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Calling behavior of males and females of a Bornean frog with male parental care and possible sex-role reversal

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Abstract

In many species that use acoustic signals for mate attraction, males are usually the most vocal sex. In frogs, females typically remain silent, while males produce advertisement calls to attract mates. In some species, females vocalize, but usually as a response to an initial male advertisement call. The smooth guardian frog (Limnonectes palavanensis), found on Borneo, has exclusive paternal care while the females mate and desert after laying the clutch. Males provide care to the eggs until hatching and then they transport the tadpoles to small bodies of water. The vocal repertoire of this species has never been described. Males have a distinctive advertisement call to attract females, but produce the call very infrequently. We found that females of L. palavanensis not only respond to male advertisement calls but also vocalize spontaneously, forming lek-like aggregations around a single male. Males may or may not respond to a particular female with a short courtship call, which is elicited only by the female call and not the male advertisement call. The calling rate of females is consistently higher throughout the night compared with the calling rate of males. These observations suggest that this species exhibits a reversal in calling behavior and possibly a sex-role-reversed mating system.

Significance statement

Exceptional cases of species with a sex-role reversed mating system have been observed in fishes and birds, but not in frogs. For sex-role reversal to occur, there must be intense parental care by the males and a surplus of females. Additionally, females should exhibit characteristics that are usually observed in males in species with conventional sex roles. We found that in L. palavanensis, females are highly vocal, exhibiting higher calling rates compared with the calling rates of the males. This behavior, where females out-signal males has not been observed in anurans. This female calling behavior coupled with observations of several females approaching a male provides evidence of a female-biased operational sex ratio, a characteristic of a sex-role-reversed mating system. Thus, this study provides quantitative evidence that L. palavanensis exhibits various aspects consistent with a sex-role reversed mating system.

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Acknowledgments

We are thankful to the director of the Institute for Biodiversity and Environmental Research (IBER), the director of the Kuala Belalong Field Studies Centre (KBFSC) Hajah Masnah binti Haji Mirasan, and Rodzay bin Haji Abdul Wahab for facilitating our field work. We thank Teddy Chua Wee Li and Muhammad Salleh bin Abdullah Bat as well as the staff at the KBFSC for the logistic support in the field. We are grateful to Jana Englmeir, Fiana Shapiro, and Alexander Terry for field work assistance. We thank Morgan Tingley and Robert Bagchi for invaluable statistical advice and Elizabeth Jockusch, Mark Urban, Charles Henry, and two anonymous reviewers for helpful comments that greatly improved the manuscript. This work was partially funded by the Ralph M. Wetzel Endowment Fund and the Ecology and Evolutionary Biology Department at the University of Connecticut. Original recordings and datasets associated with this paper are available from the corresponding author on reasonable request.

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Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, University of Connecticut, 75 N Eagleville Rd. Unit 3043, Storrs, CT, 06269, USA

    Johana Goyes Vallejos & Kentwood D. Wells

  2. Department of Biology, Faculty of Science, Universiti Brunei Darussalam, Gadong, 1410, Brunei Darussalam

    T. Ulmar Grafe & Hanyrol H. Ahmad Sah

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  1. Johana Goyes Vallejos
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  2. T. Ulmar Grafe
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  3. Hanyrol H. Ahmad Sah
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  4. Kentwood D. Wells
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Contributions

JGV designed the study, collected and analyzed the data, and drafted the manuscript. TUG helped with the experimental design and data collection and provided comments on the manuscript. HHAS facilitated fieldwork. KDW helped with the experimental design of the study, drafting of the manuscript, and provided funding for fieldwork.

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Correspondence to Johana Goyes Vallejos.

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The authors declare that they have no conflict of interest.

Ethical Approval

All the behavioral observations and experimental methods done in this study were done in accordance with the Institutional Animal Care and Use Committee at the University of Connecticut (Approved Protocol No. A12-028) and followed the guidelines of the Animal Behavior Society (ABS) for the treatment of animals in behavioral research.

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Communicated by K. Summers

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Goyes Vallejos, J., Ulmar Grafe, T., Ahmad Sah, H.H. et al. Calling behavior of males and females of a Bornean frog with male parental care and possible sex-role reversal. Behav Ecol Sociobiol 71, 95 (2017). https://doi.org/10.1007/s00265-017-2323-3

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