Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-12-03T12:51:29.288Z Has data issue: false hasContentIssue false

Food selection in the black howler monkey following habitat disturbance: implications for the importance of mature leaves

Published online by Cambridge University Press:  13 February 2012

Alison M. Behie*
Affiliation:
School of Archaeology and Anthropology, College of Arts and Social Sciences, The Australian National University, Canberra, Australia, 0200
Mary S. M. Pavelka
Affiliation:
Department of Anthropology, University of Calgary, 2500 University Drive NW, Calgary, Alberta, Canada, T2N 1N4
*
1Corresponding author. Email: alison.behie@anu.edu.au

Abstract:

Primates commonly consume leaves that are high in protein but low in digestion-inhibiting fibre. Due to the fact that mature leaves do not meet these criteria, they are typically avoided and many leaf-eating primates select for leaves high in protein and low in fibre leading to the theory that food selection is based on protein maximization. However, feeding records for a population of black howler monkey (Alouatta pigra) in Monkey River, Belize, collected over a 5-y period, together with synchronous phenological data, indicate that this population does not meet the expectation and actually prefer mature leaves. This study aims to describe the nutritional composition of the food supply and investigate the possibility that, rather than to maximize protein ingestion, mature leaves are eaten to balance nutrient intake. Macronutrient analyses (moisture, lipids, protein, NDF, ADF and simple sugars) were conducted on a sample of 96 plant samples from 18 food species of this population of black howler. Results reported here show that mature leaves eaten by howlers in this forest contain sufficient protein to meet minimum metabolic requirements (range: 11.6–24%; mean: 16.4% ± 3.8%) and have significantly higher concentrations of simple sugars than young leaves (means of 7.2% ± 2.7% vs. 4.4% ± 2.3% respectively). Thus, it appears that mature leaf ingestion is likely serving to balance energy and protein intake. This result may be due to the disruptive effects of a hurricane in 2001 that resulted in a loss of 80% of the howler population, changed forest composition and may have affected plant chemistry. Despite this, the data reported here suggest that the accepted view that mature leaves are simply fallback foods for primates, eaten only in times of preferred food scarcity, may have to be revised.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

LITERATURE CITED

ALTMANN, J. 1974. Observational study of behaviour: sampling methods. Behaviour 69:227263.CrossRefGoogle Scholar
BALICK, M. J., NEE, M. H. & ATHA, D. E. 2000. Checklist of the vascular plants of Belize. Memoirs of the New York Botanical Garden 85:1246.Google Scholar
BELOVSKY, G. E. 1997. Optimal foraging and community structure: allometry of herbivore food selection and competition. Evolutionary Ecology 11:641672.CrossRefGoogle Scholar
CHAPMAN, C. A. & Chapman, L. J. 2002. Foraging challenges of red colobus monkeys: influence of nutrients and secondary compounds. Comparative Biochemistry and Physiology 133:861875.CrossRefGoogle ScholarPubMed
COLEY, P. D. 1983. Herbivory and defense characteristics of tree species in a lowland tropical forest. Ecological Monographs 53:209234.CrossRefGoogle Scholar
COLEY, P. D. 1987. Interspecific variation in plant anti-herbivore properties: the role of habitat quality and rate of disturbance. New Phytologist 106:251263.CrossRefGoogle Scholar
DASILVA, G. L. 1992. The western black-and-white colobus as a low energy strategist: activity budgets, energy expenditure and energy intake. Journal of Animal Ecology 61:7991.CrossRefGoogle Scholar
ESTRADA, A., ANZURES, A. & COATES-ESTRADA, R. 1999. Tropical rain forest fragmentation, howler monkeys (Alouatta palliata), and dung beetles at Los Tuxlas, Mexico. American Journal of Primatology 48:253262.3.0.CO;2-D>CrossRefGoogle ScholarPubMed
FASHING, P. J., DIERNFELD, E. S. & MOWRY, C. B. 2007. Influence of plant and soil chemistry on food selection, ranging patterns, and biomass of Colobus guereza in Kakamega Forest, Kenya. International Journal of Primatology 28:673703.CrossRefGoogle Scholar
FELTON, A. M., FELTON, A., WOOD, J. T., FOLEY, W. J., RAUBENHEIMER, D., WALLIS, I. R. & LINDENMAYER, D. B. 2009a. Nutritional ecology of Ateles chamek in lowland Bolivia: how macronutrient balancing influences food choices. International Journal of Primatology 30:675696.CrossRefGoogle Scholar
FELTON, A. M., FELTON, A., RAUBENHEIMER, D., SIMPSON, S. J., FOLEY, W. J., WOOD, J. T., WALLIS, I. R., LINDENMAYER, D. B. 2009b. Protein content of diets dictates energy intake of a free-ranging primate. Behavioral Ecology 20:685690.CrossRefGoogle Scholar
GANAS, J., ORTMANN, S. & ROBBINS, M. M. 2009. Food choices of the mountain gorilla in Bwindi Impenetrable National Park, Uganda: the influence of nutrients, phenolics and availability. Journal of Tropical Ecology 25:125134.CrossRefGoogle Scholar
GANZHORN, J. U. 1992. Leaf chemistry and the biomass of folivorous primates in tropical forests. Oecologia 91:540547.CrossRefGoogle ScholarPubMed
HALL, M. B., HOOVER, W. H., JENNINGS, J. P. & MILLER, T. K. 1999. A method for partitioning neutral detergent soluble carbohydrates. Journal of Science in Food Agriculture 79:20792086.3.0.CO;2-Z>CrossRefGoogle Scholar
HANLEY, T. A. 1982. The nutritional basis for food selection by ungulates. Journal of Range Management 35:146151.CrossRefGoogle Scholar
HUME, I. D. 1999. Marsupial nutrition. Cambridge University Press, Cambridge. 418 pp.Google Scholar
HUNTER, M. D. & FORKNER, R. E. 1999. Hurricane damage influences foliar polyphenolics and subsequent herbivory on surviving trees. Ecology 80:26762682.CrossRefGoogle Scholar
ILLIUS, A. W. & GORDON, I. J. 1992. Modeling the nutritional ecology of ungulate herbivores: evolution of body size and competitive interactions. Oecologia 89:428434.CrossRefGoogle ScholarPubMed
JANSON, C. H. 1988. Intraspecific food competition and primate social structure: a synthesis. Behaviour 105;117.CrossRefGoogle Scholar
JULLIOT, C. & SABATIER, D. 1993. Diet of the red howler monkey (Alouatta seniculus) in French Guiana. International Journal of Primatology 14:527550.CrossRefGoogle Scholar
KAVANAGH, R. P. & LAMBERT, M. J. 1990. Food selection by greater glider (Petauroides volans): is foliar nitrogen a determinant of habitat quality? Australian Wildlife Research 17:285299.CrossRefGoogle Scholar
LAMBERT, J. 2011. Primate nutritional ecology: Feeding biology and diet at ecological and evolutionary scales. Pp. 512522 in Campbell, C. J., Fuentes, A., Mackinnon, K. C., Panger, M. & Bearder, S. K. (eds.). Primates in perspective. Oxford University Press, New York.Google Scholar
LAWLER, I. R., FOLEY, W. J., ESCHLER, B. M., PASS, D. M. & HANDASYDE, K. 1998. Intraspecific variation in Eucalyptus secondary metabolites determines food intake by folivorous marsupials. Oecologia 116:160169.CrossRefGoogle ScholarPubMed
MILTON, K. 1979. Factors influencing leaf choice by howler monkeys: a test of some hypotheses of food selection by generalist herbivores. American Naturalist 114:362378.CrossRefGoogle Scholar
MILTON, K. 1980. The foraging strategy of howler monkeys: a study in primate economics. Columbia University Press, New York. 165 pp.Google Scholar
MILTON, K. 1982. Dietary quality and demographic regulation in a howler monkey population. Pp. 273289 in Leigh, E. G., Rand, A. S. & Windsor, D. M. (eds.). The ecology of a tropical forest. Smithsonian Institution Press, Washington, DC.Google Scholar
MILTON, K. 1998. Physiological ecology of howlers (Alouatta): energetic and digestive considerations and comparison with the Colobinae. International Journal of Primatology 19:513548.CrossRefGoogle Scholar
NAKAGAWA, N. 2003. Difference in food selection between patas monkeys (Erythrocebus patas) and tantalus monkeys (Cercopithecus aethiops tantalus) in Kala Maloue National Park, Cameroon, in relation to nutrient content. Primates 44:311.CrossRefGoogle ScholarPubMed
NEVES, A. M. A. & RYLANDS, A. B. 1991. Diet of a group of howling monkeys, Alouatta seniculus, in an isolated forest patch in Central Amazonia. A Primatologia no Brazil 3:263274.Google Scholar
NICHOLS-ORIANS, C. 1987. the acceptability of young and mature leaves to leaf-cutter ants varies with light environment. Biotropica 24:211214.CrossRefGoogle Scholar
OATES, J. F. 1978. Water-plant and soil consumption by Guereza monkeys (Colobus guereza): a relationship with minerals and toxins in the diet. Biotropica 10:241253.CrossRefGoogle Scholar
OATES, J. F., WATERMAN, P. G. & CHOO, G. M. 1980. Food selection by the South Indian leaf monkey (Presbytis johnii) in relation to leaf chemistry. Oecologia 45:4556.CrossRefGoogle ScholarPubMed
PAVELKA, M. S. M. & BEHIE, A. M. 2005. The effect of a hurricane on the food supply of black howlers (Alouatta pigra) in Southern Belize. Biotropica 37:102108.CrossRefGoogle Scholar
PAVELKA, M. S. M., BRUSSELERS, O. T., NOWAK, D. & BEHIE, A. M. 2003. Population reduction and social disorganization in Alouatta pigra following a hurricane. International Journal of Primatology 24:10371055.CrossRefGoogle Scholar
POLLOCK, C. J. & HOUSELY, T. L. 1985. Light-induced increase in sucrose phosphate synthetase activity in leaves of Lolium temulentum. Annals of Botany 55:593596.CrossRefGoogle Scholar
ROTHMAN, J. M., CHAPMAN, C. A. & PELL, N. A. 2008. Fibre-bound protein in gorilla diets: implications for estimating the intake of dietary protein by primates. American Journal of Primatology 70:690694.CrossRefGoogle Scholar
SILVER, S. C., OSTRO, L. E. T., YOUNG, C. P. & HORWICH, R. 1998. Feeding ecology of the black howler monkeys (Alouatta pigra) in Northern Belize. American Journal of Primatology 45:263279.3.0.CO;2-U>CrossRefGoogle ScholarPubMed
SILVER, S. C., OSTRO, L. E. T., YEAGER, C. P. & DIERENFELD, E. S. 2000. Phytochemical and mineral components of foods consumed by black howler monkeys (Alouatta pigra) at two sites in Belize. Zoo Biology 19:95109.3.0.CO;2-D>CrossRefGoogle Scholar
STANFORD, C. B. 1991. The diet of the capped langur (Presbytis pileata) in a moist deciduous forest in Bangladesh. International Journal of Primatology 12:199216.CrossRefGoogle Scholar
TORRES-CONTRERAS, H. & BOZINOVIC, F. 1997. Food selection in an herbivorous rodent: balancing nutrition with thermoregulation. Ecology 78:22302237.CrossRefGoogle Scholar
VAN SOEST, P. J. 1963. Use of detergents in the analysis of fibrous feeds: II. A rapid method for the determination of fibre and lignin. Journal of the Association of Official Agricultural Chemists 46:829835.Google Scholar
VEDDER, A. L. 1984. Movement patterns of a group of free-ranging mountain gorillas (Gorilla gorilla berengei) and relation to food availability. American Journal of Primatology. 7:7388.CrossRefGoogle Scholar
WASSERMAN, M. B. & CHAPMAN, C. A. 2003. Determinants of colobine monkey abundance: the importance of food energy, protein and fibre content. Journal of Animal Ecology 72:650659.CrossRefGoogle ScholarPubMed
WILLIG, M. R. & LACHER, T. E. 1991. Food selection of a tropical mammalian folivore in relation to leaf-nutrient content. Journal of Mammalogy 72:314321.CrossRefGoogle Scholar
YEAGER, C. P., SILVER, S. C. & DIERENFELD, E. S. 1997. Mineral and phytochemical influences on foliage selection by the proboscis monkey (Nasalis larvatus). American Journal of Primatology 41:117128.3.0.CO;2-#>CrossRefGoogle ScholarPubMed