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Diet and Feeding Behavior of Leontopithecus chrysomelas (Callitrichidae) in Degraded Areas of the Atlantic Forest of South-Bahia, Brazil

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Abstract

Habitat disturbance alters plant diversity and food resource availability, affecting the ecology, and ultimately the survival and reproduction, of species depending on those plants. Studies in degraded areas serve to improve our understanding of the consequences of habitat modification for endangered species and to guide conservation actions. We studied diet composition, monthly variation in feeding behavior and fruit feeding time, and dietary diversity in two golden-headed lion tamarin (Leontopithecus chrysomelas) groups ranging in a degraded area of the Atlantic Forest in South-Bahia, Brazil, over a 12-mo period. We recorded feeding behavior and food items consumed through continuous observations and focal animal sampling, and performed dietary analyses on samples from consumed fruits. Substrate manipulation to search for animal prey was the feeding activity most frequently observed, followed by fruit consumption. We observed nectar drinking and exudate feeding at low frequencies from April through July. Bromeliads were the principal foraging substrate. We observed the use of 114 plant species, confirming the large dietary diversity reported for the species. Individual trees from the family Melastomataceae, common in degraded forests, accounted for the highest visiting frequencies (40%). Fruit availability was the main factor explaining variation in monthly fruit feeding time, despite the absence of climatic seasonality. Nutritional or energetic characteristics did not affect fruit choice. Differences in floristic composition appear to be a major determinant of the species’ diet in different study areas. Regional forest restoration programs should consider including advanced forest species, to improve both forest quality and animal mobility between fragments.

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References

  • Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour, 49, 227–267.

    Article  CAS  PubMed  Google Scholar 

  • Alves, T. F. (2005). Distribuição geográfica, forófitos e eespécies de bromélias epífitas nas matas e nas plantações de cacau da região de Una, Bahia. Dissertation, Universidade Estadual de Campinas, São Paulo.

  • Arroyo-Rodríguez, V., & Mandujano, S. (2006). Forest fragmentation modifies habitat quality for Alouatta palliata. International Journal of Primatology, 27(4), 1079–1096.

    Article  Google Scholar 

  • Cardoso, N. A., Le Pendu, Y., Lapenta, M. J., & Raboy, B. E. (2011). Frugivory patterns and seed dispersal by golden-headed lion tamarins (Leontopithecus chrysomelas) in Una Biological Reserve, Bahia, Brazil. Mammalia, 75, 327–337.

    Article  Google Scholar 

  • Caselli, C. B., & Setz, E. Z. F. (2011). Feeding ecology and activity pattern of black-fronted titi monkeys (Callicebus nigrifrons) in a semideciduous tropical forest of southern Brazil. Primates, 52, 351–359.

    Article  PubMed  Google Scholar 

  • Catenacci, L. S., De Vleeschouwer, K. M., & Nogueiro-Filho, S. L. G. (2009). Seed dispersal by Leontopithecus chrysomelas (Primates, Callitrichidae) in Southern Bahian Atlantic Forest, Brazil. Biotropica, 41, 744–750.

    Article  Google Scholar 

  • Chancellor, R. L., Rundus, A. S., & Nyandwi, S. (2012). The influence of seasonal variation on chimpanzee (Pan troglodytes schweinfurthii) fallback food consumption, nest group size, and habitat use in Gishwati, a Montane Rain Forest Fragment in Rwanda. International Journal of Primatology, 33, 115–133.

    Article  Google Scholar 

  • Chavez, C. M., & Bicca-Marquez, J. (2013). Dietary flexibility of the brown howler monkey throughout its geographic distribution. American Journal of Primatology, 75(1), 16–29.

    Article  Google Scholar 

  • Coelho, A. S., Ruiz-Miranda, C. R., Beck, B. B., Martins, A., de Oliveira, C. R., & Sabatini, V. (2008). Comportamento do mico-leão-dourado (Leontopithecus rosalia, Linnaeus 1766) em relação à fragmentação do habitat. In P. Procópio de Oliveira (Ed.), Conservação do mico-leão-dourado: Enfrentando os desafios de uma paisagem fragmentado. Rio de Janeiro: Associação Mico-Leão-Dourado/Universidade Estadual do Norte Fluminense Darcy Ribeiro.

    Google Scholar 

  • Coimbra-Filho, A. F., & Mittermeier, R. A. (1977). Conservation of Brazilian lion tamarins (Leontopithecus rosalia). In HSH Prince Rainier III of Monaco and G. H. Bourne (Eds.), Primate conservation (pp. 59–94). New York: Academic Press.

  • De Vleeschouwer, K. M., & Raboy, B. E. (2013). Multi-level and multi-disciplinary approaches to understanding endangered primates in complex landscapes: Golden-headed lion tamarins in Southern Bahia, Brazil. In L. Marsh & C. Chapman (Eds.), Primates in fragments: Complexity and resilience. Developments in primatology: progress and prospects. New York: Springer Science+Business Media.

    Google Scholar 

  • Di Bitetti, M. S., & Janson, C. H. (2000). When will the stork arrive? Patterns of birth seasonality in neotropical primates. American Journal of Primatology, 50, 109–130.

    Article  PubMed  Google Scholar 

  • Dietz, J. M., Baker, A. J., & Miglioretti, D. (1994). Seasonal variation in reproduction, juvenile growth, and adult body mass in golden lion tamarins (Leontopithecus rosalia). American Journal of Primatology, 34, 115–132.

    Article  Google Scholar 

  • Dietz, J. M., de Sousa, S. N., & Billerbeck, R. (1996). Population dynamics of golden-headed-lion-tamarins Leontopithecus chrysomelas in Una Reserve, Brazil. Dodo, 32, 115–122.

    Google Scholar 

  • Dietz, J. M., Peres, C. A., & Pinder, L. (1997). Foraging ecology and use of space in wild golden lion tamarins (Leontopithecus rosalia). American Journal of Primatology, 41, 289–305.

    Article  CAS  PubMed  Google Scholar 

  • Dunn, J. C., Cristóbal-Azkarate, J., & Veà, J. J. (2009). Differences in diet and activity pattern between two groups of Alouatta palliata associated with the availability of big trees and fruit of top food taxa. American Journal of Primatology, 71(8), 654–662.

    Article  PubMed  Google Scholar 

  • Erbesdobler, D. E. (2003). Ecologia nutricional de Callitrichidae (Primates: Anthropoidea): Composição químico-bromatológica da dieta, aspectos do comportamento alimentar e metabolismo energético. Dissertation, Universidade Estadual do Norte Fluminense, Rio de Janeiro.

  • Fahrig, L. (2013). Rethinking patch size and isolation effects: The habitat amount hypothesis. Journal of Biogeography, 40(9), 1649–1663.

    Article  Google Scholar 

  • Fan, P. F., Fei, H. L., & Ma, C. Y. (2012). Behavioral responses of Cao Vit gibbon (Nomascus nasutus) to variations in food abundance and temperature in Bangliang, Jingxi, China. American Journal of Primatology, 74(7), 632–641.

    Article  PubMed  Google Scholar 

  • Faria, D., Mariano-Neto, E., Martini, A. M. Z., Ortiz, J. V., Montingelli, R., Rosso, S., Paciencia, M. L. B., & Baumgarten, J. (2009). Forest structure in a mosaic of rainforest sites: The effect of fragmentation and recovery after clear cut. Forest Ecology and Management, 257, 2226–2234.

    Article  Google Scholar 

  • Felton, A. M., Felton, A., Lindenmayer, D. B., & Foley, W. J. (2009). Nutritional goals of wild primates. Functional Ecology, 23(1), 70–78.

    Article  Google Scholar 

  • Fontoura, T., Cazetta, E., Nascimento, W., Catenacci, L. S., De Vleeschouwer, K. M., & Raboy, B. E. (2010). Frugivory on the bromeliad species Aechmea depressa L.B. Smith (Bromeliaceae) from northeastern Brazil: The prominent role taken by a small forest primate? Biota Neotropical, 10, 351–354.

    Google Scholar 

  • Fournier, L. A. (1974). Un método cuantitativo para la medición de características fenológicas en arboles. Turrialba, 24(4), 422–423.

    Google Scholar 

  • Garcia, L. C., Hobbs, R. J., Mães dos Santos, F. A., & Rodrigues, R. R. (2014). Flower and fruit availability along a forest restoration gradient. Biotropica, 46(1), 114–123.

    Article  Google Scholar 

  • Gouvêa, J. B. S., Mattos Silva, L. A., & Hori M. (1976). Fitogeografia. In Diagnóstico socioeconômico da região cacaueira (pp. 1–7). Ilhéus: Comissão Executiva do Plano da Lavoura Cacaueira and the Instituto Interamericano de Ciências Agricolas-OEA.

  • Guidorizzi, C. E. (2008). Ecologia e comportamento do mico-leão-da-cara dourada, Leontopithecus chrysomelas (Kuhl, 1820) (Primates, callitrichidae), em um fragmento de floresta semidecidual em Itororó, Bahia, Brasil. Dissertation, Universidade Estadual de Santa Cruz–UESC, Ilhéus.

  • Hammer, O., Harper, D. A. T., & Ryan, P. D. (2001). PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica, 4(1), http://palaeo-electronica.org/2001_1/past/issue1_01.htm.

  • Hernández-Stefanoni, J. L., & Dupuy, J. M. (2008). Effects of landscape patterns on species density and abundance of trees in a tropical subdeciduous forest of the Yucatan Peninsula. Forest Ecology and Management, 255(11), 3797–3805.

    Article  Google Scholar 

  • IUCN (2015). The IUCN Red List of Threatened Species. Version 2015.2.

  • Jolliffe, I. (2014). Principal component analysis. Wiley StatsRef: Statistics Reference Online.

  • Keuroghlian, A., & Passos, F. C. (2001). Prey foraging behavior, seasonality and time-budgets in black lion Leontopithecus chrysopygus (Mikan 1823) (Mammalia, Callitrichidae). Brazilian Journal of Biology, 61, 455–459.

    Article  CAS  Google Scholar 

  • Kierulff, M. C. M., Raboy, B., Oliveira, P. P., Miller, K., Passos, F. C., & Prado, F. (2002). Behavioral ecology of Leontopithecus. In D. G. Kleiman & A. B. Rylands (Eds.), Lion Tamarins–biology and conservation (pp. 157–187). Washington, DC: Smithsonian Institution Press.

    Google Scholar 

  • Laurance, W. F., Camargo, J. L. C., Luizão, R. C. C., Laurance, S. G., Pimm, S. L., Bruno, E. M., Stouffer, P. C., Williamson, G. B., Benítez-Malvido, J., Vasconcelos, H. L., Van Houtan, K. S., Zartman, C. E., Boyle, S. A., Didham, R. K., Andrade, A., & Lovejoy, T. E. (2011). The fate of Amazonian forest fragments: A 32–year investigation. Biological Conservation, 144(1), 56–67.

    Article  Google Scholar 

  • Laurance, W. F., Rankin-de Merona, J. M., Andrade, A., Laurance, S. G., D’Angelo, S., Lovejoy, T. E., & Vasconcelos, H. L. (2003). Rain-forest fragmentation and the phenology of Amazonian tree communities. Journal of Tropical Ecology, 19(3), 343–347.

    Article  Google Scholar 

  • Lorenzi, H. (2002a). Árvores Brasileiras. Manual de identificação e cultivo de plantas arbóreas nativas do Brasil, Vol. 01. Nova Odessa, SP, Brasil: Instituto Plantarum.

  • Lorenzi, H. (2002b). Árvores Brasileiras. Manual de identificação e cultivo de plantas arbóreas nativas do Brasil, Vol. 02. Nova Odessa: Instituto Plantarum.

    Google Scholar 

  • Melo, F. P. L., Martínez-Salas, E., Benítez-Malvido, J., & Ceballos, G. (2010). Forest fragmentation reduces recruitment of large-seeded tree species in a semi-deciduous tropical forest of southern Mexico. Journal of Tropical Ecology, 26(01), 35.

    Article  Google Scholar 

  • Miller, K., & Dietz, J. (2006). The effects of individual and group characteristics on feeding behaviors in wild Leontopithecus rosalia. International Journal of Primatology, 26, 1291–1319.

    Article  Google Scholar 

  • MMA. (2007). Ministério do Meio Ambiente. http://mma.gov.br.

  • Mori, S. A., Boom, B. M., Carvalho, A. M., & Santos, T. S. (1983). Southern Bahian moist forests. The Botanical Review, 49, 155–232.

    Article  Google Scholar 

  • Munoz, D., Estrada, A., Naranjo, E., & Ochoa, S. (2006). Foraging e cology of howler monkeys in a Cacao (Theobroma cacao) plantation in Comalcalca, México. American Journal of Primatology, 68, 127–142.

    Article  PubMed  Google Scholar 

  • Nogueira, A. R. A., & Souza, G. B. (2005). Manual de Laboratórios: Solo, água, Nutrição vegetal, Nutrição animal e alimentos (1ªth ed.). São Carlos: Gráfica & Editora Guillen e Andrioli.

    Google Scholar 

  • Oliveira, P. P. (2002). Ecologia alimentar, dieta e área de uso de micos-leões-dourados translocados e sua relação com a distribuição espacial e temporal de recursos alimentares da Reserva Biológica União-RJ. Dissertation: Universidade Federal de Minas Gerais, Minas Gerais.

    Google Scholar 

  • Oliveira, L. C., Hankerson, S. J., Dietz, J., & Raboy, B. (2010). Key tree species for the golden-headed lion tamarin and implications for shade-cocoa management in southern Bahia, Brazil. Animal Conservation, 13, 60–70.

    Article  Google Scholar 

  • Oliveira, L. C., Neves, L. G., Raboy, B. E., & Dietz, J. M. (2011). Abundance of jackfruit (Artocarpus heterophyllus) affects group characteristics and use of space by golden-headed lion tamarins (Leontopithecus chrysomelas) in cabruca agroforest. Environmental Management, 48, 248–262.

    Article  PubMed  Google Scholar 

  • Pardini, R. (2004). Effects of forest fragmentation on small mammals in an Atlantic forest landscape. Biodiversity and Conservation, 13, 2567–2586.

    Article  Google Scholar 

  • Passos, F., & Alho, C. J. R. (2001). Importância de diferentes microhabitats no comportamento de forrageio por presas do mico-leão-preto, Leontopithecus chrysopygus (Mikan) (Mammalia, Callitrichidae). Brazilian Journal of Zoology, 16, 335–342.

    Google Scholar 

  • Pessoa, M. S. (2008). Comparação da Comunidade Arbórea e Fenlogia Fenologia reprodutiva de duas fisionomias em Floresta Atlântica do Sul da Bahia. Brasil: Dissertation, Universidade Estadual de Santa Cruz, Ilhéus, Bahia.

    Google Scholar 

  • Pessoa, M., De Vleeschouwer, K. M., Amorim, A. M., & Talora, D. C. (2011). Calendário fenológico. Uma ferramenta para auxiliar no cultivo de espécies arbóreas nativas da floresta Atlântica do Sul da Bahia. Ilhéus, Bahia: Instituto Cabruca. Editus.

    Google Scholar 

  • Pessoa, M. S., De Vleeschouwer, K. M., Talora, D. C., Rocha, L., & Amorim, A. M. (2012). Reproductive phenology of Miconia mirabilis (Melastomataceae) within three distinct physiognomies of Atlantic Forest, Bahia, Brazil. Biota Neotropical, 12, 49–56.

    Article  Google Scholar 

  • Prado, F. (1999). Ecologia, comportamento e conservação do mico-leão-da-cara-preta (Leontopithecus caissara) no Parque Nacional do Superagui, Guaraqueçaba, Paraná. Dissertation: Universidade Federal Paraná.

    Google Scholar 

  • Raboy, B. E. (2002). The ecology and behavior of wild golden-headed lion tamarins (Leontopithecus chrysomelas). Dissertation: University of Maryland.

    Google Scholar 

  • Raboy, B. E., Christman, M. C., & Dietz, J. M. (2004). The use of degraded and shade cocoa forests by endangered golden-headed lion tamarins Leontopithecus chrysomelas. Oryx, 38, 75–83.

    Article  Google Scholar 

  • Raboy, B. E., & Dietz, J. M. (2004). Diet, foraging, and use of space in wild golden-headed lion tamarins. American Journal of Primatology, 63, 1–15.

    Article  PubMed  Google Scholar 

  • Raboy, B. E., Neves, L. N., Zeigler, S., Saraiva, N. A., Cardoso, N., Santos, G. R., Ballou, J. D., & Leimgruber, P. (2010). Strength of habitat and landscape metrics in predicting golden-headed lion tamarin presence or absence in forest patches in Southern Bahia, Brazil. Biotropica, 42, 388–397.

    Article  Google Scholar 

  • Reis, P. (2012). Comportamento do mico-leão-da-cara-dourada, Leontopithecus chrysomelas, em áreas de cabruca do sudeste da Bahia. Dissertation, Universidade Estadual da Santa Cruz, Ilhéus, Bahia, Brazil.

  • Restrepo, C., Gomez, N., & Heredia, S. (1999). Anthropogenic edges, treefall gaps, and fruit-frugivore interactions in a neotropical montane forest. Ecology, 80(2), 668–685.

    Google Scholar 

  • Rode, K. D., Chapman, C. A., McDowell, L. R., & Stickler, C. (2006). Nutritional correlates of population density across habitats and logging intensities in redtail monkeys (Cercopithecus ascanius). Biotropica, 38, 625–634.

    Article  Google Scholar 

  • Rylands, A. B. (1982). The ecology and behavior of three species of marmosets and tamarins (Callitrichidae, Primates) in Brazil. Dissertation: University of Cambridge.

    Google Scholar 

  • Rylands, A. B. (1989). Sympatric callithrichids: The black tuffed ear marmoset, Callithrix kuhli, and the golden-headed lion tamarins, Leontopithecus chrysomelas. Journal of Human Evolution, 18, 679–695.

    Article  Google Scholar 

  • Rylands, A. B. (1996). Habitat and the evolution of social and reproductive behavior in callitrichidae. American Journal of Primatology, 38(1), 5–18.

    Article  Google Scholar 

  • Silva, L. V. C. (1993). Comparação fitossociológica entre duas amostragens numa área de clareira em anos consecutivos, Estação Biológica de Caratinga, MG. Acta Botânica Brasílica, 7, 119–127.

    Article  Google Scholar 

  • Silva, J. M., & Tabarelli, M. (2000). Tree species impoverishment and the future flora of the Atlantic forest of northeast Brazil. Nature, 404(6773), 72–74.

    Article  Google Scholar 

  • Tabarelli, M., Aguiar, A. V., Girão, L. C., Peres, C. A., & Lopes, A. V. (2010). Effects of pioneer tree species hyperabundance on forest fragments in northeastern Brazil. Conservation Biology, 24(6), 1654–1663.

    Article  PubMed  Google Scholar 

  • Tabarelli, M., & Peres, C. A. (2002). Abiotic and vertebrate seed dispersal in the Brazilian Atlantic forest: Implications for forest regeneration. Biological Conservation, 106, 165–176.

    Article  Google Scholar 

  • Tardif, S. D., Santos, C. V., Baker, A. J., Van Elsacker, L., Feistner, A. T. C., Kleiman, D. G., Ruiz-Miranda, C. R., Moura, A. C., Passos, F., Price, E. C., Rappaport, L., & De Vleeschouwer, K. (2002). Infant care and development in lion tamarins. In D. G. Kleiman & A. B. Rylands (Eds.), Lion tamarins: Biology and conservation (pp. 213–232). Washington, DC: Smithsonian Institution Press.

    Google Scholar 

  • Valadares-Pádua, C. B. (1993). The ecology, behavior and conservation of the black-lion tamarins (Leontopithecus chrysopygus, mikan,1823). Dissertation: University of Florida.

    Google Scholar 

  • Watts, D. P., Potts, K. B., Lwanga, J. S., & Mitani, J. C. (2012a). Diet of chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda. 1. Diet composition and diversity. American Journal of Primatology, 74, 114–129.

    Article  PubMed  Google Scholar 

  • Watts, D. P., Potts, K. B., Lwanga, J. S., & Mitani, J. C. (2012b). Diet of chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda. 2. Temporal variation and fallback foods. American Journal of Primatology, 74, 130–144.

    Article  PubMed  Google Scholar 

  • Worman, C. O., & Chapman, C. A. (2006). Densities of two frugivorous primates with respect to forest and fragment tree species composition and fruit availability. International Journal of Primatology, 27(1), 203–225.

    Article  Google Scholar 

  • Zeigler, S., Fagan, W. F., DeFries, R., & Raboy, B. E. (2010). Identifying important forest patches for the long-term persistence of the endangered golden-headed lion tamarin (Leontopithecus chrysomelas). Tropical Conservation Science, 3, 63–77.

    Google Scholar 

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Acknowledgments

We thank Project BioBrasil, the Royal Zoological Society of Antwerp (Belgium), and IESB for their investment in this study, and ICMBio and the reserve directors Saturnino N. F. de Sousa and Paulo C. D. Cruz for support and permission to work inside the Una Biological Reserve. We are grateful to Antonio Ribeiro Santos Junior, José Alves das Neves Filho, and Josinei da Silva Santos for help with data collection and to José Lima Paixão for help with the botanical identifications. We thank the following funding agencies: CNPq, Scott Neotropical Fund of the Cleveland Metroparks Zoo, the Center for Research and Conservation of the Royal Zoological Society of Antwerp, Lion Tamarins of Brazil Fund, National Lottery of Belgium, Primate Action Fund, and Zoological Society of London. The Flemish Ministry of Science (Belgium) provided structural support to the Center for Research and Conservation of the Royal Zoological Society of Antwerp. We thank Paul Garber, Editor-in-Chief Joanna M. Setchell, Lisa G. Rapaport, and two anonymous reviewers for comments on earlier versions of this manuscript, and Nikki Tagg for English editing. This research was authorized by IBAMA permits (Process n° 02001,006792/05-64 (L. S. Catenacci), Process n° 02001,005594/02-31 (K. M. De Vleeschouwer), and Portaria MCT n°195, of March 25 2002 (K. M. De Vleeschouwer).

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The list of plant species (ESM Appendix S1) and nutrient and energy composition of dry matter for 19 fruit species consumed by two groups of golden-headed lion tamarins in Una Biological Reserve from January 2005 through January 2007 (ESM Appendix S2) are available online.

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Catenacci, L.S., Pessoa, M.S., Nogueira-Filho, S.L.G. et al. Diet and Feeding Behavior of Leontopithecus chrysomelas (Callitrichidae) in Degraded Areas of the Atlantic Forest of South-Bahia, Brazil. Int J Primatol 37, 136–157 (2016). https://doi.org/10.1007/s10764-016-9889-x

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