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.
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References
Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267
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
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
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
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
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
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 22:159–168
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
Bicca-Marques JC, Calegaro-Marques C (1994) Exotic plans species can serve as staple food sources for wild howler populations. Folia Primatologia 63(4):209–211
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
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
Byers CR, Steinhorst RK, Krausman PR (1984) Clarification of a technique for analysis of utilization-availability data. J Wildl Manag 48:1050–1053
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
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
Cassano CR, Barlow J, Pardini R (2014) Forest loss or management intensification? Identifying causes of mammal decline in cacao agroforests. Biol Conserv 169:14–22
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
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
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
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 61:397–404
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 32:115–122
Donald PF (2004) Biodiversity impacts of some agricultural commodity production systems. Conserv Biol 18:17–37
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
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
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
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
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 9:735–757
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
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
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
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
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
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
Magurran AE (1988) Ecological diversity and its measurement. Champman and Hall Inc., London
Marsh LK, Chapman CA, Arroyo-Rodríguez V et al (2013) Primates in fragments. Springer, New York
Mech LD (1983) A handbook of animal radio-tracking. University of Minnesota Press, Minneapolis
Mohr CO (1947) Table of equivalent populaions of North American small mammals. Am Midl Nat 37:223–249
Nash LT (1986) Dietary, behavioral, and morphological aspects of gummivory in primates. Yearb Phys Anthropol 29:113–137
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 93
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
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
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
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
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
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
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
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 155–168
Rylands AB (1989) Sympatric brazilian callitrichids: the black tufted-ear marmoset, Callithrix kuhli, and the golden-headed lion tamarin, Leontopithecus chrysomelas. J Human Evol 18:679–695
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
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 262–272
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
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
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
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
Vilela SL (2007) Simpatria e dieta de Callithrix penicillata (Hershkovitz) (Callitrichidae) e Cebus libidinosus (Spix) (Cebidae) em matas de galeria do Distrito Federal. Brasil 24:601–607
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
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
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.
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Ferreira, A.S., Le Pendu, Y. & Martinez, R.A. The use of a mixed rubber landscape by tufted-ear marmosets. Primates 59, 293–300 (2018). https://doi.org/10.1007/s10329-017-0645-4
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DOI: https://doi.org/10.1007/s10329-017-0645-4