated whether Calyptraeotheres garthi, a pea crab from the southwestern Atlantic, is a parasitic castrator and explored whether the two hypotheses above explain castration in the limpet Crepidula cachimilla. None of three studied limpet species brooded embryos during the reproductive season when infested by mature female pea crabs. Also, limpets of C. cachimilla infested by C. garthi did not reproduce during a 90-day experimental period while crab-free limpets did spawn embryos during this period. Limpets resumed reproduction soon after pea crabs were experimentally removed from their brooding chamber. Thus, C. garthi does castrate limpets, and castration is reversible. Pea crabs ‘steal’ food from limpets, and infested limpets did not modify their feeding behavior to counteract nutrient loss. Thus, infested limpets are expected to ingest less food which provides partial support for the ‘energy drain’ hypothesis. However, the limpet’s body condition increased or was not affected by pea crabs during the breeding season which argues against the same hypothesis. Furthermore, that limpets promptly recovered reproductive activity once pea crabs were experimentally removed, that castration was not induced by the smallest pea crabs in the population (that fill only partially the brooding chamber), and that parasitized limpets did exhibit fully mature ovaries, support the ‘steric interference’ hypothesis explaining parasitic castration.

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Acknowledgments

We are grateful to Emiliano Pisani for providing us with phytoplankton, Nicolas Chiaradia for helping us with photographs, and the fishermen Mario (el Ruso) and Gabriel for helping us in collecting limpets at Piedras Coloradas. We also thank Enrique Morsan and colleagues at IBMP (Instituto de Biología Marina y Pesquera, Almirante Storni) for their hospitality during sampling at San Matias Gulf. Part of the material used for the present study was collected by E.O. during the campaign Mejillón II-2009, on board the Oceanographic R/V Puerto Deseado. We are grateful to two anonymous reviewers for valuable suggestions on the manuscript. The present work was partially supported by PIP 2008 112-384 200-801-02190 (CONICET—Consejo Nacional de Investigaciones Científicas y Técnicas de Argentina) and EXA 515/10 (UNMdP—Universidad Nacional de Mar del Plata, Argentina). E.O. received scholarship support from CONICET. The present results are part of the PhD dissertation of E.O. This is a contribution of the Smithsonian Marine Station at Fort Pierce, Smithsonian Institution.

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Authors and Affiliations

  1. Laboratorio de Invertebrados, IIMYC – Instituto de Investigaciones Marinas y Costeras, CONICET–UNMDP, Funes 3350, Mar del Plata 7600, Buenos Aires, Argentina

    Emiliano H. Ocampo & Jesús D. Nuñez

  2. EGEM–Laboratorio de Ecología y Genética de Especies Marinas, IIMYC, CONICET–UNMDP, Funes 3350, Mar del Plata 7600, Buenos Aires, Argentina

    Maximiliano Cledón

  3. Department of Biological Sciences, Clemson University, Clemson, SC, 29632, USA

    J. Antonio Baeza

  4. Smithsonian Marine Station at Fort Pierce, Fort Pierce, FL, 34949, USA

    J. Antonio Baeza

  5. Departamento de Biología Marina, Facultad de Ciencias del Mar, Universidad Católica del Norte, Coquimbo, Chile

    J. Antonio Baeza

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  1. Emiliano H. Ocampo
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  2. Jesús D. Nuñez
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  3. Maximiliano Cledón
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  4. J. Antonio Baeza
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Correspondence to Emiliano H. Ocampo.

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Communicated by M. G. Chapman.

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Ocampo, E.H., Nuñez, J.D., Cledón, M. et al. Parasitic castration in slipper limpets infested by the symbiotic crab Calyptraeotheres garthi . Mar Biol 161, 2107–2120 (2014). https://doi.org/10.1007/s00227-014-2490-y

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