Frugivory and potential seed dispersal by the exotic-invasive marmoset Callithrix jacchus (Primates, Callitrichidae) in an urban Atlantic Forest, Rio de Janeiro, Brazil
Abstract
The common marmoset, originally from Northeastern Brazil, has been introduced into several Brazilian states as a result of illegal traffic. Despite the long history of introduction, few studies have described the diet of this primate in regions where it is exotic and none have evaluated its role as a seed disperser. The importance of fruits in the diet of Callithrix jacchus and its potential as a seed disperser were investigated in the Tijuca National Park (TNP, 3.593 ha), southeastern Brazil, where the species is exotic. Data were collected from September 2013 to January 2015, through focal observations. A sampling effort of 361 h of observation resulted in 60 independent feeding records. Fruits were the most often consumed item, comprising 48.3% of the observed feeding records, followed by gum (30%), invertebrates (18.3%) and lichens (3.3%). Seeds from four out of 13 species were swallowed and seeds from seven additional species were found intact in collected feces. These results show C. jacchus’ potential to act as a seed disperser for some plant species, and that should be considered for managing this primate in TNP, where other callitrichids are absent.
Acknowledgments
This article is part of the MSc dissertation of the first author. We thank Peterson de Almeida, Luciana Carnevale, Luiz Siciliano, Rodrigo Zucarato and Thuany Araujo for helping with the fieldwork; Marcelo Souza and Thiago Amorim for plant identification; CAPES and CNPq for grants provided to MAFS and ASP, respectively; ICMBio for providing the license and logistical support at TNP, especially through Katyucha von Kossell de Andrade Silva. L.C. Oliveira, C.E.L. Esberárd and F.A.S Fernandez provided useful suggestions for the first draft of this work. We are in debt to the two anonymous reviewers who besides improving considerably the scientific quality of the manuscript also helped a lot with the English, doing much more than was their job.
References
Alonso, C. and A. Langguth. 1989. Ecologia e comportamento de Callithrix jacchus (Primates: Callitrichidae) numa ilha de Floresta Atlântica. Rev. Nordestina Biol. 6: 105–137.Search in Google Scholar
Amora, T.D., R. Beltrão-Mendes and S.F. Ferrari. 2013. Use of alternative plant resources by common marmosets (Callithrix jacchus) in the semi-arid Caatinga scrub forests of northeastern Brazil. Am. J. Primatol. 75: 333–341.10.1002/ajp.22110Search in Google Scholar PubMed
Angiosperm Phylogeny Group. 2009. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot. J. Linn. Soc. 161: 105–121.10.1111/j.1095-8339.2009.00996.xSearch in Google Scholar
Begotti, R.A. and L.F. Landesmann. 2008. Predação de ninhos por um grupo híbrido de saguis (Callithrix jacchus/penicillata) introduzidos em área urbana: implicações para a estrutura da comunidade. Neotrop. Primates 15: 28–29.10.1896/044.015.0107Search in Google Scholar
Bufalo, F.S., M. Galetti, and L. Culot. 2016. Seed dispersal by primates and implications for the conservation of a biodiversity hotspot, the Atlantic Forest of South America. Int. J. Primatol. 37: 333–349.10.1007/s10764-016-9903-3Search in Google Scholar
Castro, C.S.S. and A. Araujo. 2007. Diet and feeding behavior of marmoset, Callithrix jacchus. Braz. J. Ecol. 7: 14–19.Search in Google Scholar
Castro, C.S.S., A.A.B. Marques, P. Izar, A.C. Oliveira and M.A. Lopes. 2003. The role of primates as seed dispersers in the vegetation structure of tropical forests. Neotrop. Primates 11: 125–127.Search in Google Scholar
Chapman, C.A. and S.E. Russo. 2007. Primate seed dispersal: Linking behavioural ecology and forest community structure. In: (C.J. Campbell, A.F. Fuentes, K.C Mackinnon, M. Panger, and S. Bearder, eds.) Primates in perspective. Oxford University Press, Oxford, pp. 510–525.Search in Google Scholar
Cid, B., L. Figueira, A.F.T. Mello, A.S. Pires and F.A.S. Fernandez. 2014. Short-term success in the reintroduction of the red-rumped agouti Dasyprocta leporina, an important seed disperser, in a Brazilian Atlantic Forest reserve. Trop. Conserv. Sci. 7: 796–810.10.1177/194008291400700415Search in Google Scholar
Coimbra-Filho, A.F. and A.D. Aldrighi. 1971. A restauração da fauna do Parque Nacional da Tijuca. Pub. Avulsas Mus. Nac. 57: 1–30.Search in Google Scholar
Coimbra-Filho, A.F. and R.A. Mittermeier. 1976. Exudate eating and tree gouging in marmosets. Nature 262: 630.10.1038/262630a0Search in Google Scholar
Coimbra-Filho, A.F. and R.A. Mittermeir. 1977. Conservation of the Brazilian lion tamarins (Leontophitecus rosalia). In: (H.R.H. Prince Rainier III and G.H. Bourne eds.) Primate conservation. Academic Press, London. pp. 60–94.Search in Google Scholar
Corrêa, H.K.M., P.E.G. Coutinho and S.F. Ferrari. 2000. Between-year differences in the feeding ecology of highland marmosets (Callithrix aurita and Callithrix flaviceps) in southeastern Brazil. J. Zool. Lond. 252: 421–427.10.1017/S0952836900000170Search in Google Scholar
Cunha, A.A. and M.V. Vieira. 2004. Present and past primate community of the Tijuca Forest, Rio de Janeiro, Brazil. Neotrop. Primates 12: 153–154.10.1896/1413-4705.12.3.153bSearch in Google Scholar
Cunha, A.A., M.V. Vieira and C.E.V. Grelle. 2006. Preliminary observations on habitat, support use and diet in two non-native primates in an urban Atlantic Forest fragment: the capuchin monkey (Cebus sp.) and the common marmoset (Callithrix jacchus) in the Tijuca Forest, Rio de Janeiro. Urban Ecosyst. 9: 351–359.10.1007/s11252-006-0005-4Search in Google Scholar
Davis, M., M.K. Chew, R.J. Hobbs, A.E. Lugo, J.J. Ewel, G.J. Vermeij, J.H. Brown, M.L. Rosenzweig, M.R. Gardener, S.P. Carroll, K. Thompson, S.T.A. Pickett, Juliet C. Stromberg, P. Tredici, K.N. Suding, J. Ehrenfeld, J.M. Grime and J.C. Briggs. 2011. Don’t judge species on their origins. Nature 474: 153–154.10.1038/474153aSearch in Google Scholar PubMed
Dietz, J.M., C.A. Peres and L. Pinder. 1997. Foraging ecology and use of space in wild golden lion tamarins (Leontopithecus rosalia). Am. J. Primatol. 41: 289–305.10.1002/(SICI)1098-2345(1997)41:4<289::AID-AJP2>3.0.CO;2-TSearch in Google Scholar
Digby, L. and C.E. Barreto. 1998. Vertebrate predation in common marmosets. Neotrop. Primates 6: 124–126.Search in Google Scholar
Digby, L.J., S.F. Ferrari and W. Saltzman. 2005. Callitrichines. The role of competition in cooperatively breeding species. In: (K.C. Maclinnon, M. Panger, S. Bearder, C. Campbell and A. Fuentes, eds.) Primates in perspective. Oxford: Oxford University Press. pp. 85–106.Search in Google Scholar
Ferrari, S.F. 1988. The behaviour and ecology of the buffy-headed marmoset, Callithrix flaviceps (O. Thomas, 1903). Thesis (PhD), Universe College of London, UK. pp. 148.Search in Google Scholar
Freitas, S.R., C.L. Neves and P. Chernicharo. 2006. Tijuca National Park: two pioneering restorationist initiatives in Atlantic Forest in southeastern Brazil. Braz. J. Biol. 66: 975–982.10.1590/S1519-69842006000600004Search in Google Scholar
Gautier-Hion, A., J.M. Duplantier, R. Quris, R. Feer, C. Sourd, J.P. Decoux, G. Dubost, L. Emmons, C. Erard, P. Hecketsweiler, A. Moungazi, C. Roussilhon and J.M. Thiollay. 1985. Fruit characters as a basis of fruit choice and seed dispersal in a tropical forest vertebrate community. Oecologia 65: 324–337.10.1007/BF00378906Search in Google Scholar
Genes, L., B. Cid, F.A.S. Fernandez and A.S. Pires. 2017. Credit of ecological interactions: a new conceptual framework to support conservation in a defaunated world. Ecol. Evol. 7: 1892–1897.10.1002/ece3.2746Search in Google Scholar
Hershkovitz, P. 1977. Living new world monkeys (Platyrrhini), v.1. Chicago University Press, Chicago. pp. 132.Search in Google Scholar
Howe, H.F. and J. Smallwood. 1982. Ecology of seed dispersal. Ann. Rev. Ecol. Evol. Syst. 13: 201–228.10.1146/annurev.es.13.110182.001221Search in Google Scholar
ICMBio – Instituto Chico Mendes para a Conservação da Biodiversidade. 2008. Plano de Manejo: Parque Nacional da Tijuca. v.1, Brasília, Brasil.Search in Google Scholar
Jordano, P., M. Galetti, M.A. Pizo and W.R. Silva. 2006. Ligando frugivoria e dispersão de sementes à Biologia da Conservação. In: (C.F.D. Rocha, H.G. Bergallo, M. Van-Sluys and M.A.S. Alves, eds.) Biologia da Conservação: Essências. São Paulo, RiMa. pp. 1–26.Search in Google Scholar
Knight, R.S. and W.R. Siegfried. 1983. Inter-relationships between type, size and color of fruits and dispersal in Southern African trees. Oecologia 56: 405–412.10.1007/BF00379720Search in Google Scholar
Lambert, J.E. and P.A. Garber. 1998. Evolutionary and ecological implications of primate seed dispersal. Am. J. Primatol. 45: 9–28.10.1002/(SICI)1098-2345(1998)45:1<9::AID-AJP3>3.0.CO;2-#Search in Google Scholar
Lapenta, M.J., P. Procópio-de-Oliveira, M.C.M. Kierulff and J.C. Motta-Junior. 2008. Frugivory and seed dispersal of golden lion tamarin (Leontopithecus rosalia (Linnaeus, 1776)) in a forest fragment in the Atlantic Forest, Brazil. Braz. J. Biol. 2: 241–249.10.1590/S1519-69842008000200004Search in Google Scholar
Lorenzi, H. 2000. Árvores brasileiras, v.1. (3a ed.). Instituto Plantarum, Nova Odessa, São Paulo. pp. 1–368.Search in Google Scholar
Lorenzi, H., H.M. Souza, M.A.V. Torres and L.B. Bacher. 2003. Árvores exóticas no Brasil. Madeireiras, ornamentais e aromáticas. Instituto Plantarum, Nova Odessa, São Paulo. pp. 1–385.Search in Google Scholar
Mantilla, G.R. 2012. Ingestão alimentar e nutricional de Callithrix jacchus: relação com hierarquia social e disponibilidade de alimento. Dissertação (Mestrado em Ecologia) – Centro de Biociências, Universidade Federal do Rio Grande do Norte, Natal. pp. 64.Search in Google Scholar
Martinelli, G. and M.A. Moraes. 2013. Livro Vermelho da Flora do Brasil. Instituto de Pesquisas Jardim Botânico, CNC Flora, Rio de Janeiro. pp. 1100.Search in Google Scholar
Martins, I.G. 2007. Padrão de atividades do sagui Callithrix jacchus numa área de Caatinga. Dissertação (Mestrado em Psicobiologia) – Centro de Biociências, Universidade Federal do Rio Grande do Norte, Natal. pp. 67.Search in Google Scholar
Morellato, L.P.C., D.C. Talora, A. Takahasi, C.C. Bencke, E.C. Romera and V.B. Zipparro, V.B. 2000. Phenology of Atlantic Rain Forest trees: a comparative study. Biotropica 32: 811–823.10.1111/j.1744-7429.2000.tb00620.xSearch in Google Scholar
Oliveira, A.C. and S.F. Ferrari. 2000. Seed dispersal by black-handed tamarins, Saguinus midas niger (Callitrichinae, Primates): implications for the regeneration of degraded forest habitats in eastern Amazonia. J. Trop. Ecol. 16: 709–716.10.1017/S0266467400001668Search in Google Scholar
Oliveira, L.D.C. and C.E.V. Grelle. 2012. Introduced primate species of an Atlantic Forest region in Brazil: present and future implications for the native fauna. Trop. Conserv. Sci. 5: 112–120.10.1177/194008291200500110Search in Google Scholar
Passamani, M. and A.B. Rylands. 2000. Feeding behavior of Geoffroy’s marmoset (Callithrix geoffroyi) in an Atlantic Forest fragment of south-eastern Brazil. Primates 41: 27–38.10.1007/BF02557459Search in Google Scholar
Perini, E.S., V.F. Pessoa and D.M.A. Pessoa. 2009. Detection of fruit by the Cerrado’s marmoset (Callithrix penicillata): modeling color signals for different background scenarios and ambient light intensities. J. Exp. Zool. 311A: 289–302.10.1002/jez.531Search in Google Scholar
Power, M.L. 2010. Nutritional and digestive challenges to being a gum-feeding primate. In: (A. Burrows and L. Nash, eds.) The evolution of exudativory in primates. Springer, New York. pp. 25–44.10.1007/978-1-4419-6661-2_2Search in Google Scholar
Power, M.L. and E.W. Myers. 2009. Digestion in the common marmoset (Callithrix jacchus), a gummivore-frugivore. Am. J. Primatol. 71: 957–963.10.1002/ajp.20737Search in Google Scholar
Raboy, B.E., G.E. Canale and J.M. Dietz. 2008. Ecology of Callithrix kuhlii and a review of eastern Brazilian marmosets. Int. J. Primatol. 29: 449–467.10.1007/s10764-008-9249-6Search in Google Scholar
Rangel, C.H., F.S.F Sousa and C.E.V. Grelle. 2011. Dieta de Callithrix jacchus (Linnaeus, 1758) e Callithrix penicillata (E. Geoffroy, 1812) (Callitrichidae – Primates) e seus híbridos, alóctones no Jardim Botânico do Rio de Janeiro. In: (J.M.D. Miranda and Z.M.B. Hirano, eds.) A Primatologia no Brasil. Soc. Bras. Primatol. 12: 74–83.Search in Google Scholar
Reis, N.R., A.L. Peracchi, W.A. Pedro and I.P. Lima. 2011. Mamíferos do Brasil. 2ed. Londrina, PR. pp. 106–117.Search in Google Scholar
Rizzini, C.T. and A.F. Coimbra-Filho. 1981. Lesões produzidas pelo sagui Callithrix p. penicillata (E. Geoffroy, 1812) em árvores do Cerrado (Callitrichidae, Primates). Rev. Bras. Biol. 41: 579–583.Search in Google Scholar
Ruiz-Miranda, C.R., M.M. Morais, V.R. Paula, A.D. Grativol and D. Rambaldi. 2011. Vítimas e vilões: O problema dos saguis introduzidos no Rio de Janeiro. Ciência Hoje 48: 44–49.Search in Google Scholar
Rylands, A.B. 1989. Sympatric Brazilian callitrichids: The black-tufted-ear marmoset, Callithrix kuhlii, and the golden-headed lion tamarin, Leontopithecus chrysomelas. J. Human Evol. 18: 679–695.10.1016/0047-2484(89)90100-0Search in Google Scholar
Rylands, A.B. and D.S. Faria. 1993. Habitats, feeding, and home range size in the genus Callithrix. In: (A.B. Rylands, ed.) Marmosets and tamarins: systemiatics, behaviour, and ecology. Oxford University Press, New York. pp. 262–272.Search in Google Scholar
Rylands, A.B., A.F. Coimbra-Filho and R.A. Mittermeier. 1993. Systematics, geographic distribution, and some notes on the conservation status of the Callitrichidae. In: (A.B. Rylands, ed.) Marmosets and tamarins: systematics, behaviour, and ecology, Oxford University Press, New York. pp. 95–120.Search in Google Scholar
Schupp, E.W. 1993. Quantity, quality and the effectiveness of seed dispersal by animals. Vegetatio 107/108: 15–29.10.1007/978-94-011-1749-4_2Search in Google Scholar
Silva, J.M., J.R. Albuquerque and M.A.B. Oliveira. 2011. Presença de artrópodes na dieta de um grupo de saguis, Callithrix jacchus (Linnaeus,1758) no Parque Estadual Dois Irmãos, Recife-PE, Brasil. In: (J.M.D. Miranda and Z.M.B. Hirano, eds.) A Primatologia no Brasil, Soc. Bras. Primatol. 12: 62–73.Search in Google Scholar
Sinclair, K.E., G.R. Hess, C.E. Moorman and J.H. Mason. 2005. Mammalian nest predators respond to greenway width, landscape context and habitat structure. Landscape Urban Plan. 71: 277–293.10.1016/S0169-2046(04)00082-9Search in Google Scholar
Sussman, R.W. and W.G. Kinzey. 1984. The ecological role of the Callitrichidae: a review. J. Phys. Anthropol. 64: 419–449.10.1002/ajpa.1330640407Search in Google Scholar PubMed
Veríssimo, K.C.S. 2007. Área domiciliar e utilização de recursos alimentares por saguis (Callithrix jacchus) na Reserva Particular do Patrimônio Natural – RPPN Nossa Senhora do Outeiro de Maracaípe, Ipojuca, PE. Dissertação (Mestrado em Biologia Animal) – Centro de Ciências Biológicas, Universidade Federal de Pernambuco, Recife. pp. 72.Search in Google Scholar
Yépez, P., S. de la Torre and C.T. Snowdon. 2005. Interpopulation differences in exudate feeding of pygmy marmosets in Ecuadorian Amazonia. Am. J. Primat. 66: 145–158.10.1002/ajp.20134Search in Google Scholar
Zavaleta, E.S., R.J. Hobbs, R.J and H.A. Mooney. 2001. Viewing invasive species removal in a whole-ecosystem context. Trends Ecol. Evol. 16: 454–459.10.1016/S0169-5347(01)02194-2Search in Google Scholar
©2018 Walter de Gruyter GmbH, Berlin/Boston
Articles in the same Issue
- Frontmatter
- Ecology
- Large mammal richness in Llanganates National Park, Ecuador
- Microhabitat structure and food availability modelling a small mammal assemblage in restored riparian forest remnants
- Determinants of home range size and spatial overlap of Gracilinanus agilis (Mammalia: Didelphidae) in central-western Brazil
- Autumn food habits of the brown bear Ursus arctos in the Golestan National Park: a pilot study in Iran
- Frugivory and potential seed dispersal by the exotic-invasive marmoset Callithrix jacchus (Primates, Callitrichidae) in an urban Atlantic Forest, Rio de Janeiro, Brazil
- Trap type and positioning: how to trap Savi’s pine voles using the tunnel system
- Ethology
- Allosuckling in a captive group of wild cavies Cavia aperea
- Biogeography
- Biogeographic implications of small mammals from Northern Highlands in Tanzania with first data from the volcanic Mount Kitumbeine
- Phylogeography of a widespread sub-Saharan murid rodent Aethomys chrysophilus: the role of geographic barriers and paleoclimate in the Zambezian bioregion
- Taxonomy/phylogeny
- First record of Dermanura anderseni (Chiroptera, Phyllostomidae) for the Atlantic Forest
- Evolutionary biology
- A Quaternary record of the big-eyed bat Chiroderma villosum (Chiroptera: Phyllostomidae) with a revised lower molar terminology
- Conservation
- The Giant Tree Rat, Toromys grandis (Wagner, 1845): new record with range extension and comments on its morphology, biology and conservation
- Andersen’s leaf-nosed bat (Hipposideros pomona) is still living in the Chittagong Hill Tracts, Bangladesh
- Long-term assessment of the success of a European badger reintroduction
Articles in the same Issue
- Frontmatter
- Ecology
- Large mammal richness in Llanganates National Park, Ecuador
- Microhabitat structure and food availability modelling a small mammal assemblage in restored riparian forest remnants
- Determinants of home range size and spatial overlap of Gracilinanus agilis (Mammalia: Didelphidae) in central-western Brazil
- Autumn food habits of the brown bear Ursus arctos in the Golestan National Park: a pilot study in Iran
- Frugivory and potential seed dispersal by the exotic-invasive marmoset Callithrix jacchus (Primates, Callitrichidae) in an urban Atlantic Forest, Rio de Janeiro, Brazil
- Trap type and positioning: how to trap Savi’s pine voles using the tunnel system
- Ethology
- Allosuckling in a captive group of wild cavies Cavia aperea
- Biogeography
- Biogeographic implications of small mammals from Northern Highlands in Tanzania with first data from the volcanic Mount Kitumbeine
- Phylogeography of a widespread sub-Saharan murid rodent Aethomys chrysophilus: the role of geographic barriers and paleoclimate in the Zambezian bioregion
- Taxonomy/phylogeny
- First record of Dermanura anderseni (Chiroptera, Phyllostomidae) for the Atlantic Forest
- Evolutionary biology
- A Quaternary record of the big-eyed bat Chiroderma villosum (Chiroptera: Phyllostomidae) with a revised lower molar terminology
- Conservation
- The Giant Tree Rat, Toromys grandis (Wagner, 1845): new record with range extension and comments on its morphology, biology and conservation
- Andersen’s leaf-nosed bat (Hipposideros pomona) is still living in the Chittagong Hill Tracts, Bangladesh
- Long-term assessment of the success of a European badger reintroduction