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Temporal niche separation between the two ecologically similar nocturnal primates Avahi meridionalis and Lepilemur fleuretae

  • Marco CamperaEmail author
  • Michela Balestri
  • Marianna Chimienti
  • Vincent Nijman
  • K. A. I. Nekaris
  • Giuseppe Donati
Original Article

Abstract

Time is considered a resource in limited supply, and temporal niche separation is one of the most common strategies that allow ecologically similar species to live in sympatry. Mechanisms of temporal niche separation are understudied especially in cryptic animals due to logistical problems in gathering adequate data. Using high-frequency accelerometers attached to radio-collars, we investigated whether the ecologically similar lemurs Avahi meridionalis and Lepilemur fleuretae in the lowland rainforest of Tsitongambarika, south-eastern Madagascar, show temporal niche separation. Accelerometers stored data with a frequency of 1 Hz for a total of 71 days on three individuals of A. meridionalis and three individuals of L. fleuretae. We extrapolated motor activity patterns via the unsupervised learning algorithm expectation maximisation and validated the results with systematic behavioural observations. Avahi meridionalis showed peaks of activity at twilights with low but consistent activity during the day, while L. fleuretae exhibited more activity in the central hours of the night. Both lemur species had their activity pattern entrained by photoperiodic variations. The pair-living A. meridionalis was found to be lunarphilic while the solitary-living L. fleuretae was lunarphobic. We suggest that these activity differences were advantageous to minimise feeding competition, as an anti-predator strategy, and/or for dietary-related benefits. These findings demonstrate a fine-tuned temporal partitioning in sympatric, ecologically similar lemur species and support the idea that an activity spread over the 24-h, defined here as cathemerality sensu lato, is more common than previously thought in lemurs.

Significance statement

Ecologically similar species may exhibit temporal niche partitioning and separate their peaks of activity when co-occurring in an area. We show for the first time that the mainly nocturnal genus Avahi can exhibit high crepuscular activity with low but consistent bouts of activity (up to 44.6% of daily activity) during the day. We defined this activity as cathemerality sensu lato as opposed to the cathemerality sensu stricto observed in Eulemur sp. We suggest that this flexible activity may be advantageous for the species to minimise feeding competition and predatory pressure, and/or to provide dietary-related benefits. This finding in the secondary nocturnal genus Avahi supports the idea that activity patterns in lemurs are graded and traditional categorisations are inadequate.

Keywords

Niche partitioning Cathemeral Diel Madagascar Bio-logging Accelerometer 

Notes

Acknowledgments

We thank the Department of Animal Biology (University of Antananarivo), Asity Madagascar-BirdLife International, QIT Madagascar Minerals, the Association of Managers of the Forests of Ambatoatsinana, the Community Forest Management of Iaboakoho, and the Ministère des Eaux et Forets for their collaboration and permission to work in Madagascar. We are also grateful to Faniry Rakotoarimanana, Nataud, Johny Rabenantoandro, Jean Baptiste Ramanamanjato, and our field assistants, translators and volunteers for their dedication and effort. We thank the darting team of the Madagascar Biodiversity Partnership and Dr Edward Louis for helping with the captures and the collaring of the lemurs. We would like to thank Maria van Noordwijk and two anonymous reviewers for their suggestions to improve previous versions of this manuscript.

Author contributions

MCa, MB, and GD conceived and designed research. MCa and MB conducted the research. MCa, MCh, and GD analysed and interpreted the data. MCa and GD led the writing of the manuscript. MB, MCh, VN, and KAIN revised the manuscript critically for important intellectual content. All authors gave final approval for publication.

Funding

We were supported by the Rufford Foundation (no. 16946-1), the Mohamed bin Zayed Species Conservation Fund (no. 142510128), Primate Conservation Inc. (no. 001185), the Conservation International Primate Action Fund (no. 1001423), and a Primate Society of Great Britain Conservation Grant (no. Feb_2014).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

We obtained permission for the field research from the Ministry of Environment and Forest of Madagascar (XX/16/MEEMF/SG/DGF/DAPT/SCBT.Re). All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of Oxford Brookes University following the “Guidelines on the observation, handling and care of animals in field research”.

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Authors and Affiliations

  1. 1.Nocturnal Primate Research Group, Department of Social SciencesOxford Brookes UniversityOxfordUK
  2. 2.Department of BioscienceAarhus UniversityRoskildeDenmark

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