Advertisement

Primates

, Volume 59, Issue 3, pp 293–300 | Cite as

The use of a mixed rubber landscape by tufted-ear marmosets

  • Aluane S. Ferreira
  • Yvonnick Le Pendu
  • Romari A. MartinezEmail author
Original Article
  • 154 Downloads

Abstract

With the loss and fragmentation of tropical forests, the survival of primates depends on their ability to adapt to human-introduced modifications in their habitat. Marmosets are known for their ecological and behavioral plasticity and have been registered in various agricultural landscapes. Our goal was to describe the ecology of tufted-ear marmosets (Callithrix sp.) in a rubber/forest landscape, monitoring their use of habitat and diet. We followed two groups using radio telemetry and visual observations for nine months at the Michelin plantation Ltd. in Bahia, Brazil. Both groups used mainly pioneer forest and rubber with pioneer vegetation more than expected according to availability, even though they explored all types of vegetation. Rubber monocultures act as corridors for marmoset locomotion among more suitable habitats. Feeding, gummivory and socialization were mainly performed in the pioneer forest (with or without rubber), in which most sleeping sites and food sources were found. Groups of marmosets can incorporate agroforest matrixes to their area of use and activity patterns. Maintenance of marmosets in fragmented landscapes might be favored by their diet flexibility, with the use of resources such as gum and fruit, including exotic plants. Although known for their ecological flexibility, marmosets do require certain resources to be present in native habitat to adapt to agricultural landscapes. Patches of forest within a rubber landscape and pioneer vegetation in the rubber inter-rows should be considered to maintain populations of Callithrix in rubber landscapes.

Keywords

Callithrichids Agroforests Fragmentation Vegetation use 

Notes

Acknowledgements

We would like to thank Michelin plantations Ltd. for logistical support and for the grant to R. Martinez that made possible to count on L. Neves for essential technical assistance during our fieldwork. A.S.F. had an MSc Grant from the Comissão de Aperfeiçõamento Profissional do Ensino Superior (CAPES). The State University of Santa Cruz provided financial support. Ariane Ferreira and Jiómario Souza helped in the field. Jose Lima and Larissa Rocha identified most of the collected plants. Veterinarian Paula Reis acted as the main person responsible for capture of the marmosets and medical procedures. Juliana Monteiro helped with data analysis. Thanks to Camila Cassano, Gastón Giné, Nayara Cardoso, Gustavo Canale, Leonardo Neves and Kevin Flesher for suggestions and corrections to the original manuscript. This research complies with all Brazilian laws and regulations for working with wild animals, and was approved by the National Institute for Biodiversity Conservation (ICMBio), license number 37876-1.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This research was approved by the Ethical Committee on Animal Welfare of UESC, and complies with all ethical regulations regarding animal manipulation in the field.

References

  1. Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267CrossRefPubMedGoogle Scholar
  2. Anderson JR (1998) Sleep, sleeping sites, and sleep-related activities: awakening to their significance. Am J Primatol 46:63–75.  https://doi.org/10.1002/(SICI)1098-2345(1998)46:1<63 CrossRefPubMedGoogle Scholar
  3. Anderson J, Rowcliffe JM, Cowlishaw G (2007) Does the matrix matter? A forest primate in a complex agricultural landscape. Biol Conserv 135:212–222.  https://doi.org/10.1016/j.biocon.2006.10.022 CrossRefGoogle Scholar
  4. Antongiovanni M, Metzger JP (2005) Influence of matrix habitats on the occurrence of insectivorous bird species in Amazonian forest fragments. Biol Conserv 122:441–451.  https://doi.org/10.1016/j.biocon.2004.09.005 CrossRefGoogle Scholar
  5. Arroyo-Rodríguez V, Fahrig L (2014) Why is a landscape perspective important in studies of primates? Am J Primatol 76:901–909.  https://doi.org/10.1002/ajp.22282 CrossRefPubMedGoogle Scholar
  6. Arroyo-Rodríguez V, González-Perez IM, Garmendia A et al (2013) The relative impact of forest patch and landscape attributes on black howler monkey populations in the fragmented Lacandona rainforest, Mexico. Landsc Ecol 28:1717–1727.  https://doi.org/10.1007/s10980-013-9929-2 CrossRefGoogle Scholar
  7. Bernard H, Bili R, Wearn OR et al (2014) The distribution and persistence of primate species in disturbed and converted forest landscapes in Sabah, Malaysia: preliminary results. Annu Rep Pro Nat Fund 22:159–168Google Scholar
  8. Bhagwat SA, Willis KJ, Birks HJB, Whittaker RJ (2008) Agroforestry: a refuge for tropical biodiversity? Trends Ecol Evol 23:261–267.  https://doi.org/10.1016/j.tree.2008.01.005 CrossRefPubMedGoogle Scholar
  9. Bicca-Marques JC, Calegaro-Marques C (1994) Exotic plans species can serve as staple food sources for wild howler populations. Folia Primatologia 63(4):209–211CrossRefGoogle Scholar
  10. Brooks TM, Bakarr MI, Boucher T et al (2004) Coverage provided by the global protected-area system: is it enough? Bioscience 54:1081–1091.  https://doi.org/10.1641/0006-3568(2004)054 CrossRefGoogle Scholar
  11. Brum FT, Debastiani VJ, Loyola R, Duarte LDS (2014) Clade-specific impacts of human land use on primates. Nat Conserv 12:144–149.  https://doi.org/10.1016/j.ncon.2014.09.009 CrossRefGoogle Scholar
  12. Byers CR, Steinhorst RK, Krausman PR (1984) Clarification of a technique for analysis of utilization-availability data. J Wildl Manag 48:1050–1053CrossRefGoogle Scholar
  13. Caryl FM, Quine CP, Park KJ (2012) Martens in the matrix: the importance of nonforested habitats for forest carnivores in fragmented landscapes. J Mammal 93:464–474.  https://doi.org/10.1644/11-MAMM-A-149.1 CrossRefGoogle Scholar
  14. Cassano CR, Barlow J, Pardini R (2012) Large mammals in an agroforestry mosaic in the Brazilian Atlantic Forest. Biotropica 44:818–825.  https://doi.org/10.1111/j.1744-7429.2012.00870.x CrossRefGoogle Scholar
  15. Cassano CR, Barlow J, Pardini R (2014) Forest loss or management intensification? Identifying causes of mammal decline in cacao agroforests. Biol Conserv 169:14–22CrossRefGoogle Scholar
  16. Chape S, Harrison J, Spalding M, Lysenko I (2005) Measuring the extent and effectiveness of protected areas as an indicator for meeting global biodiversity targets. Philos Trans R Soc B Biol Sci 360:443–455.  https://doi.org/10.1098/rstb.2004.1592 CrossRefGoogle Scholar
  17. Chapman CA, Chapman LJ, McLaughlin RL (1989) Multiple central place foraging by spider monkeys: travel consequences of using many sleeping sites. Oecologia 79:506–511.  https://doi.org/10.1007/BF00378668 CrossRefPubMedGoogle Scholar
  18. Coleman BT, Hill RA (2014) Living in a landscape of fear: the impact of predation, resource availability and habitat structure on primate range use. Anim Behav 88:165–173.  https://doi.org/10.1016/j.anbehav.2013.11.027 CrossRefGoogle Scholar
  19. de Miranda GH, de Faria DS (2001) Ecological aspects of black-pincelled marmoset (Callithrix penicillata) in the cerradão and dense cerrado of the Brazilian central plateau. Braz J Biol 61:397–404CrossRefPubMedGoogle Scholar
  20. Dietz JM, De Souza SN, Billerbeck R (1996) Population dynamics of golden-headed lion tamarins Leontopithecus chrysomelas in Una Reserve, Brazil. Dodo, J Wildlife Preser Trust 32:115–122Google Scholar
  21. Donald PF (2004) Biodiversity impacts of some agricultural commodity production systems. Conserv Biol 18:17–37CrossRefGoogle Scholar
  22. Estrada A, Raboy BE, Oliveira LC (2012) Agroecosystems and primate conservation in the tropics: a review. Am J Primatol 74:696–711.  https://doi.org/10.1002/ajp.22033 CrossRefPubMedGoogle Scholar
  23. Estrada A, Garber PA, Rylands AB et al (2017) Impending extinction crisis of the world’s primates: why primates matter. Sci Adv 3:1–16.  https://doi.org/10.1126/sciadv.1600946 CrossRefGoogle Scholar
  24. Flesher KM (2015) The distribution, habitat use, and conservation status of three Atlantic forest monkeys (Sapajus xanthosternos, Callicebus melanochir, Callithrix sp.) in an agroforestry/forest mosaic in Southern Bahia, Brazil. Int J Primatol 36:1172–1197.  https://doi.org/10.1007/s10764-015-9884-7 CrossRefGoogle Scholar
  25. Foley JA, DeFries R, Asner GP et al (2005) Global consequences of land use. Science 80(309):570–574.  https://doi.org/10.1126/science.1111772 CrossRefGoogle Scholar
  26. Guy C, Cassano CR, Cazarre L et al (2016) Evaluating landscape suitability for golden-headed lion tamarins (Leontopithecus chrysomelas) and Wied’s black tufted-ear marmosets (Callithrix kuhlii) in the Bahian Atlantic forest. Trop Conserv Sci 9:735–757CrossRefGoogle Scholar
  27. Isabirye-Basuta GM, Lwanga JS (2008) Primate populations and their interactions with changing habitats. Int J Primatol 29:35–48.  https://doi.org/10.1007/s10764-008-9239-8 CrossRefGoogle Scholar
  28. Jenkins CN, Joppa L (2009) Expansion of the global terrestrial protected area system. Biol Conserv 142:2166–2174.  https://doi.org/10.1016/j.biocon.2009.04.016 CrossRefGoogle Scholar
  29. Kupfer JA, Malanson GP, Franklin SB (2006) Not seeing the ocean for the islands: the mediating influence of matrix-based processes on forest fragmentation effects. Glob Ecol Biogeogr 15:8–20.  https://doi.org/10.1111/j.1466-822X.2006.00204.x CrossRefGoogle Scholar
  30. Lindenmayer DB, Cunningham RB, Pope ML (1999) A large-scale “experiment” to examine the effects of landscape context and habitat fragmentation on mammals. Biol Conserv 88:387–403.  https://doi.org/10.1016/S0006-3207(98)00111-6 CrossRefGoogle Scholar
  31. Lindenmayer DB, Cunningham RB, MacGregor C et al (2001) A prospective longitudinal study of landscape matrix effects on fauna in woodland remnants: experimental design and baseline data. Biol Conserv 101:157–169.  https://doi.org/10.1016/S0006-3207(01)00061-1 CrossRefGoogle Scholar
  32. Lutermann H, Verburgt L, Rendigs A (2010) Resting and nesting in a small mammal: sleeping sites as a limiting resource for female grey mouse lemurs. Anim Behav 79:1211–1219.  https://doi.org/10.1016/j.anbehav.2010.02.017 CrossRefGoogle Scholar
  33. Magurran AE (1988) Ecological diversity and its measurement. Champman and Hall Inc., LondonCrossRefGoogle Scholar
  34. Marsh LK, Chapman CA, Arroyo-Rodríguez V et al (2013) Primates in fragments. Springer, New YorkCrossRefGoogle Scholar
  35. Mech LD (1983) A handbook of animal radio-tracking. University of Minnesota Press, MinneapolisGoogle Scholar
  36. Mohr CO (1947) Table of equivalent populaions of North American small mammals. Am Midl Nat 37:223–249CrossRefGoogle Scholar
  37. Nash LT (1986) Dietary, behavioral, and morphological aspects of gummivory in primates. Yearb Phys Anthropol 29:113–137CrossRefGoogle Scholar
  38. Neves LG (2008) Distribuição geográfica e conservação de Callithrix kuhlii (Coimbra-Filho, 1985) no Sul da Bahia, Brasil. MSc in Zoology Thesis. Universidade Estadual de Santa Cruz, Ilhéus, Bahia, p 93Google Scholar
  39. Oliveira LC, Dietz JM (2011) Predation risk and the interspecific association of two Brazilian Atlantic forest primates in Cabruca agroforest. Am J Primatol 73:852–860.  https://doi.org/10.1002/ajp.20952 CrossRefPubMedGoogle Scholar
  40. 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 Manag 48:248–262.  https://doi.org/10.1007/s00267-010-9582-3 CrossRefGoogle Scholar
  41. Oliveira LC, de Almeida Rocha JM, dos Reis PP, Dietz J (2016) 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.  https://doi.org/10.1007/s10329-016-0580-9 PubMedGoogle Scholar
  42. Perfecto I, Vandermeer J (2008) Biodiversity conservation in tropical agroecosystems: a new conservation paradigm. Ann N Y Acad Sci 1134:173–200.  https://doi.org/10.1196/annals.1439.011 CrossRefPubMedGoogle Scholar
  43. Phoonjampa R, Koenig A, Borries C et al (2010) Selection of sleeping trees in pileated gibbons (Hylobates pileatus). Am J Primatol 72:617–625.  https://doi.org/10.1002/ajp.20818 PubMedGoogle Scholar
  44. Raboy BE, Canale GR, Dietz JM (2008) Ecology of Callithrix kuhlii and a review of Eastern Brazilian marmosets. Int J Primatol 29:449–467.  https://doi.org/10.1007/s10764-008-9249-6 CrossRefGoogle Scholar
  45. Rodrigues NN, Martinez RA (2014) Wildlife in our backyard: interactions between Wied’s marmoset Callithrix kuhlii (Primates: Callithrichidae) and residents of Ilhéus, Bahia, Brazil. Wildl Biol 20:91–96.  https://doi.org/10.2981/wlb.13057 CrossRefGoogle Scholar
  46. Rylands AB (1984) Exudate-eating and tree-gouging by marmosets (Callitrichidae, Primates). In: Chadwick AC, Sutton SL (eds) Tropical rain forest: the Leeds Symposium and Literary Society. Leeds Philosophical and Literary Society, Leeds, pp 155–168Google Scholar
  47. Rylands AB (1989) Sympatric brazilian callitrichids: the black tufted-ear marmoset, Callithrix kuhli, and the golden-headed lion tamarin, Leontopithecus chrysomelas. J Human Evol 18:679–695CrossRefGoogle Scholar
  48. Rylands AB (1996) Habitat and the evolution of social and reproductive behavior in callitrichidae. Am J Primatol 38:5–18.  https://doi.org/10.1002/(SICI)1098-2345(1996)38:1<5:AID-AJP2>3.0.CO;2-2 CrossRefGoogle Scholar
  49. Rylands AB, Faria DS (1993) Habitats, feeding ecology, and home range size in the genus Callithrix. In: Rylands AB (ed) Marmosets and tamarins: systematics, behaviour, and ecology. Oxford University Press, Oxford, pp 262–272Google Scholar
  50. Smith AC, Knogge C, Huck M et al (2007) Long-term patterns of sleeping site use in wild saddleback (Saguinus fuscicollis) and mustached tamarins (S. mystax): effects of foraging, thermoregulation, predation, and resource defense constraints. Am J Phys Anthropol 134:340–358.  https://doi.org/10.1002/ajpa.20676 CrossRefPubMedGoogle Scholar
  51. Teixeira B, Hirsch A, Goulart VDL et al (2015) Good neighbours: distribution of black-tufted marmoset (Callithrix penicillata) in an urban environment. Wildl Res 42:579–589.  https://doi.org/10.1071/WR14148 CrossRefGoogle Scholar
  52. Tisovec KC, Cassano CR, Boubli JP, Pardini R (2014) Mixed-species groups of marmosets and tamarins across a gradient of agroforestry intensification. Biotropica 46:248–255.  https://doi.org/10.1111/btp.12098 CrossRefGoogle Scholar
  53. Umetsu F, Paul Metzger J, Pardini R (2008) Importance of estimating matrix quality for modeling species distribution in complex tropical landscapes: a test with Atlantic forest small mammals. Ecography (Cop) 31:359–370.  https://doi.org/10.1111/j.2008.0906-7590.05302.x CrossRefGoogle Scholar
  54. Vilela SL (2007) Simpatria e dieta de Callithrix penicillata (Hershkovitz) (Callitrichidae) e Cebus libidinosus (Spix) (Cebidae) em matas de galeria do Distrito Federal. Brasil 24:601–607Google Scholar
  55. Vilela SL, de Faria DS (2004) Seasonality of the activity pattern of Callithrix penicillata (Primates, Callitrichidae) in the Cerrado (Scrub Savanna Vegetation) Brazilian. J Biol 64:363–370.  http:doi.org/10.1590/S1519-69842004000200023 Google Scholar
  56. Zago L, Miranda JMD, Neto CD et al (2013) Dieta de Callithrix penicillata (E. Geoffroy, 1812) (Primates, Callitrichidae) introduzidos na Ilha de Santa Catarina. Biotemas 26:227–235.  https://doi.org/10.5007/2175-7925.2013v26n2p227 Google Scholar

Copyright information

© Japan Monkey Centre and Springer Japan KK, part of Springer Nature 2017

Authors and Affiliations

  1. 1.Applied Ecology and Conservation Lab, Programa de Pós-Graduação em Ecologia e Conservação da BiodiversidadeUniversidade Estadual de Santa Cruz (UESC)IlhéusBrazil
  2. 2.Programa de Pós-Graduação em ZoologiaUESCIlhéusBrazil
  3. 3.Departamento de Ciências BiológicasUESCIlhéusBrazil
  4. 4.Departamento de Filosofia e Ciências HumanasUESCIlhéusBrazil

Personalised recommendations