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Leaf nutritional quality as a predictor of primate biomass: further evidence of an ecological anomaly within prosimian communities in Madagascar

Published online by Cambridge University Press:  13 February 2012

Bruno Simmen ,
Laurent Tarnaud  and
Annette Hladik
Bruno Simmen*
Affiliation:
CNRS/MNHN, UMR 7206, Département Hommes, Natures, Sociétés, 4 avenue du Petit Château, 91800, Brunoy, France
Laurent Tarnaud
Affiliation:
CNRS/MNHN, UMR 7206, Département Hommes, Natures, Sociétés, 4 avenue du Petit Château, 91800, Brunoy, France
Annette Hladik
Affiliation:
CNRS/MNHN, UMR 7206, Département Hommes, Natures, Sociétés, 4 avenue du Petit Château, 91800, Brunoy, France
*
1Corresponding author. Email: [email protected]
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Abstract:

The correlation between the biomass of forest primates and a chemical index of the average nutritional quality of leaves in tropical forests has been repeatedly documented since 1990. We tested the role played by protein : fibre on lemur biomass in a gallery forest in southern Madagascar. Plant species abundance was determined based on transect censuses. We calculated an average ratio of protein-to-fibre in leaves and an abundance-weighted ratio, i.e. the mean weighted by the basal area of tree species, to be compared with the figures available for other forest ecosystems in Madagascar and a number of anthropoid habitats. Lemur densities were evaluated through compilation of previous studies made from prior to 1975 and up until 2011 based on strip censuses and/or identification of all groups supplemented with new censuses. A high mean ratio of protein to fibre (> 0.4) supports high folivore biomass at 390 kg km−2 (reaching 630 kg km−2 in the closed-canopy forest area) compared with primate communities in other Malagasy forests (protein : fibre: < 0.5; folivore biomass: < 440 kg km−2), as predicted. However, the data corroborate the finding that the total biomass of lemur communities as well as the biomass of folivorous lemur species are low compared with those of African and Asian primate communities for a given protein : fibre ratio. Tree diversity and leaf production do not consistently explain this pattern. In contrast, the extinction of large folivorous lemurs during the past two millennia presumably allowed too little time for smaller-sized species to evolve equally effective morphological and physiological specializations for processing a large range of fibrous foods.

Keywords

gallery forestleaf chemistrylemur abundanceprotein : fibre ratiospecies extinction
Type
Research Article
Information
Journal of Tropical Ecology , Volume 28 , Issue 2 , March 2012 , pp. 141 - 151
Copyright
Copyright © Cambridge University Press 2012

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References

LITERATURE CITED

ABRAHAM, J. P., BENJA, R., RANDRIANASOLO, M., GANZHORN, J. U., JEANNODA, V. & LEIGH, E. G. 1996. Tree diversity on small plots in Madagascar: a preliminary review. Revue d'Ecologie (Terre et Vie) 51:93–116.Google Scholar
BLUMENFELD-JONES, K., RANDRIAMBOAVONJY, T. M., WILLIAMS, G., MERTL-MILLHOLLEN, A. S., PINKUS, S. & RASAMIMANANA, H. 2006. Tamarind recruitment and long-term stability in the gallery forest at Berenty, Madagascar. Pp. 69–85 in Jolly, A., Sussman, R. W., Koyama, N. & Rasamimanana, H. (eds.). Ringtailed lemur biology. Springer, Chicago.CrossRefGoogle Scholar
BURNEY, D. A., BURNEY, L. P., GODFREY, L. R., JUNGERS, W. L., GOODMAN, S. M., WRIGHT, H. T. & JULL, A. J. T. 2004. A chronology for late prehistoric Madagascar. Journal of Human Evolution 47:25–63.CrossRefGoogle ScholarPubMed
CAMPBELL, J. L., EISEMANN, J. H., GLANDER, K. E. & CRISSEY, S. D. 1999. Intake, digestibility, and passage of a commercially designed diet by two Propithecus species. American Journal of Primatology 48:237–246.3.0.CO;2-V>CrossRefGoogle ScholarPubMed
CHAPMAN, C. A. & CHAPMAN, L. J. 2002. Foraging challenges of red colobus monkeys: influence of nutrients and secondary compounds. Comparative Biochemistry and Physiology Part A 133:861–875.CrossRefGoogle ScholarPubMed
CHAPMAN, C. A., CHAPMAN, L. J., BJORNDAL, K. A. & ONDERDONK, D. A. 2002. Application of protein-to-fibre ratios to predict colobine abundance on different spatial scales. International Journal of Primatology 23:283–310.CrossRefGoogle Scholar
CHAPMAN, C. A., CHAPMAN, L. J., NAUGHTON-TREVES, L., LAWES, M. J. & MCDOWELL, L. R. 2004. Predicting folivorous primate abundance: validation of a nutritional model. American Journal of Primatology 62:55–69.CrossRefGoogle ScholarPubMed
CHAPMAN, C. A., STRUHSAKER, T. T. & LAMBERT, J. E. 2005. Thirty years of research in Kibale National Park, Uganda, reveals a complex picture for conservation. International Journal of Primatology 26:539–555.CrossRefGoogle Scholar
CHARLES-DOMINIQUE, P. & HLADIK, C. M. 1971. Le lépilemur du sud de Madagascar: écologie, alimentation et vie sociale. Revue d'Ecologie (Terre et Vie) 25:3–66.Google Scholar
CROWLEY, B. E., GODFREY, L. R. & IRWIN, M. T. 2011. A glance to the past: subfossils, stable isotopes, seed dispersal, and lemur species loss in Southern Madagascar. American Journal of Primatology 75:25–37.CrossRefGoogle Scholar
DAMMHAHN, M. & KAPPELER, P. M. 2010. Scramble or contest competition over food in solitarily foraging mouse lemurs (Microcebus spp.): new insights from stable isotopes. American Journal of Physical Anthropology 141:181–189.CrossRefGoogle ScholarPubMed
DASILVA, G. 1994. Diet of Colobus polykomos on Tiwai Island: selection of food in relation to its seasonal abundance and nutritional quality. International Journal of Primatology 15:655–680.CrossRefGoogle Scholar
EDWARDS, M. S. & ULLREY, D. E. 1999. Effect of dietary fibre concentration on apparent digestibility and digesta passage in non-human primates. II. Hindgut- and foregut-fermenting folivores. Zoo Biology 18:537–549.3.0.CO;2-F>CrossRefGoogle Scholar
FLEAGLE, J. G. & REED, K. E. 1996. Comparing primate communities: a multivariate approach. Journal of Human Evolution 30:489–510.CrossRefGoogle Scholar
GANZHORN, J. U. 1988. Food partitioning among Malagasy Primates. Oecologia 75:436–450.CrossRefGoogle ScholarPubMed
GANZHORN, J. U. 1992. Leaf chemistry and the biomass of folivorous primates in tropical forests. Test of a hypothesis. Oecologia 91:540–547.CrossRefGoogle ScholarPubMed
GANZHORN, J. U. 1995. Low-level forest disturbance effects on primary production, leaf chemistry, and lemur populations. Ecology 76:2084–2096.CrossRefGoogle Scholar
GANZHORN, J. U., MALCOMBER, S., ANDRIANANTOANINA, O. & GOODMAN, S. 1997. Habitat characteristics and lemur species richness in Madagascar. Biotropica 29:331–343.CrossRefGoogle Scholar
GANZHORN, J. U., ARRIGO-NELSON, S., BOINSKI, S., BOLLEN, A., CARRAI, V., DERBY, A., DONATI, G., KOENIG, A., KOWALEWSKI, M., LAHANN, P., NORSCIA, I., POLOWINSKY, S. Y., SCHWITZER, C., STEVENSON, P. R., TALEBI, M. G., TAN, C., VOGEL, E. R. & WRIGHT, P. G. 2009. Possible fruit protein effects on primate communities in Madagascar and the Neotropics. PLoS One 4: e8253.CrossRefGoogle ScholarPubMed
GARTLAN, J. S., MCKEY, D. B., WATERMAN, P. G., MBI, C. N. & STRUHSAKER, T. T. 1980. A comparative study of the phytochemistry of two African rain forests. Biochemical Systematics and Ecology 8:401–422.CrossRefGoogle Scholar
GODFREY, L. R. & IRWIN, M. T. 2007. The evolution of extinction risk: past and present anthropogenic impacts on the primate communities of Madagascar. Folia Primatologica 78:405–419.CrossRefGoogle ScholarPubMed
HLADIK, A. 1980. The dry forest of the west coast of Madagascar: climate, phenology, and food available for Prosimians. Pp. 3–40 in Charles-Dominique, P., Cooper, H. M., Hladik, A., Hladik, C. M., Pagès, E., Pariente, G. F., Petter-Rousseaux, A., Petter, J.-J. & Schilling, A. (eds.). Nocturnal malagasy primates. Ecology, physiology, and behavior. Academic Press, New York.Google Scholar
HLADIK, C. M. 1981. Diet and the evolution of feeding strategies among forest primates. Pp. 215–254 in Harding, R. S. O. & Teleki, G. (eds.). Omnivorous primates. Gathering and hunting in human evolution. Columbia University Press, New York.CrossRefGoogle Scholar
HLADIK, C. M., CHARLES-DOMINIQUE, P. & PETTER, J.-J. 1980. Feeding strategies of five nocturnal prosimians in the dry forest of the West coast of Madagascar. Pp. 41–73 in Charles-Dominique, P., Cooper, H. M., Hladik, A., Hladik, C. M., Pagès, E., Pariente, G. F., Petter-Rousseaux, A., Petter, J.-J. & Schilling, A. (eds.). Nocturnal malagasy primates. Ecology, physiology, and behavior. Academic Press, New York.Google Scholar
HLADIK, C. M., PINTE, M. & SIMMEN, B. 1998. Les densités de population des prosimiens nocturnes du sud de Madagascar varient-elles à long terme dans les réserves forestières accessibles au public. Revue d'Ecologie (Terre Vie) 53:181–185.Google Scholar
JOLLY, A., GUSTAFSON, H., OLIVER, W. L. R. & O'CONNOR, S. M. 1982. Propithecus verreauxi population and ranging at Berenty, Madagascar, 1975 and 1980. Folia Primatologica 39:124–144.CrossRefGoogle ScholarPubMed
JOLLY, A., DOBSON, A., RASAMIMANANA, H., WALKER, J., O'CONNOR, S., SOLBERG, M. & PEREL, V. 2002. Demography of Lemur catta at Berenty Reserve, Madagascar: effects of troop size, habitat and rainfall. International Journal of Primatology 23:327–353.CrossRefGoogle Scholar
JOLLY, A., RASAMIMANANA, H., BRAUN, M., DUBOVICK, T., MILLS, C. & WILLIAMS, G. 2006. Territory as bet-hedging: Lemur catta in a rich forest and an erratic climate. Pp. 187–207 in Jolly, A., Sussman, R. W., Koyama, N. & Rasamimanana, H. (eds.). Ringtailed lemur biology. Springer, Chicago.CrossRefGoogle Scholar
KAMATA, N., IGARASHI, Y. & OHARA, S. 1996. Induced response of the Siebold's beech (Fagus crenata Biume) to manual defoliation. Journal of Forest Research 1:1–7.CrossRefGoogle Scholar
KOECHLIN, K., GUILLAUMET, J. L. & MORAT, P. 1974. Flore et végétation de Madagascar. Cramer, Vaduz. 687 pp.Google Scholar
LEIGH, E. G., HLADIK, A., HLADIK, C. M. & JOLLY, A. 2007. The biogeography of large islands, or how does the size of the ecological theater affect the evolutionary play? Revue d'Ecologie (Terre Vie) 62:105–168.Google Scholar
MILTON, K. 1979. Factors influencing leaf choice by howler monkeys: a test of some hypothesis of food selection by generalist herbivores. American Naturalist 114:362–378.CrossRefGoogle Scholar
MITTERMEIER, R. A., GANZHORN, J. U., KONSTANT, W. R., GLANDER, K., TATTERSALL, I., GROVES, C. P., RYLANDS, A. B., HAPKE, A., RATSIMBAZAFY, J., MAYOR, M. I., LOUIS, E. E., RUMPLER, Y., SCHWITZER, C. & RASOLOARISON, R. M. 2008. Lemur diversity in Madagascar. International Journal of Primatology 29:1607–1656.CrossRefGoogle Scholar
MULCHINSKI, M. N., GODFREY, L. R., MULDOON, K. M. & TONGASOA, L. 2010. Evidence for dietary niche separation based on infraorbital foramen size variation among subfossil lemurs. Folia Primatologica 81:330–345.Google Scholar
NIJBOER, J. 2006. Fibre intake and faeces quality in leaf-eating primates. Ph.D. thesis. Utrecht University, the Netherlands.Google Scholar
NORSCIA, I. & PALAGI, E. 2008. Berenty 2006: census of Propithecus verreauxi and possible evidence of population stress. International Journal of Primatology 29;1099–1115.CrossRefGoogle Scholar
OATES, J. F., WHITESIDES, G. H., DAVIES, A. G., WATERMAN, P. G., GREEN, S. M., DASILVA, G. L. & MOLE, S. 1990. Determinants of variation in tropical forest primate biomass: new evidence from West Africa. Ecology 71:328–343.CrossRefGoogle Scholar
O'CONNOR, S. 1987. The effect of human impact on vegetation and the consequences to primates on two riverine forests, southern Madagascar. Ph.D. thesis, Cambridge University, Cambridge.Google Scholar
O'CONNOR, S. 1988. Une revue des différences écologiques entre deux forêts galeries, une protégée et une dégradée, au centre sud de Madagascar. Pp. 216–227 in Rakotovao, L., Barre, V. & Sayer, J. (eds.). L'équilibre des écosystèmes forestiers à Madagascar. Actes d'un séminaire international. IUCN, Gland.Google Scholar
ODUM, E. P. 1959. Fundamentals of ecology. (Second edition). W. B. Saunders, Philadelphia. 546 pp.Google Scholar
PERRET, M., AUJARD, F. & VANNIER, G. 1998. Influence of daylength on metabolic rate and daily water loss in the male prosimian primate Microcebus murinus. Comparative Biochemistry and Physiology, part A 119:981–989.CrossRefGoogle ScholarPubMed
PICHON, C., RAMANAMISATA, R., TARNAUD, L., BAYART, F., HLADIK, A., HLADIK, C. M. & SIMMEN, B. 2010. Feeding ecology of the crowned sifaka (Propithecus coronatus) in a coastal dry forest in northwest Madagascar (SFUM, Antrema). Lemur News 15:43–47.Google Scholar
PINKUS, S., SMITH, J. N. M. & JOLLY, A. 2006. Feeding competition between introduced Eulemur fulvus and native Lemur catta during the birth season at Berenty reserve, Southern Madagascar. Pp. 119–140 in Jolly, A., Sussman, R. W., Koyama, N. & Rasamimanana, H. (eds.). Ringtailed lemur biology. Springer, Chicago.CrossRefGoogle Scholar
POWZYK, J. A. & MOWRY, C. B. 2003. Dietary and feeding differences between sympatric Propithecus diadema diadema and Indri indri. International Journal of Primatology 24;1143–1162.CrossRefGoogle Scholar
RAICHLEN, D. A., GORDON, A. D. & SECHREST, W. 2011. Bioenergetic constraints on primate abundance. International Journal of Primatology 32:118–133.CrossRefGoogle Scholar
RANAIVOSON, T. N., RAZAKANIRINA, H., RAJERIARISON, C., HLADIK, A. & ROGER, E. (in press). Structure de l'habitat et disponibilités alimentaires de Propithecus coronatus dans la forêt sèche de Badrala (Station Forestière à Usages Multiples d'Antrema, Madagascar): application de la méthode des tris de litière et interprétations des adaptations des espèces arborescentes et lianescentes. Proceedings of the 19th congress of the AETFAT, April 25–30. Antananarivo, Madagascar.Google Scholar
RASAMIMANANA, H. R. & RAFIDINARIVO, E. 1993. Feeding behavior of Lemur catta females in relation to their physiological state. Pp. 123–133 in Kappeler, P. M. & Ganzhorn, J. U. (eds.). Lemur social systems and their ecological basis. Plenum, New York.CrossRefGoogle Scholar
RICHARD, A. 1978. Behavioural variation. Bucknell University Press, Lewisburg. 213 pp.Google Scholar
RICHARD, A. F. & NICOLL, M. E. 1987. Female social dominance and basal metabolism in a Malagasy primate, Propithecus verreauxi. American Journal of Primatology 12:309–314.CrossRefGoogle Scholar
RICHARD, A. F., DEWAR, R. E., SCHWARTZ, M. & RATSIRARSON, J. 2000. Mass change, environmental variability and female fertility in wild Propithecus verreauxi. Journal of Human Evolution 39:381–391.CrossRefGoogle ScholarPubMed
ROSS, C. 1992. Basal metabolic rate, body weight and diet in primates: an evaluation of the evidence. Folia Primatologica 58:7–23.CrossRefGoogle ScholarPubMed
SIMMEN, B., HLADIK, A., RAMASIARISOA, P. L., IACONELLI, S. & HLADIK, C. M. 1999. Taste discrimination in lemurs and other primates, and the relationships to distribution of plant allelochemicals in different habitats of Madagascar. Pp. 201–219 in Rakotosamimanana, B., Rasamimanana, H., Ganzhorn, J. U. & Goodman, S. J. (eds.). New directions in lemur studies. Kluwer Academic/Plenum Publishers, New York.CrossRefGoogle Scholar
SIMMEN, B., HLADIK, A. & RAMASIARISOA, P. L. 2003. Food intake and dietary overlap in native Lemur catta and Propithecus verreauxi and introduced Eulemur fulvus at Berenty, Southern Madagascar. International Journal of Primatology 24:949–968.CrossRefGoogle Scholar
SIMMEN, B., BAYART, F., RASAMIMANANA, H., ZAHARIEV, A., BLANC, S. & PASQUET, P. 2010. Total energy expenditure and body composition in two free-living sympatric lemurs. PLoS ONE 5:e9860.CrossRefGoogle ScholarPubMed
VAN SCHAIK, C. P. & KAPPELER, P. M. 1996. The social system of gregarious lemurs: lack of convergence with anthropoids due to evolutionary disequilibrium? Ethology 102:915–941.CrossRefGoogle Scholar
VAN SOEST, P. J., ROBERTSON, J. B. & LEWIS, B. A. 1991. Methods for dietary fibre, neutral detergent fibre, and non starch polysaccharides in relation to animal nutrition. Journal of Dairy Science 74:3583–3597.CrossRefGoogle ScholarPubMed
WANG, D., HECKATHORN, S. A., WANG, X. & PHILPOTT, S. M. 2011. A meta-analysis of plant physiological and growth responses to temperature and elevated CO2. Oecologia DOI 10.1007/s00442011-21720.Google Scholar
WATERMAN, P. G. & KOOL, K. M. 1994. Colobine food selection and plant chemistry. Pp. 251–284 in Davies, A. G. & Oates, J. F. (eds.). Colobine monkeys: their ecology, behaviour and evolution. Cambridge University Press, Cambridge.Google Scholar
WRIGHT, P. C. 1999. Lemur traits and Madagascar ecology: coping with an island environment. Yearbook of Physical Anthropology 42:31–72.3.0.CO;2-0>CrossRefGoogle Scholar
YAMASHITA, N. 2008. Chemical properties of the diets of two lemur species in Southwestern Madagascar. International Journal of Primatology 29;339–364.CrossRefGoogle Scholar