Predator avoidance and dietary fibre predict diurnality in the cathemeral folivore Hapalemur meridionalis
- 244 Downloads
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.
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.
KeywordsPredator avoidance strategy Diel activity Dietary fibre Lunarphilia Southern bamboo lemur Thermoregulation
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.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
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.
- Aschoff J (1988) Masking of circadian rhythms by zeitgebers as opposed to entrainment. In: Hekkens WTJM, Kerkhof GA, Rietveld WJ (eds) Trends in chronobiology: advances in the biosciences. Pergamon Press, Oxford, pp. 149–161Google Scholar
- Bates D, Maechler M, Bolker B (2012) lme 4: Linear mixed-effects models using S4 classes. R package version 0.999375-42, http://CRAN.R-project.org/package=lme4
- Beier P, McCullough DR (1990) Factors influencing white-tailed deer activity patterns and habitat use. Wildlife Monogr 109:3–51Google Scholar
- Cabre-Vert N, Feistner ATC (1995) Comparative gut passage time in captive lemurs. Dodo 31:76–81Google Scholar
- Charles-Dominique P (1975) Nocturnality and diurnality: an ecological interpretation of these two modes of life by an analysis of the higher vertebrate fauna in tropical forest ecosystems. In: Luckett WP, Szalay FS (eds) Phylogeny of the primates: a multidisciplinary approach. Plenum Press, New York, pp. 69–88CrossRefGoogle Scholar
- Charles-Dominique P, Cooper HM, Hladik A, Hladik CM, Pages E, Pariente GF, Petter Rousseaux A, Petter JJ, Schilling A (1980) Nocturnal Malagasy primates: ecology, physiology and behavior. Academic Press, New YorkGoogle Scholar
- Cohen J, Cohen P, West SG, Aiken LS (2003) Applied multiple regression/correlation analysis for the behavioral sciences, 3rd edn. Erlbaum, Mahwah, New JerseyGoogle Scholar
- Cork SJ, Foley WJ (1991) Digestive and metabolic strategies of arboreal mammalian folivores in relation to chemical defences in temperate and tropical forests. In: Palo RT, Robbins CT (eds) Plant defences against mammalian herbivory. CRC Press, Boca Raton, FL, pp. 133–166Google Scholar
- Curtis DJ, Rasmussen MA (2002) Cathemerality in lemurs. Evol Anthropol 11(Suppl):83–86Google Scholar
- Donati G, Borgognini-Tarli SM (2006b) From darkness to daylight: cathemeral activity in primates. J Anthropol Sci 84:7–32Google Scholar
- Donati G, Lunardini A, Kappeler PM (1999) Cathemeral activity of red-fronted brown lemurs (Eulemur fulvus rufus) in the Kirindy Forest/CFPF. In: Rakotosamimanana B, Rasamimanana H, Ganzhorn JU, Goodman SM (eds) New directions in lemur studies. Plenum Press, New York, pp. 119–137CrossRefGoogle Scholar
- Donati G, Ramanamanjato JB, Ravoahangy AM, Vincelette M (2007b) Translocation as a conservation measure for a threatened species: the case of Eulemur collaris in the Mandena littoral forest, south-eastern Madagascar. In: Ganzhorn JU, Goodman SM, Vincelette M (eds) Biodiversity, ecology, and conservation of the littoral ecosystems in southeastern Madagascar, Tolagnaro (Fort Dauphin). Smithsonian Institution Press, Washington, DC, pp. 237–243Google Scholar
- Eppley TM, Ravelomanantsoa R (2015) Predation of an adult southern bamboo lemur Hapalemur meridionalis by a Dumeril’s boa Acrantophis dumerili. Lemur News 19:2–3Google Scholar
- Fidgett AL, Feistner ATC, Galbraith H (1996) Dietary intake, food composition and nutrient intake in captive Alaotran gentle lemurs Hapalemur griseus alaotrensis. Dodo 32:44–62Google Scholar
- Field A (2013) Discovering statistics using SPSS, 4th edn. Sage, LondonGoogle Scholar
- Holley AJF (2001) The daily activity period of the brown hare (Lepus europaeus). Mammal Biol 66:357–364Google Scholar
- Martin RD (1990) Primate origins and evolution: a phylogenetic reconstruction. Chapman & Hall, LondonGoogle Scholar
- Ortmann S, Bradley BJ, Stolter C, Ganzhorn JU (2006) Estimating the quality and composition of wild animal diets—a critical survey of methods. In: Hohmann G, Robbins MM, Boesch C (eds) Feeding ecology in apes and other primates. Cambridge University Press, Cambridge, pp. 395–418Google Scholar
- Polat ES, Coskun B, Gurbuz E, Balevi T (2013) The effects of roughage type on the daily patterns of feed intake and eating behaviour in young sheep. Rev Med Vet-Toulouse 164:503–510Google Scholar
- Rasmussen MA (1999) Ecological influences on activity cycle in two cathemeral primates, Eulemur mongoz (mongoose lemur) and Eulemur fulvus fulvus (common brown lemur). PhD Dissertation, Duke UniversityGoogle Scholar
- R Development Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, http://www.R-project.org/
- Schwitzer N, Kaumanns W, Seitz PC, Schwitzer C (2007) Cathemeral activity patterns of the blue-eyed black lemur Eulemur macaco flavifrons in intact and degraded forest fragments. Endanger Species Res 3:239–247Google Scholar
- Singmann H (2014) afex: analysis of factorial experiments. R package (version 0.9-109), http://CRAN.R-project.org/package=afex
- Zalewski A (2000) Factors affecting the duration of activity by pine martens (Martes martes) in the Białowieża National Park, Poland. J Zool 251:439–447Google Scholar