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Extreme tadpoles II: the highly derived larval anatomy of Occidozyga baluensis (Boulenger, 1896), an obligate carnivorous tadpole

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Abstract

Tadpoles of Occidozyga species have been reported to be carnivorous, feeding on insects and other tadpoles. We present photographic evidence for the previously undocumented larval feeding behavior in O. baluensis. Furthermore, we present a detailed anatomical description of the skull, cranial musculature, and gross gut morphology based on three-dimensional reconstructions from serial sections and μCT imagery. The cranial anatomy of larval O. baluensis is highly derived in many characters, with respect to taxa outside the genus Occidozyga, most notably the palatoquadrate and hyobranchial apparatus, that play a major role in tadpole feeding. A large larval stomach was present in the specimens examined, indicative of a macrophagous carnivorous mode of feeding. Because of the relatively small oral orifice, relatively large-sized food items found in the larval stomach, and the tunnel-like arrangement of structures that form the buccal cavity, we hypothesize that suction feeding utilizing strong negative pressure is employed by this species. Furthermore, we propose that force, rather than speed, is the main characteristic of their feeding. The unique features of the study species substantially expand the known morphospace for tadpoles, particularly among the Acosmanura (Pelobatoidea, Pelodytoidea, and Neobatrachia). Except for Microhylidae, acosmanurans previously described possess limited innovative larval morphologies. Larval carnivory has evolved convergently several times in distant anuran clades and shows structural, behavioral, and functional differences in the known examples.

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Abbreviations

3D:

Three-dimensional

cart.:

Cartilago

for.:

Foramen

lev.:

Levator

m.:

Musculus

mand.:

Mandibulae

proc.:

Processus

prof.:

Profundus

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Acknowledgments

We wish to thank the Sarawak Forest Department, in particular Datuk Cheong Ek Choon, Director, and Bolhan Budeng, for issuing collecting permits (NPW.907.4–36) and export permits. The Economic Planning Unit, The Prime Minister’s Department, Malaysia, and especially Mrs. Munirah Abd. Manan were supportive in issuing research permit No. 1168 to A. Haas. Sabah Parks provided research permit TS/PTD/5/4, and we thank J. Nais. At the DESY facility, work would not have been possible without unconditional support of F. Beckmann and J. Herzen. We received skillful help from A.M. Vogt with some of the serial sectioning and clearing and staining. We gratefully acknowledge funding of the Volkswagen Foundation, Germany (Grant I/79 405 to AH and ID), Naturhistorisches Museum der Burgergemeinde Bern, Universität Hamburg, and Universiti Malaysia Sarawak. The work at Gunung Mulu National Park was generously supported in many different ways and on several occasions by Brian and Sue Clark and their staff, whom we cannot thank enough. The work of Rolf Beutel and Frank Friedrich for determination of the beetle larvae extracted from O. baluensis tadpoles is much appreciated.

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  1. Biozentrum Grindel und Zoologisches Museum Hamburg, Martin-Luther-King-Platz 3, 20146, Hamburg, Germany

    Alexander Haas & Jana Pohlmeyer

  2. University of Kansas Biodiversity Institute, 1345 Jayhawk Boulevard, Lawrence, KS, 66045-7561, USA

    David S. McLeod

  3. Functional Morphology and Biomechanics, Christian-Albrechts-Universität Kiel, Am Botanischen Garten 1–9, 24098, Kiel, Germany

    Thomas Kleinteich

  4. Naturhistorisches Museum der Burgergemeinde Bern, Bernastrasse 15, 3005, Bern, Switzerland

    Stefan T. Hertwig

  5. Institute of Biodiversity and Environmental Conservation, Universiti Malaysia Sarawak, 94300, Kota Samarahan, Sarawak, Malaysia

    Indraneil Das

  6. Department of Biological Sciences, University of Cincinnati, 711A Rieveschl Hall, 312 Clifton Ct., Cincinnati, OH, 45221, USA

    Daniel R. Buchholz

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  1. Alexander Haas
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Correspondence to Alexander Haas.

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Communicated by A. Schmidt-Rhaesa.

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Haas, A., Pohlmeyer, J., McLeod, D.S. et al. Extreme tadpoles II: the highly derived larval anatomy of Occidozyga baluensis (Boulenger, 1896), an obligate carnivorous tadpole. Zoomorphology 133, 321–342 (2014). https://doi.org/10.1007/s00435-014-0226-7

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