Skip to main content
Log in

Dietary modification by common brown lemurs (Eulemur fulvus) during seasonal drought conditions in western Madagascar

  • Original Article
  • Published:
Primates Aims and scope Submit manuscript

Abstract

Primates often modify dietary composition in relation to seasonal changes in food availability or climate conditions. We studied the feeding patterns of a troop of common brown lemurs (Eulemur fulvus), a semi-frugivorous strepsirhine, in a dry forest in northwestern Madagascar. To understand the mechanism of dietary modification, we recorded daily feeding times of diet items during 101 full-day observations over 1 year, and then conducted a linear model analysis to examine the effects of fruiting tree density in the forest, daily ambient temperature, and weekly rainfall (index of water retained in the forest) on the lemurs' daily feeding time. The lemurs spent dramatically more time on leaf-eating as well as total feeding time, and less time on fruit-eating during the late dry season (total 152 min/day, frugivory 56 min/day, folivory 77 min/day), as compared with other seasons when the diet was highly frugivorous (total 96 min/day, frugivory 81 min/day, folivory 8 min/day). Folivory increased as temperatures rose under the condition of low weekly rainfall, whereas frugivory was unrelated to fruiting tree density. Most (97.4 %) diurnal folivory during the late dry season was spent consuming Lissochilus rutenbergianus, chewing the succulent leaves and licking the juice. Because the nutritional analysis showed that L. rutenbergianus is rich in water (80.1 % of fresh weight) but poor in protein and nonstructural carbohydrates, its increased use was probably for rehydration. We conducted 13 full-night observations, because brown lemurs increase nocturnal activities during the dry season. At nighttime, the lemurs tended to spend more time eating fruit in the late dry season (32 min/night) than in the early dry season (14 min/night), and never consumed Lrutenbergianus. Fruits rich in nonstructural carbohydrates can be energy sources for Eulemur. They likely engaged in additional nocturnal frugivory for energy compensation. Brown lemurs have a flexible strategy of modifying their diet and feeding activities to cope with environmental stresses.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Agetsuma N (1995) Dietary selection by Yakushima macaques (Macaca fuscata yakui): the influence of food availability and temperature. Int J Primatol 16:611–627

    Article  Google Scholar 

  • Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267

    Article  PubMed  CAS  Google Scholar 

  • Andrews JR, Birkinshaw CR (1998) A comparison between the daytime and night-time diet, activity and feeding height of the black lemur, Eulemur macaco (Primates: Lemuridae), in Lokobe Forest, Madagascar. Folia Primatol 69:175–182

    Article  Google Scholar 

  • Budnitz N, Dainis K (1975) Lemur catta, ecology and behavior. In: Tattersall I, Sussman RW (eds) Lemur biology. Plenum Press, New York, pp 219–235

    Chapter  Google Scholar 

  • Campbell JL, Williams CV, Eisemann JH (2004) Use of total dietary fiber across four lemur species (Propithecus verrauxi coquereli, Hapalemur griseus griseus, Varecia variegata, and Eulemur fulvus): does fiber type affect digestive efficiency? Am J Primatol 64:323–335

    Article  PubMed  CAS  Google Scholar 

  • Camperio Ciani A, Martinoli L, Capiluppi C, Arahou M, Mouna M (2001) Effects of water availability and habitat quality on bark-stripping behavior in Barbary macaques. Conserv Biol 15:259–265

    Article  Google Scholar 

  • Charles-Dominique P, Bearder SK (1979) Field studies of lorisoid behavior: methodological aspects. In: Doyle GA, Martin RD (eds) The study of prosimian behavior. Academic Press, New York, pp 567–629

    Google Scholar 

  • Chivers DJ (1998) Measuring food intake in wild animals: primates. Proc Nutr Soc 57:321–332

    Article  PubMed  CAS  Google Scholar 

  • Curtis DJ (2004) Diet and nutrition in wild mongoose lemur (Eulemur mongoz) and their implications for the evolution of female dominance and small group size in lemurs. Am J Phys Anthropol 124:234–247

    Article  PubMed  Google Scholar 

  • Curtis DJ, Zaramody A, Martin RD (1999) Cathemerality in the mongoose lemur, Eulemur mongoz. Am J Primatol 47:279–298

    Article  PubMed  CAS  Google Scholar 

  • Daniels HL (1984) Oxygen consumption in Lemur fulvus: deviation from the ideal model. J Mammal 65:584–592

    Article  Google Scholar 

  • Donati G, Bollen A, Borgognini Tarli SM, Ganzhorn JU (2007) Feeding over the 24-h cycle: dietary flexibility of cathemeral collared lemurs (Eulemur collaris). Behav Ecol Sociobiol 61:1237–1251

    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 

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

    Article  PubMed  CAS  Google Scholar 

  • Fietz J, Dausmann KH (2006) Big is beautiful: fat storage and hibernation as a strategy to cope with marked seasonality in the fat-tailed dwarf lemur (Cheirogaleus medius). In: Gould L, Sauther ML (eds) Lemurs: ecology and adaptation. Springer, New York, pp 97–110

    Chapter  Google Scholar 

  • Hanya G (2004) Diet of a Japanese macaque troop in the coniferous forest of Yakushima. Int J Primatol 25:55–69

    Article  Google Scholar 

  • Hanya G, Kiyono M, Takafumi H, Tsujino R, Agetsuma N (2007) Mature leaf selection of Japanese macaques: effects of availability and chemical content. J Zool 273:140–147

    Article  Google Scholar 

  • Hasegawa K (1993) Nutritional analysis (in Japanese). Baifukan, Tokyo

    Google Scholar 

  • Hemingway CA, Bynum N (2005) The influence of seasonality on primate diet and ranging. In: Brockman DK, van Schaik CP (eds) Seasonality in primates: studies of living and extinct human and non-human primates. Cambridge University Press, Cambridge, pp 57–104

    Chapter  Google Scholar 

  • Jury MR (2003) The climate of Madagascar. In: Goodman SM, Benstead JP (eds) The natural history of Madagascar. The University of Chicago Press, Chicago, pp 75–87

    Google Scholar 

  • Kappeler PM, Erkert HG (2003) On the move around the clock: correlates and determinants of cathemeral activity in wild red-fronted lemurs (Eulemur fulvus rufus). Behav Ecol Sociobiol 54:359–369

    Article  Google Scholar 

  • Kenagy GJ (1973) Adaptations for leaf eating in the great basin kangaroo rat, Dipodomys microps. Oecologia 12:383–412

    Article  Google Scholar 

  • Lambert JE, Chapmam CA, Wrangham RW, Conklin-Brittain NL (2004) Hardness of cercopithecine foods: implications for the critical function of enamel thickness in exploiting fallback foods. Am J Phys Anthropol 125:363–368

    Article  PubMed  Google Scholar 

  • Marshall AJ, Leighton M (2006) How does food availability limit the population density of white-bearded gibbons? In: Hohmann G, Robbins MM, Boesch C (eds) Feeding ecology of the apes and other primates. Cambridge University Press, Cambridge, pp 311–333

    Google Scholar 

  • Mertl-Millhollen AS, Rambeloarivony H, Miles W, Kaiser VA, Gray L, Dorn LT, Williams G, Rasamimanana H (2006) The influence of tamarind tree quality and quantity on Lemur catta behavior. In: Jolly A, Sussman RW, Koyama N, Rasamimanana H (eds) Ringtailed lemur biology: Lemur catta in Madagascar. Springer, New York, pp 102–118

    Chapter  Google Scholar 

  • Mitchell D, Fuller A, Maloney SK (2009) Homeothermy and primate bipedalism: is water shortage or solar radiation the main threat to baboon (Papio hamadryas) homeothermy? J Hum Evol 56:439–446

    Article  PubMed  Google Scholar 

  • Mittermeier RA, Louis EE Jr, Richardson M, Schwitzer C, Langrand O, Rylands AB, Hawkins F, Rajaobelina S, Ratsimbazafy J, Rasoloarison R, Roos C, Kappeler PM, Mackinnon J (2010) Lemurs of Madagascar, 3rd edn. Conservation International, Washington DC

    Google Scholar 

  • Nagy KA (1994) Seasonal water, energy and food use by free-living, arid-habitat mammals. Aust J Zool 42:55–63

    Article  Google Scholar 

  • Nakayama T, Hori T, Nagasaka T, Tokura T, Tadaki E (1971) Thermal and metabolic responses in the Japanese monkey at temperature of 5–38°C. J Appl Physiol 31:332–337

    PubMed  CAS  Google Scholar 

  • Neter J, Wasserman W, Kutner MH (1990) Applied linear statistical models, 3rd edn. Irwin, Boston

    Google Scholar 

  • Ossi K, Kamilar JM (2006) Environmental and phylogenetic correlates of Eulemur behavior and ecology (Primates: Lemuridae). Behav Ecol Sociobiol 61:53–64

    Article  Google Scholar 

  • Overdorff DJ (1993) Similarities, differences, and seasonal patterns in the diets of Eulemur rubriventer and Eulemur fulvus rufus in the Ranomafana National Park, Madagascar. Int J Primatol 14:721–753

    Article  Google Scholar 

  • Porter LJ (1989) Tannins. In: Dey PM, Harborne JB (eds) Methods in plant biochemistry, vol 1., Plant phenolicsAcademic Press, London, pp 389–419

    Google Scholar 

  • Rasmussen MA (1999) Ecological influences on activity cycle in two cathemeral primates, the mongoose lemur (Eulemur mongoz) and the common brown lemur (Eulemur fulvus fulvus) (Ph.D. thesis). Duke University, Durham

  • Rautio P, Bergvall UA, Karonen M, Salminen JP (2007) Bitter problems in ecological feeding experiments: commercial tannin preparations and common methods for tannin quantifications. Biochem Syst Ecol 35:257–262

    Article  CAS  Google Scholar 

  • Richard AF, Dewar RE (1991) Lemur ecology. Annu Rev Ecol Syst 22:145–175

    Article  Google Scholar 

  • Rothman JM, Chapman CA, Van Soest PJ (2012) Methods in primate nutritional ecology: a user’s guide. Int J Primatol 33:542–566

    Article  Google Scholar 

  • Sato H (2012) Diurnal resting in brown lemurs in a dry deciduous forest, northwestern Madagascar: implications for seasonal thermoregulation. Primates 53:255–263

    Article  PubMed  Google Scholar 

  • Sato H (2013) Seasonal fruiting and seed dispersal by the brown lemur in a tropical dry forest, north-western Madagascar. J Trop Ecol 29:61–69

    Article  Google Scholar 

  • Schmidt-Nielsen K (1997) Animal physiology: adaptation and environment (5th edit). Cambridge University Press, Cambridge

    Google Scholar 

  • Shimada T (2006) Salivary proteins as a defense against dietary tannins. J Chem Ecol 32:1149–1163

    Article  PubMed  CAS  Google Scholar 

  • Sorg J-P, Rohner U (1996) Climate and phenology of the dry deciduous forest at Kirindy. In: Ganzhorn JU, Sorg J-P (eds) Ecology and economy of a tropical dry forest in Madagascar (Primate Report 46). German Primate Center, Göttingen, pp 57–80

    Google Scholar 

  • Sussman RW (1977) Feeding behaviour of Lemur catta and Lemur fulvus. In: Clutton-Brock TH (ed) Primate ecology: studies of feeding and ranging behaviour in lemurs, monkeys, and apes. Academic Press, New York, pp 1–36

    Google Scholar 

  • Tarnaud L (2006) Cathemerality in the Mayotte brown lemur (Eulemur fulvus): seasonality and food quality. Folia Primatol 77:166–177

    Article  PubMed  Google Scholar 

  • Tattersall I, Sussman RW (1998) ‘Little Brown Lemurs’ of northern Madagascar: phylogeny and ecological role in resource partitioning. Folia Primatol 69:379–388

    Article  Google Scholar 

  • Terborgh J (1983) Five new world primates: a study in comparative ecology. Princeton University Press, Princeton

    Google Scholar 

  • Tsuji Y (2010) Regional, temporal, and inter-individual variation in the feeding ecology of Japanese macaques. In: Nakagawa N, Nakamichi M, Sugiura H (eds) The Japanese macaques. Springer, Tokyo, pp 95–123

    Google Scholar 

  • van Soest PJ, Robertson JB, Lewis BA (1991) Methods for dietary fiber, neutral detergent fiber, and non-starch polysaccharides in relation to animal nutrition. J Dairy Sci 74:3583–3597

    Article  PubMed  Google Scholar 

  • Vasey N (2002) Niche separation in Varecia variegata rubra and Eulemur fulvus albifrons: II. intraspecific patterns. Am J Phys Anthropol 118:169–183

    Article  PubMed  Google Scholar 

  • Wright PC (1999) Lemur traits and Madagascar ecology: coping with an island environment. Yrbk Phys Anthropol 42:31–72

    Article  Google Scholar 

Download references

Acknowledgments

The authors are grateful to A. Mori, F. Rakotondraparany, B. Razafimahatratra, T. M. Randriamboavonjy, members of the research team, and all of the staff at Ankarafantsika National Park for their support in carrying out field research, to Durrell Wildlife Cheloniean Breeding Center for providing the climatic data, to J. Rakotoroa, Tsiahifika, A. Rakotovoavy and M. Rasolofomanana for their help with vegetation surveys, to the staff of Tsimbazaza Botanical and Zoological Park and R. H. Robuste for identifying the plant specimens, to G. idani for his support in conducting the nutritional analysis, and to G. Yamakoshi, A. Mori, and N. Nakagawa for helpful comments on the manuscript. This work was partially supported by the MEXT Grants-in-Aid for Scientific Research (Nos. 17405008, 18681036, 21-3399, 21405007, 24405008, 25870344) from the Japan Society for the Promotion of Science, and the Cooperation Research Programs of Primate Research Institute and Wildlife Research Center, Kyoto University.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hiroki Sato.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Online Resource 1 Common brown lemurs (Eulemur fulvus) chewing mature leaves of Lissochilus rutenbergianus (Shooting date: September 22, 2007).

Supplementary material 1 (MPG 8500 kb)

About this article

Cite this article

Sato, H., Ichino, S. & Hanya, G. Dietary modification by common brown lemurs (Eulemur fulvus) during seasonal drought conditions in western Madagascar. Primates 55, 219–230 (2014). https://doi.org/10.1007/s10329-013-0392-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10329-013-0392-0

Keywords

Navigation