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Preliminary findings on social and ecological correlates of a polyspecific association between a golden-headed lion tamarin (Leontopithecus chrysomelas) and Wied’s marmosets (Callithrix kuhlii)

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Abstract

The advantages of living in a group include feeding benefits and/or predation avoidance, while the disadvantages are typically related to competition. One way to avoid competition while maintaining the benefits of living in a group is to form interspecific associations with species with relatively little dietary overlap. Here we report a stable association between a male golden-headed lion tamarin (GHLT), Leontopithecus chrysomelas, and a group of Wied’s black-tufted-ear marmosets (WBTMs), Callithrix kuhlii. We collected ecological and behavioral data on a duo of GHLTs from May to August 2008, totaling 62 h of observations. On 19 August 2008, the radio-collared GHLT dispersed alone and was located on 28 August in association with WBTMs. To examine possible changes in GHLT ecology and behavior, we monitored the mixed-species group between September and December 2008, totaling 122 h of observations. We found that the GHLT’s home range and daily path length decreased by about ten and three times, respectively, after joining the WBTM group, suggesting adaptations to the WBTMs’ use of space. All non-agonistic behaviors recorded in the mixed group were directed from GHLT to the WBMTs, whereas all agonistic interactions were directed from the WBMTs to the GHLT, indicating a subordinate position of GHLT in the mixed group. In golden lion tamarins, reproductive success of subordinate adult males that remain in the group is higher than that of those that disperse and “prospect” for a breeding opportunity. If dispersing individuals are unable to find a mate and defend a territory, they will likely die within a year. The dispersing GHLT in this study assumed a subordinate role in a mixed-species group outside a GHLT territory. Apparently, the benefits of waiting for a dispersing female in a relatively safe situation may exceed the costs of prospecting elsewhere or being a subordinate.

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References

  • Abbott DH (1984) Behavioral and physiological suppression of fertility in subordinate marmoset monkeys. Am J Primatol 6:169–186

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Baker AJ, Dietz JM, Kleiman DG (1993) Behavioral evidence for monopolization of paternity in multi-male groups of golden lion tamarins. Anim Behav 46:1091–1103

    Article  Google Scholar 

  • Beyer HL (2004) Hawth’s analysis tools for ArcGIS. http://www.spatialecology.com/htools. Accessed 4 Sept 2016

  • Buchanan-Smith HM (1999) Tamarin polyspecific associations: forest utilization and stability of mixed-species groups. Primates 40:233–247

    Article  CAS  PubMed  Google Scholar 

  • Chapman CA, Chapman LJ (2000) Interdemic variation in mixed-species association patterns: common diurnal primates of Kibale National Park, Uganda. Behav Ecol Sociobiol 47:129–139

    Article  Google Scholar 

  • Chapman CA, Chapman LJ, Wrangham RW (1995) Ecological constraints on group size: an analysis of spider monkey and chimpanzee subgroups. Behav Ecol Sociobiol 36:59–70

    Article  Google Scholar 

  • Curio E (1976) The ethology of predation. Springer, Berlin

    Book  Google Scholar 

  • Dietz JM, de Sousa SN, da Silva JRO (1994) Population structure and territory size in golden-headed lion tamarins, Leontopithecus chrysomelas. Neotrop Primates 2(Suppl):21–23

    Google Scholar 

  • Dietz JM, de Sousa SN, Billerbeck R (1996) Population dynamics of golden-headed lion tamarins in Una Reserve, Brazil. Dodo J Wildl Preserv Trusts 32:115–122

    Google Scholar 

  • ESRI (2009) ArcGIS desktop: release 9.3.1. Environmental Systems Research Institute, Redlands

  • Ferrari FS (2009) Predation risk and antipredator strategies. In: Garber PA, Estrada A, Bicca-Marques JC, Heymann EW, Strier KB (eds) South American primates—comparative perspectives in the study of behavior, ecology and conservation. Springer, Chicago, pp 251–277

    Google Scholar 

  • Fleury M, Gautier-Hion A (1997) Better to live with allogenerics than to live alone? The case of single male Cercopithecus pogonias in troops of Colobus satanas. Int J Primatol 18:967–974

    Article  Google Scholar 

  • Garber PA (1997) One for all and breeding for one: cooperation and competition as a tamarin reproductive strategy. Evol Anthropol 5:187–198

    Article  Google Scholar 

  • Hamilton WD (1971) Geometry for the selfish herd. J Theor Biol 31:295–311

    Article  CAS  PubMed  Google Scholar 

  • Hardie SM, Buchanan-Smith HM (1997) Vigilance in single- and mixed-species groups of tamarins (Saguinus labiatus and Saguinus fuscicollis). Int J Primatol 18:217–234

    Article  Google Scholar 

  • Heymann EW (1990) Interspecific relations in a mixed-species troop of moustached tamarins, Saguinus mystax, and saddleback tamarins, Saguinus fuscicollis (Primates: Callitrichidae), at the Rio Blanco, Peruvian Amazonia. Am J Primatol 21:115–127

    Article  Google Scholar 

  • Heymann EW, Buchanan-Smith HM (2000) The behavioural ecology of mixed-species troops of callitrichine primates. Biol Rev 75:169–190

    Article  CAS  PubMed  Google Scholar 

  • IUCN (2016) The IUCN red list of threatened species. Version 2016.1. http://www.iucnredlist.org. Accessed 20 Aug 2016

  • Janson CH, Goldsmith ML (1995) Predicting group size in primates: foraging costs and predation risks. Behav Ecol 6:326–336

    Article  Google Scholar 

  • Johns ND (1999) Conservation in Brazil’s chocolate forest: the unlikely persistence of the traditional cocoa agroecosystem. Environ Manage 23:31–47

    Article  CAS  PubMed  Google Scholar 

  • Kierulff MCM, Rylands AB, Mendes SL, de Oliveira MM (2008) Leontopithecus chrysomelas. The IUCN red list of threatened species 2008: http://dx.doi.org/10.2305/IUCN.UK.2008.RLTS.T40643A10347712.en. Accessed 28 Aug 2015

  • Landau EC, Hirsch A, Musinsky J (2003) Cobertura Vegetal e Uso do Solo do Sul da Bahia-Brasil. In: Prado PI, Landau EC, Moura RT, Pinto LPS, Fonesca GAB, Alger K (eds) Corredor de Biodiversidade da Mata Atla˜ntica do Sul da Bahia. IESB/DI/CABS/UFMF/UNICAMP, Publicaça˜o em CD-ROM, Ilhe´us, Brazil

  • Lucas JR, Waser MP, Creel SR (1994) Death and disappearance: estimating mortality risks associated with philopatry and dispersal. Behav Ecol 5:135–141

    Article  Google Scholar 

  • McNamara JM, Houston AI (1987) Starvation and predation as factors limiting population size. Ecology 68:1515–1519

    Article  Google Scholar 

  • MMA (2014) Lista nacional oficial de espécies da fauna ameaçadas de extinção. Portaria no. 444, 17 dezembro 2014

  • Mohr C (1947) Table of equivalent populations of North American small mammals. Am Midl Nat 37:223–449

    Article  Google Scholar 

  • Oliveira LC, Dietz MJ (2011) Predation risk and the interspecific association of two Brazilian Atlantic Forest primates in cabruca agroforest. Am J Primatol 73:852–860

    Article  PubMed  Google Scholar 

  • Oliveira LC, Hankerson S, Dietz JM, Raboy BE (2010) Key tree species for the golden-headed lion tamarin and implications for shade-cocoa management in southern Bahia, Brazil. Anim Conserv 13:60–70

    Article  Google Scholar 

  • Oliveira LC, Neves LG, Raboy BE, Dietz JM (2011) Abundance of jackfruit (Artocarpus heterophyllus) affects group characteristics and use of space by golden-headed lion tamarins (Leontopithecus chrysomelas) in cabruca agroforest. Environ Manage 48(2):248–262

    Article  PubMed  Google Scholar 

  • Olupot W, Waser PM (2001) Activity patterns, habitat use and mortality risks of mangabey males living outside social groups. Anim Behav 61:1227–1235

    Article  Google Scholar 

  • Peres CA (1992) Prey-capture benefits in a mixed-species group of Amazonian tamarins, Saguinus fuscicollis and S. mystax. Behav Ecol Sociobiol 31:339–347

    Article  Google Scholar 

  • Peres CA (1993) Anti-predator benefits in a mixed-species group of Amazonian tamarins. Folia Primatol 61:61–76

    Article  CAS  PubMed  Google Scholar 

  • Peres CA (1996) Food patch structure and plant resource partitioning in inter-specific associations of Amazonian tamarins. Int J Primatol 17:695–723

    Article  Google Scholar 

  • Raboy BE (2002) The ecology and behavior of wild golden-headed lion tamarins (Leontopithecus chrysomelas). Department of Biology, University of Maryland, College Park, MD

  • Raboy BE, Dietz JM (2004) Diet, foraging, and the use of space in wild golden-headed lion tamarins. Am J Primatol 63:1–15

    Article  PubMed  Google Scholar 

  • Raboy BE, Canale G, Dietz JM (2008) Ecology of Callithrix kuhlii and a review of eastern Brazilian marmosets. Int J Primatol 29:449–467

    Article  Google Scholar 

  • R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/. Accessed 4 Sept 2016

  • Rylands AB (1989) Sympatric Brazilian callitrichids: the black tufted-ear marmoset, Callithrix kuhli, and the golden-headed lion tamarin, Leontopithecus chrysomelas. J Hum Evol 18:679–695

    Article  Google Scholar 

  • Rylands AB, Kierullf MCM (2008) Callithrix kuhlii. IUCN red list of threatened species 2008: http://dx.doi.org/10.2305/IUCN.UK.2008.RLTS.T3575A9955873.en. Accessed 28 Aug 2015

  • Sambuichi RHR, Haridasan M (2007) Recovery of species richness and conservation of native Atlantic forest trees in the cacao plantations of southern Bahia in Brazil. Biodivers Conserv 16:3681–3701

    Article  Google Scholar 

  • Schino G (2001) Grooming, competition and social rank among female primates: a meta-analysis. Anim Behav 62:265–271

    Article  Google Scholar 

  • Seyfarth RM (1976) Social relationships among adult female baboons. Anim Behav 24:917–938

    Article  Google Scholar 

  • Seyfarth RM (1977) A model of social grooming among adult female monkeys. J Theor Biol 65:671–698

    Article  CAS  PubMed  Google Scholar 

  • Stensland E, Angerbjorn A, Berggren P (2003) Mixed species groups in mammals. Mamm Rev 33:205–223

    Article  Google Scholar 

  • Struhsaker TT (1988) Male tenure, multi-male influxes, and reproductive success in redtail monkeys (Cercopithecus ascanius). In: Gautier-Hion A, Bourliere F, Gautier JP, Kingdon J (eds) A primate radiation; evolutionary biology of the African guenons. Cambridge University Press, London, pp 340–363

    Google Scholar 

  • Terborgh J (1983) Five new world primates. Princeton University Press, Princeton

    Google Scholar 

  • Terborgh J (1986) The social systems of new world primates: an adaptationist view. In: Else JG, Lee PC (eds) Primate ecology and conservation. Cambridge University Press, Cambridge, pp 199–211

    Google Scholar 

  • Terborgh J (1990) Mixed flocks and polyspecific associations: costs and benefits of mixed groups to birds and monkeys. Am J Primatol 21:87–100

    Article  Google Scholar 

  • Terborgh J, Janson CH (1986) The socioecology of primate groups. Annu Rev Ecol Syst 17:111–136

    Article  Google Scholar 

  • Treves A, Chapman CA (1996) Conspecific threat, predation avoidance, and resource defense: implications for grouping in langurs. Behav Ecol Sociobiol 39:43–53

    Article  Google Scholar 

  • van Schaik CP (1983) Why are diurnal primates living in groups? Behaviour 87(1/2):120–144

    Article  Google Scholar 

  • van Schaik CP, van Hooff JA (1983) On the ultimate causes of primate social systems. Behaviour 85:91–117

    Article  Google Scholar 

  • van Schaik CP, van Noordwijk MA, Warsono B, Sutriono E (1983) Party size and early detection of predators in Sumatran forest primates. Primates 24:211–221

    Article  Google Scholar 

  • Wachter B, Schabel M, Noe R (1997) Diet overlap and polyspecific associations of red colobus and Diana monkeys in the Tai National Park, Ivory Coast. Ethology 103:514–526

    Article  Google Scholar 

  • Whitesides GH (1989) Interspecific associations of Diana monkeys, Cercopithecus diana, in Sierra Leone, West Africa: biological significance or chance? Anim Behav 37:760–776

    Article  Google Scholar 

  • Wrangham RW, Gittleman JL, Chapman CA (1993) Constraints on group size in primates and carnivores: population density and day-range as assays of exploitation competition. Behav Ecol Sociobiol 32:199–210

    Article  Google Scholar 

Download references

Acknowledgments

We thank the Brazilian Institute of the Environment and Renewable Natural Resources (Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis) and the Instituto Chico Mendes de Biodiversidade for the permits to capture the study group. We are grateful to the owners and employees of the São José and Sempre Viva farms, especially to Sr Elias. We are grateful to Fábio Falcão and Gastón Giné for their help with the data analysis. We also thank our field team: Leonardo Neves, Jiomário dos Santos Souza, and Edimalvan da Purificação. Financial support was provided by the University of Maryland Biology Department, Seeds of Change, Lion Tamarins of Brazil Fund, the Wildlife Conservation Society, International Foundation for Science, the Rufford Small Grants Foundation and Idea Wild. L. C. O. received doctoral fellowships from the University of Maryland (College of Chemical and Life Sciences Board of Visitors, Ann G. Wylie Dissertation Fund, Drs Wayne T. and Mary T. Hockmeyer Doctoral Fellowship), and from the Fundação Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Fulbright.

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Authors and Affiliations

  1. Departamento de Ciências, Faculdade de Formação de Professores, Universidade do Estado do Rio de Janeiro (UERJ), Rua Dr. Francisco Portela, 1470-Patronato, CEP 24435-005, São Gonçalo, RJ, Brazil

    Leonardo de Carvalho Oliveira

  2. Program in Behavior, Ecology, Evolution and Systematics, University of Maryland, College Park, MD, 20742, USA

    James Dietz

  3. Programa de pós-graduação em Ecologia e Conservação da Biodiversidade, Universidade Estadual de Santa Cruz (UESC), Salobrinho, CEP 45662-900, Ilhéus, BA, Brazil

    Leonardo de Carvalho Oliveira, Juliana Monteiro de Almeida Rocha & Paula Pedreira dos Reis

  4. Instituto de Estudos Socioambientais do Sul da Bahia (IESB), Rua Araujo Pinho, 72-3° Andar, Centro, CEP 45.653-145, Ilhéus, BA, Brazil

    Paula Pedreira dos Reis

  5. Bicho do Mato Instituto de Pesquisa, Av. Cônsul Antônio Cadar, 600, CEP 30360-082, Belo Horizonte, MG, Brazil

    Leonardo de Carvalho Oliveira

  6. Save the Golden Lion Tamarin, Silver Spring, MD, USA

    James Dietz

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  1. Leonardo de Carvalho Oliveira
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  2. Juliana Monteiro de Almeida Rocha
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  4. James Dietz
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Correspondence to Leonardo de Carvalho Oliveira.

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Ethical approval

All animal captures were approved by the Brazilian Environmental Agency (ICMBio/SISBIO) under permit nos. 18444-1 and 12334-1. In addition, this research adhered to the American Society of Primatologists’ ethical principles for the treatment of primates.

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de Carvalho Oliveira, L., de Almeida Rocha, J.M., dos Reis, P.P. et al. Preliminary findings on social and ecological correlates of a polyspecific association between a golden-headed lion tamarin (Leontopithecus chrysomelas) and Wied’s marmosets (Callithrix kuhlii). Primates 58, 179–186 (2017). https://doi.org/10.1007/s10329-016-0580-9

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