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 L. rutenbergianus. 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.
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
Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267
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
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
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
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
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
Chivers DJ (1998) Measuring food intake in wild animals: primates. Proc Nutr Soc 57:321–332
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
Curtis DJ, Zaramody A, Martin RD (1999) Cathemerality in the mongoose lemur, Eulemur mongoz. Am J Primatol 47:279–298
Daniels HL (1984) Oxygen consumption in Lemur fulvus: deviation from the ideal model. J Mammal 65:584–592
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
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
Engqvist A, Richard A (1991) Diet as a possible determinant of cathemeral activity patterns in primates. Folia Primatol 57:169–172
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
Hanya G (2004) Diet of a Japanese macaque troop in the coniferous forest of Yakushima. Int J Primatol 25:55–69
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
Hasegawa K (1993) Nutritional analysis (in Japanese). Baifukan, Tokyo
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
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
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
Kenagy GJ (1973) Adaptations for leaf eating in the great basin kangaroo rat, Dipodomys microps. Oecologia 12:383–412
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
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
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
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
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
Nagy KA (1994) Seasonal water, energy and food use by free-living, arid-habitat mammals. Aust J Zool 42:55–63
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
Neter J, Wasserman W, Kutner MH (1990) Applied linear statistical models, 3rd edn. Irwin, Boston
Ossi K, Kamilar JM (2006) Environmental and phylogenetic correlates of Eulemur behavior and ecology (Primates: Lemuridae). Behav Ecol Sociobiol 61:53–64
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
Porter LJ (1989) Tannins. In: Dey PM, Harborne JB (eds) Methods in plant biochemistry, vol 1., Plant phenolicsAcademic Press, London, pp 389–419
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
Richard AF, Dewar RE (1991) Lemur ecology. Annu Rev Ecol Syst 22:145–175
Rothman JM, Chapman CA, Van Soest PJ (2012) Methods in primate nutritional ecology: a user’s guide. Int J Primatol 33:542–566
Sato H (2012) Diurnal resting in brown lemurs in a dry deciduous forest, northwestern Madagascar: implications for seasonal thermoregulation. Primates 53:255–263
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
Schmidt-Nielsen K (1997) Animal physiology: adaptation and environment (5th edit). Cambridge University Press, Cambridge
Shimada T (2006) Salivary proteins as a defense against dietary tannins. J Chem Ecol 32:1149–1163
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
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
Tarnaud L (2006) Cathemerality in the Mayotte brown lemur (Eulemur fulvus): seasonality and food quality. Folia Primatol 77:166–177
Tattersall I, Sussman RW (1998) ‘Little Brown Lemurs’ of northern Madagascar: phylogeny and ecological role in resource partitioning. Folia Primatol 69:379–388
Terborgh J (1983) Five new world primates: a study in comparative ecology. Princeton University Press, Princeton
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
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
Vasey N (2002) Niche separation in Varecia variegata rubra and Eulemur fulvus albifrons: II. intraspecific patterns. Am J Phys Anthropol 118:169–183
Wright PC (1999) Lemur traits and Madagascar ecology: coping with an island environment. Yrbk Phys Anthropol 42:31–72
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
Corresponding author
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10329-013-0392-0