Abstract
Howler monkeys (Alouatta spp.) have long been considered strongly vegetarian primates. Their occasional ingestion of invertebrates has largely been interpreted as unintentional. Recent observations of the consumption of bird eggs by Alouatta caraya living in small and resource-impoverished habitat patches in the state of Rio Grande do Sul (RS), Brazil help to confirm that such behavior by howler monkeys is at times intentional. We report the findings of an experimental study on artificial nest predation by free-ranging Alouatta guariba clamitans in RS and third-party unpublished observations of intentional feeding on animal matter by Alouatta arctoidea in Venezuela and Alouatta palliata in Mexico. A nest station composed of ten artificial nests baited daily with two quail eggs each was placed at six study sites. Each site was monitored from dawn to dusk during 10–12 consecutive days. Individuals (juvenile males and an adult female) from two of the six study groups inspected the nests and ate eggs once. Study subjects from these two groups were the only ones to be supplemented with food (basically fruit) by local inhabitants, a habit that may have decreased their level of neophobia and facilitated their visit to the artificial nests. We suggest that faunivory is an opportunistic and infrequent, but intentional howler monkey feeding behavior.
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References
Bicca-Marques JC, Muhle CB, Prates HM, Oliveira SG, Calegaro-Marques C (2009) Habitat impoverishment and egg predation by Alouatta caraya. Int J Primatol 30:743–748
Burke DM, Elliot E, Moore L et al (2004) Patterns of nest predation on artificial and natural nests in forests. Conserv Biol 18:381–388
Crockett CM, Eisenberg JF (1987) Howlers: variations in group size and demography. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, Chicago, pp 54–68
Estrada A, Rivera A, Coates-Estrada R (2002) Predation of artificial nests in a fragmented landscape in the tropical region of Los Tuxtlas, Mexico. Biol Conserv 106:199–209
Fashing PJ (2007) African colobine monkeys: patterns of between-group interaction. In: Campbell CJ, Fuentes A, MacKinnon KC, Panger M, Bearder SK (eds) Primates in perspective. Oxford University Press, New York, pp 201–224
Feeley KJ, Terborgh JW (2008) Direct versus indirect effects of habitat reduction on the loss of avian species from tropical forest fragments. Anim Conserv 11:353–360
Grzimek B (1972) Grzimek’s animal life encyclopedia. Van Nostrand, New York
Keyser AJ, Hill GE, Soehren EC (1998) Effects of forest fragment size, nest density, and proximity to edge on the risk of predation to ground-nesting passerine birds. Conserv Biol 12:986–994
Marini MÂ, Melo C (1998) Predators of quail eggs, and the evidence of the remains: implications for nest predation studies. Condor 100:395–399
Martin P, Bateson P (2007) Measuring behaviour: an introductory guide, 3rd edn. Cambridge University Press, Cambridge
Martin TE (1987) Artificial nest experiments: effects of nest appearance and type of predator. Condor 89:925–928
Moore RP, Robinson WD (2004) Artificial bird nests, external validity, and bias in ecological field studies. Ecology 85:1562–1567
Nowak RM (1999) Walker’s mammals of the world, vol 1, 6th edn. The Johns Hopkins University Press, Baltimore
Strier KB (2003) Howler monkeys and spider monkeys (Atelidae). In: Hutchins M, Kleiman DG, Geist V, McDade MC (eds) Grzimek’s animal life encyclopedia, volume 14, mammals III, 2nd edn. Gale Group, Farmington Hills, pp 155–169
Terborgh J, Lopez L, Tello J, Yu D, Bruni AR (1997) Transitory states in relaxing ecosystems or land bridge islands. In: Laurance WF, Bierregaard RO (eds) Tropical forest remnants. University of Chicago Press, Chicago, pp 256–274
Visalberghi E, Janson CH, Agostini I (2003) Response toward novel foods and novel objects in wild Cebus apella. Int J Primatol 24:653–675
Walker EP (1968) Mammals of the world, 2nd edn. The John Hopkins University Press, Baltimore
White TCR (1985) When is a herbivore not a herbivore? Oecologia 67:596–597
White TCR (2011) The significance of unripe seeds and animal tissues in the protein nutrition of herbivores. Biol Rev 86:217–224
Acknowledgments
We thank João Vieira, Marília Weingaertner, Emerson Chassot, Oivar Giacobbo, Paulo Souza de Lima, Cesar Hoffmann, Rafael Sittoni Goelzer, and Ana Lúcia de Souza Rangel for logistical support and permission to conduct this research at the study sites; the Brazilian National Research Council for financial support (CNPq, proc. PQ #306090/2006-6 and 303154/2009-8 and PIBIC/PUCRS #897/2009 and 1831/2010); Carolyn M. Crockett, Alejandro Estrada, Dorothy M. Fragaszy, and Marie-Claude Huynen for sharing and giving permission to publish their observations; Paul A. Garber and Katharine Milton for making excellent critical suggestions and revising the text; and Lilian Alves Schmitt for field assistance in one study site.
Ethical standards
The research complied with protocols approved by the Scientific Committee of the Faculdade de Biociências/PUCRS (project FABIO #3477), and it adhered to the legal requirements of Brazil. JCBM has a license issued by the federal environmental protection agency—Instituto Chico Mendes de Conservação da Biodiversidade (SISBIO #23748) to conduct research with free-ranging primates in Brazil.
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The authors declare that they have no conflict of interest.
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Bicca-Marques, J.C., Silveira, I.R.R.I., de Souza Martins, L. et al. Artificial nest predation by brown howler monkeys (Alouatta guariba clamitans). Eur J Wildl Res 60, 109–112 (2014). https://doi.org/10.1007/s10344-013-0756-1
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DOI: https://doi.org/10.1007/s10344-013-0756-1