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Reef manta ray cephalic lobe movements are modulated during social interactions

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Abstract

Reef manta rays (Mobula alfredi) are social elasmobranchs that have structured societies and actively interact with preferred social partners. Being able to detect cues and signals produced by conspecifics is vital in enabling social behavior. Many elasmobranch species communicate via body and fin postures, but it is not yet known if or how mobulid rays communicate or respond to cues produced by conspecifics. These rays have specialized cephalic lobes that are highly flexible and used in feeding, but may have other functions such as gestural communication. In this study, we developed a standardized method to assess manta ray behavior in the wild via focal sampling and frame-by-frame video analysis. From observations recorded at cleaning stations in Raja Ampat, West Papua, we described various types of cephalic lobe positioning and movements made by free-ranging M. alfredi and investigated these in different behavioral contexts. We found that cephalic lobe curls were modulated when approaching both conspecifics and human divers, as well as during interactions with cleaner fish, suggesting that these lobes may be used in sensing water movements, olfactory sensing, and/or gestural communication. Cephalic lobes were moved independently of one another, but we found no evidence of individual laterality. The lack of chemosensory capacity on the lobes suggests that gestural communication is the most likely function, but further research is required to determine this. These results are informative in understanding the function of gestural communication in manta ray social interactions and add to our growing understanding of elasmobranchs’ sophisticated social behavior.

Significance statement

Social animals rely on communication and cues produced by conspecifics to respond to opportunities and threats. Many elasmobranch species use body and fin postures as gestural signals during competitive, courtship, and other social interactions. Reef manta rays (Mobula alfredi) are social elasmobranchs that form groups in near-shore, shallow water habitats. They possess paired, flexible cephalic lobes positioned on the side of the head which are specialized for feeding but may have a variety of functions. Here, we describe, quantify, and suggest likely explanations for the movement and positioning of cephalic lobes during various manta ray social behaviors, including conspecific, human, and cleaner fish interactions. Our results suggest that lobe movements may be used in detecting water movements, olfactory sensing, and/or gestural communication, and are an important aspect of social behavior in this species.

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Data availability

All data used for the analyses in this manuscript is available on request to the lead author.

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Acknowledgments

We would like to thank Papua Explorers Dive Resort, Raja Ampat SEA Centre, the University of Papua, Dr. Ricardo Tapilatu, Barefoot Conservation and RisTek-Dikti, for their invaluable support in enabling our fieldwork in Raja Ampat. Thanks also to Stephanie Venables and Loïc Van Doorn for their help with data collection, and to Charles Griffiths for supervision of Ms. Carpenter’s input to this study. Mr. Perryman would like to thank Macquarie University for their academic support and the provision of his PhD scholarship. We also thank two anonymous reviewers and the journal editor for their useful input which helped to improve this manuscript.

Funding

This research was funded through Marine Megafauna Foundation and RJYP’s PhD scholarship.

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Authors and Affiliations

  1. Department of Biological Sciences, Macquarie University, Sydney, Australia

    Robert J.Y. Perryman & Culum Brown

  2. Marine Megafauna Foundation, Truckee, CA, USA

    Robert J.Y. Perryman & Andrea D. Marshall

  3. Department of Biological Sciences, University of Cape Town, Cape Town, South Africa

    Michelle Carpenter

  4. Department of Mathematics and Statistics, Macquarie University, Sydney, Australia

    Eric Lie & Georgy Sofronov

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  1. Robert J.Y. Perryman
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Contributions

RJYP and MC conceived the central idea of the manuscript. RJYP collected all video recording data from the field study location. MC recorded all behavioral observations from video data, with input from RJYP. RJYP conducted all statistical analyses, except for the Markov-based analysis, which was developed by RJYP, GS, and EL, and conducted by EL. RJYP wrote the manuscript with input from MC. All authors contributed to editing and manuscript revisions.

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Correspondence to Robert J.Y. Perryman.

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All applicable international, national, and/or institutional guidelines for the use of animals were followed. This research was part of a larger overall project for which ethical approval for all research was granted under an Australian Animal Research Authority permit, number: 2017/037 (Social Behaviour and Social Network Analysis in a Reef Manta Ray Population). Because this was an observation study only, however, no ethical approval for the data collected during this study was required. No capture, manipulation, or harm of animals was undertaken.

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Permission to conduct research in Indonesia was granted to RJYP by Ristek-Dikti, research permit numbers: 773/FRP/E5/Dit.Kl/IV/2016; 426/SIP/FRP/E5/Dit.Kl./XI/2017; 39/E5/E5.4/SIP/2019. All legal and institutional requirements to conduct research in Indonesia were met.

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Communicated by I. Hamilton

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Perryman, R.J., Carpenter, M., Lie, E. et al. Reef manta ray cephalic lobe movements are modulated during social interactions. Behav Ecol Sociobiol 75, 51 (2021). https://doi.org/10.1007/s00265-021-02973-x

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