Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-13T00:41:45.884Z Has data issue: false hasContentIssue false
  • English
  • Français

Habitat selection by the black-tufted marmoset Callithrix penicillata in human-disturbed landscapes

Published online by Cambridge University Press:  15 March 2018

Helio Secco Open the ORCID record for Helio Secco [Opens in a new window] ,
Clara Grilo  and
Alex Bager
Helio Secco*
Affiliation:
Programa de Pós-Graduação em Ecologia Aplicada, Departamento de Biologia, Universidade Federal de Lavras, Campus Universitário, CP 3037, Lavras, CEP 37200 000Brasil
Clara Grilo
Affiliation:
Programa de Pós-Graduação em Ecologia Aplicada, Departamento de Biologia, Universidade Federal de Lavras, Campus Universitário, CP 3037, Lavras, CEP 37200 000Brasil
Alex Bager
Affiliation:
Centro Brasileiro de Estudos em Ecologia de Estradas, Universidade Federal de Lavras, Campus Universitário, CP 3037, Lavras, CEP 37200 000Brasil
*
*Corresponding author. Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract:

There are several primate species with high risk of extinction in small forest fragments disturbed by human activities. However, some species exhibit high ecological plasticity, which allows them to persist in human-modified landscapes. The main goal of this study is to examine the relative roles of vegetation (mean distance among trees and mean canopy cover), human disturbance (distance to the road, distance to the fragment edge and edge type), and habitat spatial configuration (spatial autocorrelation index, category of quadrat – position within the fragment/fragment type) on the habitat selection of the black-tufted marmoset Callithrix penicillata in forest patches. We selected forest patches near and away from roads/urban areas, in southern Minas Gerais state, south-eastern Brazil. We used generalized linear mixed models to explain the presence of black-tufted marmoset in those patches. Our results show that black-tufted marmoset tend to occupy forest fragments closer to roads/urban areas, and consequently are under the influence of anthropic disturbance. In addition to the area delimited by these fragments, there is a preference for edge environments, where disturbances are exacerbated and the ecological conditions are suitable for exploitation by the black-tufted marmoset (supply of gum trees and reduced risk of competition). We suggest that a cross-habitat spillover by marmoset occur from forests to small habitat patches close to human-modified areas, such as those in proximity to roads and urban zones.

Keywords

anthropogenic landscapescross-habitat spilloveredge effectsprimatesspatial ecology
Type
Research Article
Information
Journal of Tropical Ecology , Volume 34 , Issue 2 , March 2018 , pp. 135 - 144
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

LITERATURE CITED

ALEXANDRINO, E. R., LUZ, D. T. A., MAGGIORINI, E. V. & FERRAZ, K. M. P. M. D. 2012. Nest stolen: the first observation of nest predation by an invasive exotic marmoset (Callithrix penicillata) in an agricultural mosaic. Biota Neotropica 12:211–215.CrossRefGoogle Scholar
ANDRÉN, H. 1995. Effects of landscape composition on predation rates at habitat edges. Pp. 225–255 in Hansson, L., Fahrig, L. & Merrian, G. (eds). Mosaic landscapes and ecological processes. Springer, Dordrecht.CrossRefGoogle Scholar
ARROYO-RODRÍGUEZ, V. & MANDUJANO, S. 2006. Forest fragmentation modifies habitat quality for Alouatta palliata. International Journal of Primatology 27:1079–1096.CrossRefGoogle Scholar
BATÁRY, P. & BÁLDÍ, A. 2004. Evidence of an edge effect on avian nest success. Conservation Biology 18:389–400.CrossRefGoogle Scholar
BLITZER, E. J., DORMANN, C. F., HOLZSCHUH, A., KLEIN, A. M., RAND, T. A. & TSCHARNTKE, T. 2012. Spillover of functionally important organisms between managed and natural habitats. Agriculture, Ecosystems & Environment 146:34–43.CrossRefGoogle Scholar
BOLKER, B. M., BROOKS, M. E., CLARK, C. J., GEANGE, S. W., POULSEN, J. R., STEVENS, M. H. H. & WHITE, J. S. S. 2008. Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology & Evolution 24:127–136.CrossRefGoogle Scholar
BURNHAM, K. P. & ANDERSON, D. R. 2002. Model selection and multimodel inference: a practical information-theoretic approach. (Second edition). Springer-Verlag, New York.Google Scholar
CANALE, G., BRAGA, A., GONDIM, L. & SANTEE, D. V. 2008. Sequência de comportamentos de Callithrix penicillata durante a gomivoria. Pp. 49–59 in Ferrari, S. F. & Rimoli, L. (eds). A primatologia no Brasil. Sociedade Brasileira de Primatologia, Biologia Geral e Experimental – UFS, Aracaju.Google Scholar
CHAPMAN, C. A. & RUSSO, S. E. 2007. Primate seed dispersal. Primates in perspective. Oxford University Press, New York. 720 pp.Google Scholar
CLARKE, M. R., COLLINS, D. A. & ZUCKER, E. L. 2002. Responses to deforestation in a group of mantled howlers (Alouatta palliata) in Costa Rica. International Journal of Primatology 23:365–381.CrossRefGoogle Scholar
CLAUZEL, C., DENG, X., WU, G., GIRAUDOUX, P. & LI, L. 2015. Assessing the impact of road developments on connectivity across multiple scales: application to Yunnan snub-nosed monkey conservation. Biological Conservation 192:207–217.CrossRefGoogle Scholar
COLLINGE, S. K. 2009. Ecology of fragmented landscapes. The John Hopkins University Press, Baltimore. 360 pp.CrossRefGoogle Scholar
DALANESI, P.E., OLIVEIRA-FILHO, A.T. & FONTES, M.A.L. 2004. Flora e estrutura do componente arbóreo da floresta do Parque Ecológico Quedas do Rio Bonito, Lavras, MG, e correlação entre a distribuição das espécies e variáveis ambientais. Acta Botanica Brasilica 18:737–757.CrossRefGoogle Scholar
DE LA TORRE, S., SNOWDON, C. T. & BEJARANO, M. 2000. Effects of human activities on wild pygmy marmosets in Ecuadorian Amazonia. Biological Conservation 94:153–163.CrossRefGoogle Scholar
DIGBY, L. J., FERRARI, S. F. & SALTZMAN, W. 2007. Callitrichines: the role of competition in cooperatively breeding species. Pp. 85–106 in Campbell, C., Fuentes, A., MacKinnon, K. C., Panger, M. & Bearder, S. (eds). Primates in perspective. Oxford University Press, New York.Google Scholar
DORNELES, L. P. P. & WAECHTER, J. L. 2004. Fitossociologia do componente arbóreo na floresta turfosa do Parque Nacional da Lagoa do Peixe, Rio Grande do Sul, Brasil. Acta Botanica Brasilica 18:815–824.CrossRefGoogle Scholar
DUARTE, M. H. L. & YOUNG, R. J. 2010. Sleeping site selection by urban marmosets (Callithrix penicillata) under conditions of exceptionally high predator density. International Journal of Primatology 32:329–334.CrossRefGoogle Scholar
DUARTE, M. H. L., VECCI, M. A., HIRSCH, A. & YOUNG, R. J. 2011. Noisy human neighbours affect where urban monkeys live. Biology Letters 7:840–842.CrossRefGoogle ScholarPubMed
DUNNING, J. B., DANIELSON, B. J. & PULLIAM, H. R. 1992. Ecological processes that affect populations in complex landscapes. Oikos 65:169–175.CrossRefGoogle Scholar
ETHIER, K. & FAHRIG, L. 2011. Positive effects of forest fragmentation, independent of forest amount, on bat abundance in eastern Ontario, Canada. Landscape Ecology 26:865–876.CrossRefGoogle Scholar
FAHRIG, L. 2003. Effects of habitat fragmentation on biodiversity. Annual Review of Ecology, Evolution, and Systematics 34:487–515.CrossRefGoogle Scholar
GALETTI, M., BOVENDORP, R. S., FADINI, R. F., GUSSONI, C. O., RODRIGUES, M., ALVAREZ, A. D., GUIMARÃES, P. R. & ALVES, K. 2009. Hyper abundant mesopredators and bird extinction in an Atlantic forest island. Zoologia 26:288–298.CrossRefGoogle Scholar
GARMENDIA, A., ARROYO-RODRÍGUEZ, V., ESTRADA, A., NARANJO, E. J. & STONER, K. E. 2013. Landscape and patch attributes impacting medium-and large-sized terrestrial mammals in a fragmented rain forest. Journal of Tropical Ecology 29:331–344.CrossRefGoogle Scholar
HARCOURT, A. H. & DOHERTY, D. A. 2005. Species-area relationships of primates in tropical forest fragments: a global analysis. Journal of Applied Ecology 42:630–637.CrossRefGoogle Scholar
HARTLEY, M. J. & HUNTER, M. L. 1998. A meta-analysis of forest cover, edge effects, and artificial nest predation rates. Conservation Biology 12:465–469.Google Scholar
HUGUENY, B. 1989. West African rivers as biogeographic islands: species richness of fish communities. Oecologia 79: 236–243.CrossRefGoogle Scholar
INGLE, N. R. 2003. Seed dispersal by wind, birds, and bats between Philippine montane rainforest and successional vegetation. Oecologia 134:251–261.CrossRefGoogle ScholarPubMed
JENNINGS, S. B., BROWN, N. D. & SHEIL, D. 1999. Assessing forest canopies and understorey illumination: canopy closure, canopy cover and other measures. Forestry 72:59–74.CrossRefGoogle Scholar
JOHNSON, E. O., KAMILARIS, T. C., CARTER, C. S., CALOGERO, A. E., GOLD, P. W. & CHROUSOS, G. P. 1996. The biobehavioral consequences of psychogenic stress in a small, social primate (Callithrix jacchus jacchus). Biological Psychiatry 40:317–337.CrossRefGoogle Scholar
LACHER, T. E., GUSTAVO, A., DA FONSECA, B., ALVES, C. & MAGALHAES-CASTRO, B. 1984. Parasitism of trees by marmosets in a central Brazilian gallery forest. Biotropica 16:202–209.CrossRefGoogle Scholar
LAURANCE, W. F., LOVEJOY, T. E., VASCONCELOS, H. L., BRUNA, E. M., DIDHAM, R. K., STOUFFER, P. C., GASCON, C., BIERREGAARD, R. O., LAURANCE, S. G. & SAMPAIO, E. 2002. Ecosystem decay of Amazonian forest fragments: a 22-year investigation. Conservation Biology 16:605–618.CrossRefGoogle Scholar
LAURANCE, W.F., GOOSEM, M. & LAURANCE, S.G. 2009. Impacts of roads and linear clearings on tropical forests. Trends in Ecology and Evolution 24:659–669.CrossRefGoogle ScholarPubMed
LI, H., CALDER, C. A. & CRESSIE, N. 2007. Beyond Moran's I: testing for spatial dependence based on the spatial autoregressive model. Geographical Analysis 39:357–375.CrossRefGoogle Scholar
LYRA-NEVES, R. M. D., OLIVEIRA, M. A., TELINO-JÚNIOR, W. R. & SANTOS, E. M. D. 2007. Interspecific behaviour between Callithrix jacchus (Linnaeus) (Callitrichidae, Primates) and some birds of the Atlantic forest, Pernambuco State, Brazil. Revista Brasileira de Zoologia 24:709–716.CrossRefGoogle Scholar
LOZADA, T., DE KONING, G. H. J., MARCHÉ, R., KLEIN, A. M. & TSCHARNTKE, T. 2007. Tree recovery and seed dispersal by birds: comparing forest, agroforestry and abandoned agroforestry in coastal Ecuador. Perspectives in Plant Ecology, Evolution and Systematics 8:131–140.CrossRefGoogle Scholar
MANDUJANO, S., ESCOBEDO-MORALES, L. A. & PALACIOS-SILVA, R. 2004. Movements of Alouatta palliata among forest fragments in Los Tuxtlas, Mexico. Neotropical Primates 12:126–131.CrossRefGoogle Scholar
MARSH, L. K. 2013. Because conservation counts. Pp. 3–11 in Marsh, L. K. & Chapman, C. A. (eds). Primates in fragments. Springer, New York.CrossRefGoogle Scholar
MCKINNEY, M. L. & LOCKWOOD, J. L. 1999. Biotic homogenization: a few winners replacing many losers in the next mass extinction. Trends in Ecology and Evolution 14:450–453.CrossRefGoogle ScholarPubMed
MILLAR, R. B. & ANDERSON, M. J. 2004. Remedies for pseudoreplication. Fisheries Research 70:397–407.CrossRefGoogle Scholar
MIRANDA, G. H. B. & FARIA, D. S. 2001. Ecological aspects of black-pincelled marmoset (Callithrix penicillata) in the Cerradão and dense Cerrado of the Brazilian Central Plateau. Brazilian Journal of Biology 61:397–404.CrossRefGoogle ScholarPubMed
MØLLER, A. P. 2009. Successful city dwellers: a comparative study of the ecological characteristics of urban birds in the Western Palearctic. Oecologia 159:849–858.CrossRefGoogle ScholarPubMed
MORAIS, M. M., RUIZ-MIRANDA, C. R., GRATIVOL, A. D., DE ANDRADE, C. C., LIMA, C. S., MARTINS, A. & BECK, B. B. 2008. Os sagüis, Callithrix jacchus penicillata, como espécies invasoras na região de ocorrência do mico-leão dourado. Pp. 86–117 in Oliveira, P. P., Grativol, A. D. & Ruiz Miranda, C. R. (eds.). Conservação do mico-leão-dourado: enfrentando os desafios de uma paisagem fragmentada. Universidade Estadual do Norte Fluminense Darcy Ribeiro, Centro de Biociências e Biotecnologia, Laboratório de Ciências Ambientais, Campos dos Goytacazes.Google Scholar
PASSAMANI, M. 1996. Uso de árvores gomíferas por Callithrix penicillata no Parque Nacional da Serra do Cipó, MG. Boletim do Museu de Biologia Mello Leitão 4:25–31.Google Scholar
PASSAMANI, M. & RYLANDS, A. B. 2000. Home range of a Geoffroy's marmoset group, Callithrix geoffroyi (Primates, Callitrichidae) in south-eastern Brazil. Revista Brasileira de Biologia 60:275–281.CrossRefGoogle ScholarPubMed
PATON, P. W. 1994. The effect of edge on avian nest success: how strong is the evidence? Conservation Biology 8:17–26.CrossRefGoogle Scholar
PERES, C. A. 2000. Effects of subsistence hunting on vertebrate community structure in Amazonian forests. Conservation Biology 14:240–253.CrossRefGoogle Scholar
PONTES, A. R. M. & SOARES, M. L. 2005. Sleeping sites of common marmosets (Callithrix jacchus) in defaunated urban forest fragments: a strategy to maximize food intake. Journal of Zoology 266:55–63.CrossRefGoogle Scholar
POZO-MONTUY, G. & SERIO-SILVA, J. C. 2007. Movement and resource use by a group of Alouatta pigra in a forest fragment in Balancán, México. Primates 48:102–107.CrossRefGoogle Scholar
RAND, T. A. & TSCHARNTKE, T. 2007. Contrasting effects of natural habitat loss on generalist and specialist aphid natural enemies. Oikos 116:1353–1362.CrossRefGoogle Scholar
RICKETTS, T. H., REGETZ, J., STEFFAN-DEWENTER, I., CUNNINGHAM, S. A., KREMEN, C., BOGDANSKI, A., GEMMILL-HERREN, B., GREENLEAF, S. S., KLEIN, A. M., MAYFIELD, M. M., MORANDIN, L. A., OCHIENG, A. & VIANA, B. F. 2008. Landscape effects on crop pollination services: are there general patterns? Ecology Letters 11:499–515.CrossRefGoogle ScholarPubMed
RUIZ-MIRANDA, C. R., AFFONSO, A. G., MORAIS, M. M. D., VERONA, C. E., MARTINS, A. & BECK, B. B. 2006. Behavioral and ecological interactions between reintroduced golden lion tamarins (Leontopithecus rosalia Linnaeus, 1766) and introduced marmosets (Callithrix spp., Linnaeus, 1758) in Brazil's Atlantic Coast forest fragments. Brazilian Archives of Biology and Technology 49:99–109.CrossRefGoogle Scholar
RYLANDS, A. B. 1996. Habitat and the evolution of social and reproductive behavior in Callitrichidae. American Journal of Primatology 38:5–18.3.0.CO;2-2>CrossRefGoogle ScholarPubMed
RYLANDS, A. B. & FARIA, D. S. 1993. Habitats, feeding ecology, and home range size in the Genus Callithrix. Pp. 262–272 in Rylands, A. B. (ed.). Marmosets and tamarins: systematics, behavior and ecology. Oxford University Press, New York.CrossRefGoogle Scholar
SANTOS, C.F., BUENO, B. & CASELLA, J. 2013. Comparison between sampling methods and baits efficiency in attracting mammals in Brazilian savanna. Neotropical Biology and Conservation 8: 156–164.Google Scholar
SAVARD, J. P. L., CLERGEAU, P. & MENNECHEZ, G. 2000. Biodiversity concepts and urban ecosystems. Landscape and Urban Planning 48:131–142.CrossRefGoogle Scholar
SCANLON, C. E., CHALMERS, N. R. & DA CRUZ, M. M. 1989. Home range use and the exploitation of gum in the marmoset Callithrix jacchus jacchus. International Journal of Primatology 10: 123–136.CrossRefGoogle Scholar
SMITH, A. C., FAHRIG, L. & FRANCIS, C. M. 2011. Landscape size affects the relative importance of habitat amount, habitat fragmentation, and matrix quality on forest birds. Ecography 34: 103–113.CrossRefGoogle Scholar
STEVENSON, M. F. & RYLANDS, A. B. 1988. The marmosets, genus Callithrix. Pp. 131–222 in Mittermeier, A., Rylands, A. B., Coimbra Filho, A. F. & Da Fonseca, G. A. B. (eds). Ecology and behavior of neotropical primates. World Wildlife Fund, Washington.Google Scholar
TEIXEIRA, B. A., HIRSCH, A., GOULART, V. D., PASSOS, L., TEIXEIRA, C. P., JAMES, P. & YOUNG, R. J. 2015. Good neighbours: distribution of black-tufted marmoset (Callithrix penicillata) in an urban environment. Wildlife Research 42:579–589.CrossRefGoogle Scholar
THIES, C. & TSCHARNTKE, T. 1999. Landscape structure and biological control in agroecosystems. Science 285:893–895.CrossRefGoogle ScholarPubMed
THOMPSON, C. L., ROBL, N. J., DE OLIVEIRA MELO, L. C., VALENÇA-MONTENEGRO, M. M., VALLE, Y. B. M., DE OLIVEIRA, M. A. B. & VINYARD, C. J. 2013. Spatial distribution and exploitation of trees gouged by common marmosets (Callithrix jacchus). International Journal of Primatology 34:65–85.CrossRefGoogle Scholar
TSCHARNTKE, T., TYLIANAKIS, J. M., RAND, T. A., DIDHAM, R. K., FAHRIG, L., BATARY, P., BENGTSSON, J., CLOUGH, Y., CRIST, T. O., DORMANN, C. F., EWERS, R. M., FRUND, J., HOLT, R. D., HOLZSCHUH, A., KLEIN, A. M., KLEIJN, D., KREMEN, C., LANDIS, D. A., LAURANCE, W., LINDENMAYER, D., SCHERBER, C., SODHI, N., DEWENTER, I. S., THIES, C., VAN DER PUTTEN, W. H. & WESTPHAL, C. 2012. Landscape moderation of biodiversity patterns and processes-eight hypotheses. Biological Reviews 87:661–685.CrossRefGoogle Scholar
TUBELIS, D. P., LINDENMAYER, D. B. & COWLING, A. 2004. Novel patch–matrix interactions: patch width influences matrix use by birds. Oikos 107:634–644.CrossRefGoogle Scholar
VAN DER REE, R., CESARINI, S. P., MOORE, S. J. L. & TAYLOR, A. 2010. Large gaps in canopy reduce road crossing by a gliding mammal. Ecology and Society 15:35.CrossRefGoogle Scholar
VAN DER REE, R., SMITH, D. J. & GRILO, C. 2015. The ecological effects of linear infrastructure and traffic. Pp. 1–9 in van der Ree, R., Smith, D. J. & Grilo, C. (eds). Handbook of road ecology. John Wiley & Sons, Chichester.CrossRefGoogle Scholar
VETTER, D., HANSBAUER, M. M., VEGVARI, Z. & STORCH, I. 2011. Predictors of forest fragmentation sensitivity in neotropical vertebrates: a quantitative review. Ecography 34:1–8.CrossRefGoogle Scholar
VILELA, A. A. & DEL-CLARO, K. 2011. Feeding behavior of the Black-Tufted-ear Marmoset (Callithrix penicillata) (Primata, Callitrichidae) in a Tropical Cerrado Savanna. Sociobiology 58:1–6.Google Scholar
VILELA, S. L. 2007. Sympatry and diet of Callithrix penicillata (Hershkovitz) (Callitrichidae) and Cebus libidinosus (Spix) (Cebidae) in gallery forests from Distrito Federal, Brasil. Revista Brasileira de Zoologia 24:601–607.CrossRefGoogle Scholar
VILELA, S. L. & FARIA, D. S. 2004. Seasonality of the activity pattern of Callithrix penicillata (Primates, Callitrichidae) in the Cerrado (Scrub Savanna Vegetation). Brazilian Journal of Biology 64: 363–370.CrossRefGoogle ScholarPubMed
VINYARD, C. J., WALL, C. E., WILLIAMS, S. H., MORK, A. L., ARMFIELD, B. A., MELO, L. C. O., VALENÇA-MONTENEGRO, M. M., VALLE, Y. B. M., OLIVEIRA, M. A. B., LUCAS, P. W., SCHMITT, D., TAYLOR, A. B. & HYLANDER, W. L. 2009. The evolutionary morphology of tree gouging in marmosets. Pp. 395–409 in Ford, S. M., Porter, L. M. & Davis, L. C. (eds). The smallest anthropoids. Springer-Verlag, New York.CrossRefGoogle Scholar
WILSON, R. F., MARSH, H. & WINTER, J. 2007. Importance of canopy connectivity for home range and movements of the rainforest arboreal ringtail possum (Hemibelideus lemuroides). Wildlife Research 34:177–184.CrossRefGoogle Scholar
ZAGO, L., MIRANDA, J., SANTOS, C., PASSOS, F. & SIMÕES-LOPES, P. C. 2014. Composição de grupos, conflitos intergrupais e uso do espaço em Callithrix penicillata (Geoffroy, 1812) introduzidos em um fragmento urbano. Biotemas 27:193–201.CrossRefGoogle Scholar
ZHANG, W., RICKETTS, T. H., KREMEN, C., CARNEY, K. & SWINTON, S. M. 2007. Ecosystem services and dis-services to agriculture. Ecological Economics 64:253–260.CrossRefGoogle Scholar
ZUUR, A., IENO, E. N., WALKER, N., SAVELIEV, A. A. & SMITH, G. M. 2009. Mixed effects models and extensions in ecology with R. Springer, New York. 574 pp.CrossRefGoogle Scholar