Skip to main content

Advertisement

Log in

Coping with low-quality diets: a first account of the feeding ecology of the southern gentle lemur, Hapalemur meridionalis, in the Mandena littoral forest, southeast Madagascar

  • News and Perspectives
  • Published:
Primates Aims and scope Submit manuscript

Abstract

Malagasy primates of the genus Hapalemur are exceptional in their exhibition of specialisations allowing for a folivorous diet despite their small body size. Members of this group are well known for their preference for specific parts of woody bamboo, the primary food resource throughout much of their range. The southern gentle lemur (H. meridionalis), however, inhabits littoral forests that contain little or no woody bamboo. Similar to its closely related congener, the Alaotran gentle lemur (H. alaotrensis), the question is raised as to how these lemurs subsist in this ecological context. The aim of this study was to gain an initial understanding of the ecological niche of the southern gentle lemur in the threatened ecosystem of the littoral forest of southeastern Madagascar. Lemurs were habituated and observed over a 3-month period during the austral winter, allowing for collection of both continuous and instantaneous focal data on their feeding ecology. Preferred food species were identified and collected, and biochemical analyses determined macronutrient and secondary compound values for consumed food items. The diet of the southern gentle lemur was found to be of low nutritional quality, as evaluated through the low protein-to-fibre ratio, especially when compared with other folivores. This lemur is also unique in spending a majority of its time grazing on terrestrial grasses (family Poaceae) during the resource-poor winter months. Our data indicate that Hapalemur spp. possess a behavioural flexibility, and possibly, digestive abilities, higher than previously thought for an animal of its small body size.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:226–267

    Article  Google Scholar 

  • Barton RA, Whiten A, Bryne RW, English M (1993) Chemical composition of baboon plant foods: implications for the interpretation of intra- and interspecific differences in diet. Folia Primatol 61:1–20

    Article  CAS  PubMed  Google Scholar 

  • Bollen A, Donati G (2006) Conservation status of the littoral forest of south-eastern Madagascar: a review. Oryx 40:57–66

    Article  Google Scholar 

  • Cabre-Vert N, Feistner ATC (1995) Comparative gut passage time in captive lemurs. Dodo 31:76–81

    Google Scholar 

  • Campbell JL, Eisemann JH, Williams CV, Glenn KM (2000) Description of the gastrointestinal tract of five lemur species: Propithecus tattersalli, Propithecus verreauxi coquereli, Varecia variegata, Hapalemur griseus, and Lemur catta. Am J Primatol 52:133–142

    Article  CAS  PubMed  Google Scholar 

  • Chapman CA, Chapman LJ, Bjorndal KA, Onderdonk DA (2002) Application of protein-to-fiber ratios to predict colobines abundance on different spatial scales. Int J Primatol 23:283–310

    Article  Google Scholar 

  • Chapman CA, Chapman LJ, Naughton-Treves L, Lawes MJ, McDowell LR (2004) Predicting folivorous primate abundance: validation of a nutritional model. Am J Primatol 62:55–69

    Article  PubMed  Google Scholar 

  • Dasilva GL (1994) Diet of Colobus polykomos on Tiwai Island: selection of food in relation to its seasonal abundance and nutritional quality. Int J Primatol 15:655–680

    Article  Google Scholar 

  • Donati G, Baldi N, Morelli V, Ganzhorn JU, Borgognini-Tarli SM (2009) Proximate and ultimate determinants of cathemeral activity in brown lemurs. Anim Behav 77:317–325

    Article  Google Scholar 

  • Dransfield S (2000) Woody bamboos (Gramineae-Bambusoideae) of Madagascar. In: Jacobs SWL, Everett J (eds) Grasses: systematics and evolution. CSIRO, Melbourne, pp 43–50

    Google Scholar 

  • Edwards MS, Ullrey DE (1999) Effect of dietary fiber concentration on apparent digestibility and digesta passage in non-human primates. I. Ruffed lemurs (Varecia variegata variegata and V. v. rubra). Zoo Biol 18:529–536

    Article  Google Scholar 

  • Engqvist A, Richard A (1991) Diet as a possible determinant of cathemeral activity patterns in primates. Folia Primatol 57:169–172

    Article  CAS  PubMed  Google Scholar 

  • Fairgrieve C, Muhumuza G (2003) Feeding ecology and dietary differences between blue monkey (Cercopithecus mitus stuhlmanni Matschie) groups in logged and unlogged forest, Budongo Forest Reserve, Uganda. Afr J Ecol 41:141–149

    Article  Google Scholar 

  • Fashing PJ, Dierenfeld ES, Mowry CB (2007) Influence of plant and soil chemistry on food selection, ranging patterns, and biomass of Colobus guereza in Kakamega Forest, Kenya. Int J Primatol 28:673–703

    Article  Google Scholar 

  • Fidgett AL, Feistner ATC, Galbraith H (1996) Dietary intake, food composition and nutrient intake in captive Alaotran gentle lemurs Hapalemur griseus alaotrensis. Dodo 32:44–62

    Google Scholar 

  • Ganzhorn JU (1995) Low-level forest disturbance effects on primary production, leaf chemistry, and lemur populations. Ecol 76:2084–2096

    Article  Google Scholar 

  • Ganzhorn JU, Lowry PP II, Schatz GE, Sommer S (2001) The biodiversity of Madagascar: one of the world’s hottest hotspots on its way out. Oryx 35:346–348

    Google Scholar 

  • Ganzhorn JU, Andrianasolo T, Andrianjazalahatra T, Donati G, Fietz J, Lahann P, Norscia I, Rakotondranary J, Rakotondratsima BM, Ralison J, Ramarokoto REAF, Randriamanga S, Rasarimanana S, Rakotosamimanana B, Ramanamanjato J-B, Randria G, Rasolofoharivelo MT, Razanahoera-Rakotomalala M, Schmid J, Sommer S (2007) Lemurs in evergreen littoral forest fragments. In: Ganzhorn JU, Goodman SM, Vincelette M (eds) Biodiversity, ecology, and conservation of the littoral ecosystems in southeastern Madagascar, Tolagnaro (Fort Dauphin). Smithsonian Institution, Washington, DC, pp 223–225

    Google Scholar 

  • Grassi C (2006) Variability in habitat, diet, and social structure of Hapalemur griseus in Ranomafana National Park, Madagascar. Am J Phys Anthropol 131:50–63

    Article  PubMed  Google Scholar 

  • Hladik CM (1978) Adaptive strategies of primates in relation to leaf-eating. In: Montgomery GG (ed) The ecology of arboreal folivores. Smithsonian Institute Press, Washington, DC, pp 373–392

    Google Scholar 

  • Johns A, Skorupa J (1987) Responses of rainforest primates to habitat disturbance: a review. Int J Primatol 8:157–191

    Article  Google Scholar 

  • Johnson KG, Schaller GB, Jinchu H (1988) Comparative behavior of red and giant pandas in the Wolong Reserve, China. J Mammal 69:552–564

    Article  Google Scholar 

  • Justice KE, Smith FA (1992) A model of dietary fiber utilization by small mammalian herbivores, with empirical results for Neotoma. Am Nat 139:398–416

    Article  Google Scholar 

  • Kar-Gupta K, Kumar A (1994) Leaf chemistry and food selection by common langurs (Presbytis entellus) in Rajaji National Park, Uttar Pradesh, India. Int J Primatol 15:75–93

    Article  Google Scholar 

  • Kleiber M (1961) The fire of life: an introduction to animal energetics. Wiley, New York, p 453

    Google Scholar 

  • Martin RD (1990) Primate origins and evolution: a phylogenetic reconstruction. Princeton University Press, Princeton, p 840

    Google Scholar 

  • McKey DB, Gartlan JS, Waterman PG, Choo GM (1981) Food selection by black colobus (Colobus satanas) in relation to plant chemistry. Biol J Linn Soc 16:115–146

    Article  Google Scholar 

  • Milton K (1978) Behavioral adaptation to leaf-eating by the mantled howler monkey (Alouatta palliata). In: Montgomery GG (ed) The ecology of arboreal folivores. Smithsonian Institution Press, Washington, DC, pp 535–549

    Google Scholar 

  • Milton K (1979) Factors influencing leaf choice by howler monkeys: a test of some hypotheses of food selection by general herbivores. Am Nat 114:362–378

    Article  CAS  Google Scholar 

  • Mittermeier RA, Konstant WR, Hawkins F, Louis EE, Langrand O, Ratsimbazafy J, Rasoloarison R, Ganzhorn JU, Rajaobelina S, Tattersall I, Meyers DM (2006) Lemurs of Madagascar, 2nd edn. Conservation International, Washington, DC, p 520

    Google Scholar 

  • Mutschler T (1999) Folivory in a small-bodied lemur: the nutrition of the Alaotran gentle lemur (Hapalemur griseus alaotrensis). In: Rasaminanana H, Rakotosamimanana B, Ganzhorn JU, Goodman SM (eds) New directions in lemur studies. Kluwer Academic/Plenum Publishing, New York, pp 221–239

    Google Scholar 

  • Mutschler T (2002) Alaotran gentle lemur: some aspects of its behavioral ecology. Evol Anthropol Suppl 1:101–104

    Google Scholar 

  • Mutschler T, Feistner ATC (1995) Conservation status and distribution of the Alaotran gentle lemur Hapalemur griseus alaotrensis. Oryx 29:267–274

    Article  Google Scholar 

  • Mutschler T, Tan CL (2003) Genus Hapalemur. In: Goodman SM, Benstead J (eds) Natural history of Madagascar. University of Chicago Press, Chicago, pp 1324–1329

    Google Scholar 

  • Mutschler T, Feistner ATC, Nievergelt CM (1998) Preliminary field data on group size, diet and activity in the Alaotran gentle lemur Hapalemur griseus alaotrensis. Folia Primatol 69:325–330

    Article  PubMed  Google Scholar 

  • Mutschler T, Randrianarisoa AJ, Feistner ATC (2001) Population status of the Alaotran gentle lemur Hapalemur griseus alaotrensis. Oryx 35:152–157

    Google Scholar 

  • Oates JF (1996) Habitat alteration, hunting and the conservation of folivorous primates in African forests. Austral J Ecol 21:1–9

    Article  Google 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. Ecological, physical and behavioural aspects. Cambridge University Press, Cambridge, pp 395–418

    Google Scholar 

  • Overdorff DJ, Strait SG, Telo A (1997) Seasonal variation in activity and diet in a small-bodied folivorous primate, Hapalemur griseus, in southeastern Madagascar. Am J Primatol 43:211–223

    Article  CAS  PubMed  Google Scholar 

  • Pollock JI (1986) A note on the ecology and behavior of Hapalemur griseus. Primate Conserv 7:97–100

    Google Scholar 

  • Powzyk JA, Mowry CB (2003) Dietary and feeding differences between sympatric Propithecus diadema diadema and Indri indri. Int J Primatol 24:1143–1162

    Article  Google Scholar 

  • Rabarivola C, Prosper P, Zaramody A, Andriaholinirina N, Hauwy M (2007) Cytogenetics and taxonomy of the genus Hapalemur. Lemur News 12:46–49

    Google Scholar 

  • Ralainasolo FB, Olivieri G, Waeber P, Mutschler T, Ratsimbazafy J, Lewis R, Durbin J (2007) Hapalemur alaotrensis: the biology of a wetland primate. In: Proceedings of the International Prosimian Conference, Durbin, South Africa

  • Rogers ME, Maisels F, Williamson EA, Fernandez M, Tutin CEG (1990) Gorilla diet in the Lopé Reserve, Gabon: a nutritional analysis. Oecologia 84:326–339

    Google Scholar 

  • Rothman JM, Dierenfeld ES, Molina DO, Shaw AV, Hintz HF, Pell AN (2006) Nutritional chemistry of foods eaten by gorillas in Bwindi Impenetrable National Park, Uganda. Am J Primatol 68:675–691

    Article  CAS  PubMed  Google Scholar 

  • Schaller GB, Jinchu H, Wenshi P, Jing Z (1985) The giant pandas of Wolong. University of Chicago Press, Chicago, p 318

    Google Scholar 

  • Tan CL (1998) Comparison of food passage time in three species of Hapalemur. Am J Phys Anthropol Suppl 26:215

    Google Scholar 

  • Tan CL (1999) Group composition, home range size, and diet of three sympatric bamboo lemur species (genus Hapalemur) in Ranomafana National Park, Madagascar. Int J Primatol 20:547–566

    Article  Google Scholar 

  • Tan CL (2006) Behavior and ecology of gentle lemurs (genus Hapalemur). In: Gould L, Sauther M (eds) Lemurs: ecology and adaptation. Springer, New York, pp 369–381

    Google Scholar 

  • Tattersall I (1987) Cathemeral activity in primates: a definition. Folia Primatol 49:200–202

    Article  Google Scholar 

  • Vincelette M, Dumouchel J, Giroux J, Heriarivo R (2007) The Tolagnaro (Fort Dauphin) region: a brief overview of the geology, hydrology, and climatology. 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 9–17

    Google Scholar 

  • Warter S, Tattersall I (1994) Update to the article “Cytogenetic study of a new subspecies of Hapalemur griseus”. Folia Primatol 63:170

    Article  Google Scholar 

  • Warter S, Randrianasolo G, Dutrillaux B, Rumpler Y (1987) Cytogenetic study of a new subspecies of Hapalemur griseus. Folia Primatol 48:50–55

    Article  Google Scholar 

Download references

Acknowledgments

We thank the Commission Tripartite of the Malagasy government, the Ministère de L’Environnement, des Eaux et Forêts, the University of Antananarivo, and CAFF/CORE for permission to conduct research, as well as the Malagasy Institute for the Conservation of Tropical Environments (MICET) for all of their logistical assistance. Financial support was provided partly by the Chester Zoo (North of England Zoological Society) and QMM. Special thanks to the QMM Environmental Team, especially Manon Vincelette, Jean-Baptiste Ramanamanjato, Johny Rabenantoandro, Faly Randriatafika, and Christophe Rambolamanana for all of their advice, support, and logistical help. We are grateful to Jörg Ganzhorn for all of his continuous support and scientific advice. Thank you to Simon Bearder, Anna Nekaris, and Vincent Nijman for their support and encouragement. Our sincere gratitude goes to Robertin Ravelomanantsoa and Abi Coleman for their assistance in the field, and to an anonymous reviewer for helpful comments.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Timothy M. Eppley.

About this article

Cite this article

Eppley, T.M., Verjans, E. & Donati, G. Coping with low-quality diets: a first account of the feeding ecology of the southern gentle lemur, Hapalemur meridionalis, in the Mandena littoral forest, southeast Madagascar. Primates 52, 7–13 (2011). https://doi.org/10.1007/s10329-010-0225-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10329-010-0225-3

Keywords

Navigation