Journal of Chemical Ecology

, Volume 33, Issue 6, pp 1186–1196 | Cite as

Feeding Selectivity by Mantled Howler Monkeys (Alouatta palliata) in Relation to Leaf Secondary Chemistry in Hymenaea courbaril

  • B. J. Welker
  • W. König
  • M. Pietsch
  • R. P. Adams


This study is a quantitative examination of primate feeding selectivity in relation to secondary chemistry within a single plant species, Hymenaea courbaril. It provides the first evidence that sesquiterpenes may act as feeding deterrents in mantled howler monkeys. A free-ranging group of mantled howler monkeys at the study site of Sector Santa Rosa, Area de Conservacion Guanacaste, Costa Rica were observed for the 2-month period of H. courbaril leaf flush in 1999. Tree characteristic data and leaf specimens were collected from 22 focal trees. Gas chromatography and mass spectrometry were used to estimate relative percentages of sesquiterpenes in leaf specimens. The monkeys fed only on the youngest leaves and only from particular trees. Whereas leaf stage selectivity was likely governed by tannin content and structural carbohydrates in younger and older leaf stages, respectively, differential tree use may be related to variability in sesquiterpene content. There is evidence that α-copaene may have played a role in interindividual tree use, and that cyperene may also be implicated. However, there is no reported evidence of antiherbivore activity for cyperene.


Primates Howler monkeys Feeding selectivity Secondary chemistry Sesquiterpenes 



BJW thanks the administration and staff of Sector Santa Rosa for their assistance and permission to conduct fieldwork. Assistance with plant specimen analyses was provided by Paul Kostyniak, Jean Langenheim, Claudia Paul, and Annagret Meiners. Ken Glander and Linda Fedigan provided advice, guidance, and animal tagging. Special thanks to the following field assistants: Bertha Fearon, Graeme Hunt, Alex Perez, and Tanya Smith. Carol Berman provided guidance in the preparation of Welker’s dissertation of which this study is a part. Financial support was received from NSF, Sigma Xi, Graduate Student Association of SUNY Buffalo, the Trimble Corp., and various grants from SUNY Geneseo.


  1. Agelopoulos, N. G., Hooper, A. M., Maniar, S. P., Pickett, J. A., and Wadhams, L. J. 1999. A novel approach for isolation of volatile chemicals released by individual leaves of a plant in situ. J. Chem. Ecol. 25:1411–1425.CrossRefGoogle Scholar
  2. Altmann, J. 1974. Observational study of behavior: Sampling methods. Behaviour 49:227–265.PubMedGoogle Scholar
  3. Artavia, D., Barrios, M., and Castro, O. 1995. A flavonol rhamnoside from Hymenaea courbaril leaves. Fitoterapia LXVI:91–92.Google Scholar
  4. Barnola, L. F., Hasegawa, M., and Cedeño, A. 1994. Mono- and sesquiterpene variation in Pinus caribaea needles and its relationship to Atta laevigata herbivory. Biochem. Syst. Ecol. 22:437–445.CrossRefGoogle Scholar
  5. Berry, J. P. 1998. The chemical ecology of mountain gorillas (Gorilla gorilla beringei), with respect to antimicrobial constituents in the diet. Ph.D. dissertation, Cornell University, Ithaca, NY.Google Scholar
  6. Calvert, J. J. 1985. Food selection by western gorillas (Gorilla gorilla) in relation to food chemistry. Oecologia 65:236–246.CrossRefGoogle Scholar
  7. Crankshaw, D. R. and Langenheim, J. H. 1981. Variation in terpenes and phenolics through leaf development in Hymenaea and its possible significance to herbivory. Biochem. Syst. Ecol. 9:115–124.CrossRefGoogle Scholar
  8. De Asevedo, N. R., Ferri, E., Seraphin, J. C., and Brandão, D. 2006. Chemical composition of intraspecific variability of the volatile constituents from the defensive secretions of Constrictotermes cyphergaster. Sociobiology 47:891–902.Google Scholar
  9. Estrada, A. 1984. Resource use by howler monkeys (Alouatta palliata) in the rainforest of “Los Tuxtlas”, Veracruz, Mexico. Intl. J. Primatol. 5:105–131.Google Scholar
  10. Glander, K. E. 1978. Howling monkey behavior and plant secondary compounds: A study of strategies, pp. 561–574, in G. G. Montgomery (ed.). The Ecology of Arboreal Folivores. Smithsonian Institution Press, Washington, DC.Google Scholar
  11. Glander, K. E. 1981. Feeding patterns in mantled howler monkeys, pp. 231–257, in A. C. Kamil and T. D. Sargent (eds.). Foraging Behavior: Ecological, Ethological, and Psychological Approaches. Garland Press, New York.Google Scholar
  12. Glander, K. E. 1982. The impact of plant secondary compounds on primate feeding behavior. Yearb. Phys. Anthropol. 25:1–18.CrossRefGoogle Scholar
  13. Haznedaroglu, M. Z., Karabay, N. U., and Zeybek, U. 2001. Antibacterial activity of Salvia tomentosa essential oil. Fitoterapia 72:829–831.PubMedCrossRefGoogle Scholar
  14. Janzen, D. H. 1983. Hymenaea courbaril, pp. 253–256, in D. H. Janzen (ed.). Costa Rican Natural History. Chicago University Press, Chicago.Google Scholar
  15. Joulain, D. and König, W. A. 1998. The Atlas of Spectral Data of Sesquiterpene Hydrocarbons. E. B. Verlag, Hamburg.Google Scholar
  16. Langenheim, J. H. 1981. Terpenoids in the Leguminosae, pp. 627–655, in R. M. Polhill and P. H. Raven (eds.). Advances in Legume Systematics. Royal Botanical Gardens, Kew.Google Scholar
  17. Langenheim, J. H., Stubblebine, W. H., and Lincoln, D. E. 1975. Vegetative growth and leaf resin composition in Hymenaea courbaril under photoperiodic extremes. Biochem. Syst. Ecol. 3:219–228.CrossRefGoogle Scholar
  18. Langenheim, J. H., Stubblebine, W. H., and Foster, C. E. 1979. Effect of moisture stress on composition and yield in leaf resin of Hymenaea courbaril. Biochem. Syst. Ecol. 7:21–28.CrossRefGoogle Scholar
  19. Langenheim, J. H., Foster, C. E., and Mcginley, R. B. 1980. Inhibitory effects of different quantitative compositions of Hymenaea leaf resins on a generalist herbivore Spodoptera exigua. Biochem. Syst. Ecol. 8:385–396.CrossRefGoogle Scholar
  20. Langenheim, J. H., Convis, C. L., Macedo, C. A., and Stubblebine, W. H. 1986. Hymenaea and Copaifera leaf sesquiterpenes in relation to lepidopteran herbivory in southeastern Brazil. Biochem. Syst. Ecol. 14:41–49.CrossRefGoogle Scholar
  21. Ling, B., Zhang, M., Kong, C., Pang, X., and Liang, G. 2003. Chemical composition of volatile oil from Chromolaena odorata and its effect on plant, fungi, and insect growth. Chin. J. Appl. Ecol. 14:744–746.Google Scholar
  22. Lopez, J. A. 1976. The isolation and characterization of funiferine N-oxide. A new alkalide from Tillacora funifera Oliver (Menispermaceae) alkaloid N-oxides. Study of the N-oxides of funiferine and pheanthine and chemical constituents of selected medicinal plants from Costa Rica L (Papaveraceae) Hymenaea courbaril L (Leguminosae) Physalis angulata L (Solanaceae). Ph.D. dissertation, University of Pittsburgh, Pittsburgh.Google Scholar
  23. Martin, S. S., Langenheim, J. H., and Zavarin, E. 1972. Sesquiterpenes in leaf pocket resin of Hymenaea courbaril. Phytochemistry 11:3049–3051.CrossRefGoogle Scholar
  24. Martin, S. S., Langenheim, J. H., and Zavarin, E. 1974. Quantitative variation in leaf pocket resin composition in Hymenaea courbaril. Biochem. Syst. Ecol. 2:75–87.CrossRefGoogle Scholar
  25. McCloskey, L. P. 1984. Leaf phenolic compounds in the tropical tree genera Hymenaea and Copaifera. Ph.D. dissertation, University of California, Santa Cruz.Google Scholar
  26. Milton, K. 1978. Behavioral adaptations to leaf-eating by the mantled howler monkey (Alouatta palliata), pp. 535–549, in G. G. Montgomery (ed.). The Ecology of Arboreal Folivores. Smithsonian Institution Press, Washington, DC.Google Scholar
  27. Milton, K. 1979. Factors influencing leaf choice by howler monkeys: A test of some hypotheses. Am. Nat. 114:362–378.CrossRefGoogle Scholar
  28. Milton, K. 1980. The Foraging Strategy of Howler Monkeys. Columbia University Press, New York.Google Scholar
  29. Milton, K. 1998. Physiological ecology of howlers (Alouatta): Energetic and digestive considerations and comparison with the colobinae. Intl. J. Primatol. 19:513–548.CrossRefGoogle Scholar
  30. Quintana, A., Reinhard, J., Faure, R., Uva, P., Bagnères, A.-G., Massiot, G., and Clément, J.-L. 2003. Interspecific variation in terpenoid composition of defensive secretions of European Reticulitermes termites. J. Chem. Ecol. 29:639–652.PubMedCrossRefGoogle Scholar
  31. Vrkočová, P., Valterová, I., Vrkoč, J., and Koutek, B. 2000. Volatiles released from oak, a host tree for the bark beetle Scolytus intricatus. Biochem. Syst. Ecol. 28:933–947.PubMedCrossRefGoogle Scholar
  32. Welker, B. J. 2004. Proximate mechanisms governing feeding behavior and selectivity in mantled howler monkeys, Alouatta palliata. Ph.D. dissertation, State University of New York, Buffalo.Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • B. J. Welker
    • 1
  • W. König
    • 2
  • M. Pietsch
    • 3
  • R. P. Adams
    • 4
  1. 1.Department of AnthropologyState University of New YorkGeneseoUSA
  2. 2.Institut für Organische ChemieUniversität HamburgHamburgGermany
  3. 3.Paul Hartman AGHeidenheimGermany
  4. 4.Department of BiologyBaylor UniversityWacoUSA

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