Comparing diet, seed size and richness in fruit ingested by red howler monkeys (Alouatta juara) in two habitat types in Central Amazonia
DOI:
https://doi.org/10.62015/np.2023.v29.776Keywords:
Alouatta juara, Amazon, feeding ecology, seed dispersal, subsistence hunting, upland forest, white-water flooded forestAbstract
Primates within the Alouatta genus (howler monkeys) inhabit a wide range of environments due to their flexible folivorous-frugivorous diet. However, the feeding ecology of Alouatta species that inhabit continuous and difficult-to-access forest environments, such as the Amazon, is poorly known. In this study, we compared diet composition, seed size, and richness of fruits ingested by Juruá red howler monkeys (Alouatta juara) in white-water flooded forest and upland for- est. Our analysis was based on 47 stomachs donated by subsistence hunters of central Amazonia in Brazil. We found no difference in the proportion of structural parts, reproductive parts, and animal matter (arthropods) ingested between these environments. However, we found a positive relationship between the richness of ingested seeds and the water level for the white-water flooded forest. This correlation was not observed for upland forest, where other environmental factors such as precipitation may influence tree phenology. The stomach analysis revealed a high diversity of seeds and a substantial percentage of whole seeds (73%) in the red-howler monkeys’ stomachs. This suggests that they have the potential to be effective seed dispersers for at least 40 taxa in the white-water flooded forest and 14 in the upland forest. The population decline or extinction of this species could have an impact on seed dispersal services, particularly for plant species with seeds larger than 20 mm of diameter, as the number of dispersing agents tends to be limited. Further studies are needed to investigate the environmental dynamics involved in the feeding ecology of red howler monkeys. These studies would help to understand the ecological impacts of local subsistence hunting and wild meat trading on seed dispersal, as well as the economic implications for human populations.
References
Altmann, J. 1974. Observational study of behavior: Sampling methods. Behaviour 49: 227–267. https://www.jstor.org/stable/4533591.
Andresen, E. 2003. Effect of forest fragmentation on dung beetle communities and functional consequences for plant regeneration. Ecography 26: 87–97. https://www.jstor.org/stable/3683529.
Bello, C., Culot, L., Agudelo, C. A. R. and Galetti, M. 2021. Valuing the economic impacts of seed dispersal loss on voluntary carbon markets. Ecosyst. Serv. 52: 101362. https://doi.org/10.1016/j.ecoser.2021.101362.
Bicca-Marques, J. C. 2003. How do howler monkeys cope with habitat fragmentation? In: Primates in Fragments, L. K. Marsh (ed.), pp.283–303. Springer, Boston.
Bufalo, F. S., Galetti, M. and Culot, L. 2016. Seed dispersal by primates and implications for the conservation of a biodiversity hotspot, the Atlantic Forest of South America. Int. J. Primatol. 37: 333–349. https://doi.org/10.1007/s10764-016-9903-3.
Chapman, C. A. and Chapman, L. J. 1990. Dietary variability in primate populations. Primates 31: 121–128. https://doi.org/10.1007/BF02381035.
Chaves, O. M., Bicca-Marques, J. C. and Chapman, C. A. 2018. Quantity and quality of seed dispersal by a large arboreal frugivore in small and large Atlantic Forest fragments. Plos One 13(3): e0193660. https://doi.org/10.1371/journal.pone.0193660.
Crockett, C.M. 1998. Conservation biology of the genus Alouatta. Int. J. Primatol. 19: 549–578. https://doi.org/10.1023/A:1020316607284.
Dew, J. L. 2003. Feeding ecology, frugivory and seed dispersal. In: Field and Laboratory Methods in Primatology: A Practical Guide, J. M. Setchell and D. J. Curtis (eds.), pp.225–235. Cambridge University Press, Cambridge.
dos Santos, J. P. V. 2016. Dieta e padrão de atividade de Alouatta juara (Primates, Atelidae) em floresta de várzea na Amazônia central. MSc Thesis, Museu Paraense Emilio Goeldi/Universidade Federal do Pará, Pará, BR.
El Bizri, H. R., Fa, J. E., Bowler, M., Valsecchi, J., Bodmer, R. and Mayor, P. 2018. Breeding seasonality in the lowland paca (Cuniculus paca) in Amazonia: interactions with rainfall, fruiting, and sustainable hunting. J. Mammal. 99: 1101–1111. https://doi.org/10.1093/jmammal/gyy102.
Feer, F. 1999. Effects of dung beetles (Scarabaeidae) on seeds dispersed by howler monkeys (Alouatta seniculus) in the French Guianan rain forest. J. Trop. Ecol. 15: 129–142. https://www.jstor.org/stable/2560014.
Fleagle, J. G. 2013. Primate Adaptation and Evolution. 3rd ed. Academic Press, New York.
Gilbert, K. A. 1997. Red howling monkey use of specific defecation sites as parasite avoidance strategy. Anim. Behav. 54: 451–455. https://doi.org/10.1006/anbe.1996.0439.
Hammer, Ø., Harper, D. A. and Ryan, P. D. 2001. PAST: Paleontological statistics software package for education and data analysis. Palaeontol. Electron. 4: 9.
Haugaasen, T. and Peres, C. A. 2005a. Primate assemblage structure in Amazonian flooded and unflooded forests. Am. J. Primatol. 67: 243–258. https://doi.org/10.1002/ajp.20180.
Haugaasen, T. and Peres, C. A. 2005b. Tree phenology in adjacent Amazonian flooded and unflooded forests. Biotropica 37: 620–630. https://doi.org/10.1111/j.1744-7429.2005.00079.x.
Hawes, J. E. and Peres, C. A. 2016. Patterns of plant phenology in Amazonian seasonally flooded and unflooded forests. Biotropica 48: 465–475. https://doi.org/10.1111/btp.12315.
Hawes, J. E. and Peres, C. A. 2014. Ecological correlates of trophic status and frugivory in Neotropical primates. Oikos 123: 365–377. https://www.jstor.org/stable/24567467.
IDSM. 2020. Banco de Dados Fluviométrico da Reserva de Desenvolvimento Sustentável Mamirauá. Instituto de Desenvolvimento Sustentável Mamirauá (IDSM). Website: https://mamiraua.org.br/fluviometrico-na-reserva. Accessed on 15 June 2020.
Jesus, A. S., Oliveira-Ramalho, M. L., El Bizri, H. R., Valsecchi, J. and Mayor, P. 2022a. Environmental and biological drivers of prevalence and number of eggs and oocysts of intestinal parasites in red howler monkeys from Central Amazonia. Folia Primatol. 93: 121–138. https://doi.org/10.1163/14219980-20210701.
Jesus, A. S., Torres, R. I. C., Cruz, A. N., El Bizri, H. R., Valsecchi, J. and Mayor, P. 2022b. Are larger primates less faunivorous? Consumption of arthropods by Amazonian primates does not fulfil the Jarman-Bell and Kay models. Acta Amazon. 52(3): 208–217. https://doi.org/10.1590/1809-4392202200842.
Jesus, A. S., Torres, R. I. C., Cruz, A. N., El Bizri, H. R., Valsecchi, J. and Mayor, P. 2021. Estimativa de quantidade de sementes potencialmente dispersas por primatas amazônicos caçados. In: Livro de Resúmenes del XIV Congreso Internacional de Manejo de Fauna Silvestre de la Amazonía y Latinoamérica, Servicio Nacional de Áreas Naturales Protegidas por el Estado, pp.156–157. SERNANP, Paracas.
Julliot, C. 1996. Seed dispersal by red howling monkeys (Alouatta seniculus) in the Tropical Rain Forest of French Guiana. Int. J. Primatol. 17: 239–258. https://doi.org/10.1007/BF02735451.
Julliot, C. 1997. Impact of seed dispersal by red howler monkeys Alouatta seniculus on the seedling population in the understorey of tropical rain forest. J. Ecol. 85: 431–440. https://doi.org/10.2307/2960567.
Julliot, C. 2001. Frugivory and seed dispersal by three Neotropical primates: Impact on plant regeneration. In: Nouragues: Dynamics and Plant-Animal Interactions in a Neotropical Rainforest, F. Bongers, P. Charles-Dominique, P-M. Forget and M. Théry (eds.), pp.197–206. Springer, New York.
Junk, W. J. 1993. Wetlands of tropical south America. In: Wetlands of the World: Inventory, Ecology and Management. Volume I, D. F. Whigham, D. Dykyjová and S. Hejný (eds.), pp.679–739. Springer, Dordrecht.
Koné, I., Lambert, J. E., Refisch, J. and Bakayoko, A. 2008. Primate seed dispersal and its potential role in maintaining useful tree species in the Taï region, Côte-d’Ivoire: implications for the conservation of forest fragments. Trop. Conserv. Sci. 1: 293–305. https://doi.org/10.1177/194008290800100309.
Kubitzki, K. and Ziburski, A. 1994. Seed dispersal in flood plain forest of Amazonia. Biotropica 26: 30–43. https://doi.org/10.2307/2389108.
Kurland, J. A. and Gaulin, S. J C. 1987. Comparability among measures of primate diets. Primates 28: 71–77. https://doi.org/10.1007/BF02382184.
Lambert, J. E. 1998a. Primate digestion: Interactions among anatomy, physiology, and feeding ecology. Evol. Anthropol. 7: 8–20. https://doi.org/10.1002/(SICI)1520-6505(1998)7:1<8::AID-EVAN3>3.0.CO;2-C.
Lambert, J. E. 1998b. Primate frugivory in Kibale National Park, Uganda, and its implications for human use of forest resources. Afr. J. Ecol. 36: 234–240. https://doi.org/10.1046/j.1365-2028.1998.00131.x.
Levi, T. and Peres, C. A. 2013. Dispersal vacuum in the seedling recruitment of a primate-dispersed Amazonian tree. Biol. Conserv. 163: 99–106. https://doi.org/10.1016/j.biocon.2013.03.016.
Loayza, P. A. and Paine, C. E. T. 2014. Guía 242: Semillas de Cocha Cashu. Estación Biológica Cocha Cashu, Parque Nacional del Manú. Field Museum, Madre de Dios.
Mayor, P., El Bizri, H. R., Bodmer, R. E. and Bowler, M. 2017. Assessment of mammal reproduction for hunting sustainability through community-based sampling of species in the wild. Conserv. Biol. 31: 912–923. https://doi.org/10.1111/cobi.12870.
Milton, K. and Nessimian, J. L. 1984. Evidence for insectivory in two primate species (Callicebus torquatus lugens and Lagothrix lagothricha lagothricha) from Northwestern Amazonia. Am. J. Primatol. 6: 367–371. https://doi.org/10.1002/ajp.1350060406.
Moreno-Black, G. 1978. The use of scat samples in primate diet analysis. Primates 19: 215–221. https://doi.org/10.1007/BF02373239.
Mozombite, E.J.A. 2018. Guía 1083: Frutos y semillas de Annonaceae más comunes del Perú. Field Museum, Iquitos.
Nielsen, J. M., Clare, E. L., Hayden, B., Brett, M. T. and Kratina, P. 2017. Diet tracing in ecology: method comparison and selection. Methods Ecol. Evol. 9: 278–291. https://doi.org/10.1111/2041-210X.12869.
Norconk, M. A., Wright, B. W., Conklin-Brittain, N. L. and Vinyard, C. J. 2009. Mechanical and nutritional properties of food as factors in platyrrhine dietary adaptations. In: South American Primates: Comparative Perspectives in the Study of Behavior, Ecology, and Conservation, P. A. Garber (ed.), pp.279–319. Springer, New York.
Nuñez‐Iturri, G. and Howe, H. F. 2007. Bushmeat and the fate of trees with seeds dispersed by large primates in a lowland rain forest in western Amazonia. Biotropica 39: 348–354. https://www.jstor.org/stable/30044947.
Paim, F. P., Chapman, C. A., Queiroz, H. L. and Paglia, A. P. 2017. Does resource availability affect the diet and behavior of the vulnerable squirrel monkey, Saimiri vanzolinii? Int. J. Primatol. 38: 572–587. https://doi.org/10.1007/s10764-017-9968-7.
Paim, F. P., Valenta, K., Chapman, C. A., Paglia, A. P. and Queiroz, H. L. 2018. Tree community structure reflects niche segregation of three parapatric squirrel monkey species (Saimiri spp.). Primates 59: 395–404. https://doi.org/10.1007/s10329-018-0659-6.
Parolin, P., Wittmann, F. and Ferreira, L. V. 2013. Fruit and seed dispersal in Amazonian floodplain trees—a review. Ecotropica 19: 19–36.
Pereira, M. J. R., Marques, J. T. and Palmeirim, J. M. 2010. Ecological responses of frugivorous bats to seasonal fluctuation in fruit availability in Amazonian forests. Biotropica 42: 680–687. https://doi.org/10.1111/j.1744-7429.2010.00635.x.
Pereira, P. M., Valsecchi, J. and Queiroz, H. 2017. Spatial patterns of primate hunting in riverine communities in Central Amazonia. Oryx 53: 165–173. https://doi.org/10.1017/S0030605317000199.
Peres, C. A. and van Roosmalen, M. 2002. Primate frugivory in two species-rich Neotropical forests: implications for the demography of large-seeded plants in overhunted areas. In: Seed Dispersal and Frugivory: Ecology, Evolution and Conservation, D. J., Levey, W. R, Silva and M. Galetti (eds.), pp.407–421. CABI Publishing, New York.
Peres, C. A. 2000. Effects of subsistence hunting on vertebrate community structure in Amazonian forests. Conserv. Biol. 14: 240–253. https://doi.org/10.1046/j.1523-1739.2000.98485.x.
Queiroz, H L. 1995. Preguiças e guaribas: os mamíferos folívoros do Mamirauá. CNPq/Sociedade Civil Mamirauá, Brasília.
Ramalho, E. E., Macedo, J., Vieira, T.M., Valsecchi, J., Calvimontes, J., Marmontel, M. and Queiroz, H. L. 2009. Ciclo hidrológico nos ambientes de várzea da Reserva de Desenvolvimento Sustentável Mamirauá médio rio Solimões, período de 1990 a 2008. Uakari 5: 61–87.
Schupp, E. W. 1993. Quantity, quality, and the effectiveness of seed dispersal by animals. Vegetation 107: 15–29. https://www.jstor.org/stable/20046297.
SEMA. 2020. Plano de Gestão da Reserva de Desenvolvimento Sustentável Amanã. Secretaria do Meio Ambiente do Estado do Amazonas, Manaus.
SNIF. 2020. Sistema Nacional de Informações Florestais. Website: https://snif.florestal.gov.br/pt-br/especies-florestais?modal=1&tipo=tableau. Accessed on 10 June 2022.
SNUC. 2000. Lei n. 9.985, de 18 de julho de 2000, Decreto n. 4.340, de 22 de agosto de 2002. Brasília-DF, 5a ed: MMA/SBF. Sistema Nacional de Unidades de Conservação da Natureza. Website: http://www.planalto.gov.br/ccivil_03/leis/l9985.htm. Accessed on 20 April 2021.
Stevenson, P. R. 2007. Estimates of the number of seeds dispersed by a population of primates in a lowland forest in western Amazonia. In: Seed dispersal: Theory and its application in a changing world, A. J. Dennis, R. J. Green, E. W. Schupp and D. A. Westcott (eds.), pp.340–362. Cambridge University Press, Cambridge.
Stevenson, P. R., Pineda, M. and Samper, T. 2005. Influence of seed size on dispersal patterns of woolly monkeys (Lagothrix lagothricha) at Tinigua Park, Colombia. Oikos 110: 435–440. https://www.jstor.org/stable/3548583.
Torres, P. C., Morsello, C., Parry, L., Barlow, J., Ferreira, J., Gardner, T. and Pardini, R. 2018. Landscape correlates of bushmeat consumption and hunting in a post-frontier Amazonian region. Environ. Conserv. 45: 352–360. https://www.jstor.org/stable/26531440.
Torres, R. I. C., Jesus, A. S., Loaiza, J. O. and Mayor, P. 2022. Dietas de primatas no humanos del norte amazónico peruano. Rev. de Investig. Vet. del Peru 33: e22159. http://doi.org/10.15381/rivep.v33i1.22159.
Valenta, K. and Fedigan, L. M. 2008. How much is a lot? Seed dispersal by white-faced capuchins and implications for disperser-based studies of seed dispersal systems. Primates 49: 169–175. https://doi.org/10.1007/s10329-008-0087-0.
Valsecchi, J., El Bizri, H. R., and Figueira, J. E. C. 2014. Subsistence hunting of Cuniculus paca in the middle of the Solimões River, Amazonas, Brazil. Braz. J. Biol. 74: 560–568. https://doi.org/10.1590/bjb.2014.0098.
Vásquez-Arévalo, F.A., Casado, J. A. G., Montenegro, L. A. T., Guerra-Torres, L. N., García, M. N. A. and Mayor, P. 2021. Guía 1297: Semillas procedentes de la dieta de fauna silvestre: aves y primates de caza de subsistencia, Ríos Yavarí-Mirín, Corrientes y Pastaza, Amazonía Oeste, Loreto, Perú. Field Museum, Loreto.
Wrangham, R. W., Chapman, C. A. and Chapman, L. J. 1994. Seed dispersal by forest chimpanzees in Uganda. J. Trop. Ecol. 10: 355–368. https://www.jstor.org/stable/2560319.
Wittmann, F., Schöngart, J., Montero, J. C., Motzer, T., Junk, W. J., Piedade, M. T. F., Queiroz, H. L. and Worbes, M. 2006. Tree species composition and diversity gradients in white-water forests across the Amazon Basin. J. Biogeogr. 33: 1334–1347. https://doi.org/10.1111/j.1365-2699.2006.01495.x.
Zambrano, V. A. B., Moncada, J. Z. and Stevenson, P. R. 2008. Diversity of regenerating plants and seed dispersal in two canopy trees from Colombian Amazon forests with different hunting pressure. Rev. Biol. Trop. 56: 1531–1542
Downloads
Published
Issue
Section
License
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
