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Predator avoidance and dietary fibre predict diurnality in the cathemeral folivore Hapalemur meridionalis

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Abstract

Though numerous mammalian taxa exhibit cathemerality (i.e. activity distributed across the 24-h cycle), this includes very few primates, exceptions being species from Aotinae and Lemuridae. Four non-mutually exclusive hypotheses have been proposed to explain the ultimate determinants for cathemeral activity in lemurs: thermoregulatory benefits, anti-predator strategy, competition avoidance and metabolic dietary-related needs. However, these have only been explored in the frugivorous genus Eulemur, with some species increasing nocturnality as a possible response to avoid diurnal raptors and to increase their ability to digest fibre during resource-scarce periods. Since Eulemur lack specializations for digesting bulk food, this strategy would allow for processing fibres over the full 24-h. The folivorous lemurids, i.e. genus Hapalemur, provide a divergent model to explore these hypotheses due to gastrointestinal adaptations for digesting dietary fibre and small body size compared to Eulemur. We linked continuous activity data collected from archival tags with observational behaviour and feeding data from three groups of adult Hapalemur meridionalis from January to December 2013. We tested the effects of thermoregulation, predator avoidance and the weighted proportion of digestible dietary fibre on the daily diurnal/nocturnal activity ratio using a Linear Mixed-Model. Our best-fit model revealed that increased canopy exposure and dietary fibre predicted greater diurnality. Our findings partly contrast with previous predictions for frugivorous lemurids. We propose a divergent adaptive explanation for folivorous lemurids. We suggest that the need to avoid terrestrial predators, as well as longer digestive bouts during bulk food periods, may override cathemerality in favour of diurnality in these bamboo lemurs.

Significance statement

Southern bamboo lemurs are active throughout the 24-h day, with high proportions of dietary fibre increasing diurnality, in contrast to other cathemeral primates. They also increase diurnality on days when using areas with greater canopy exposure, potentially avoiding nocturnal predators in risky foraging areas. We suggest that folivorous lemurids may require long periods of inactivity to conserve energy and digest dietary fibre, thus limiting activity to periods of optimal foraging efficiency over the 24-h cycle.

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Acknowledgments

We thank the Direction du Système des Aires Protégées and the Ministère de l’Environnement et Forêts of Madagascar for permission to conduct research. We are grateful to Jacques Rakotondranary and Tolona Andrianasolo for obtaining our research permits and to Katie Hall and Natalie Breden for assistance in the field. We also thank the Environment Team at QMM Rio Tinto for their assistance and provision of logistical support on-site and acknowledge their helpful staff, especially Jean-Baptiste Ramanamanjato, Johny Rabenantoandro, Faly Randriatafika, Laza Andriamandimbiarisoa, David Rabehevitra, Claude Soanary and Robertin Ravelomanantsoa. Many thanks are due to Irene Tomaschewski for the plant biochemical analyses. We would like to thank Maria van Noordwijk and two anonymous reviewers for their suggestions to improve previous versions of this manuscript.

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Authors and Affiliations

  1. Department of Anthropology, University of Texas, Austin, TX, USA

    Timothy M. Eppley

  2. Biozentrum Grindel, Department of Animal Ecology and Conservation, University of Hamburg, Hamburg, Germany

    Timothy M. Eppley & Jörg U. Ganzhorn

  3. Nocturnal Primate Research Group, Department of Social Sciences, Oxford Brookes University, Oxford, UK

    Timothy M. Eppley & Giuseppe Donati

  4. Language Research Center, Department of Psychology, Georgia State University, Atlanta, GA, USA

    Julia Watzek

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Correspondence to Timothy M. Eppley.

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Ethical statement

This work was supported by the American Society of Primatologists, Conservation International (Primate Action Fund), Idea Wild, Mohamed bin Zayed Species Conservation Fund (Project Number: 11253008), Primate Conservation Inc. and Primate Society of Great Britain/Knowsley Safari Park. This research was carried out under the Accord de Collaboration between the Department of Animal Biology of the University of Antananarivo and the Department of Animal Ecology and Conservation of the University of Hamburg and QIT Madagascar Minerals (QMM). Research protocols were approved and permits authorized by the Commission Tripartite of the Direction des Eaux et Forêts de Madagascar (Autorisation de recherché No. 240/12/MEF/SG/DGF/DCB.SAP/SCB du 17 September 2012), adhering to the legal requirements of Madagascar. All data were collected in accordance with the ASAB/ABS Guidelines for Use of Animals in Research.

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Communicated by M. A. van Noordwijk

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Eppley, T.M., Watzek, J., Ganzhorn, J.U. et al. Predator avoidance and dietary fibre predict diurnality in the cathemeral folivore Hapalemur meridionalis . Behav Ecol Sociobiol 71, 4 (2017). https://doi.org/10.1007/s00265-016-2247-3

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