Skip to main content

Advertisement

SpringerLink
Log in

The Density of Callicebus coimbrai is Better Predicted by Vegetation Structure Variables than by Surrounding Landscape

  • Published:
International Journal of Primatology Aims and scope Submit manuscript

Abstract

Primate population density often varies considerably between sites, reflecting differences in site conditions and resource availability. Understanding these differences may provide important insights for habitat management. We identified environmental variables that affect the population density of Callicebus coimbrai in forest patches throughout its geographic distribution in northeastern Brazil. We sampled the vegetation structure of 19 forest patches and assessed the composition of the surrounding landscape and the resistance of the surrounding matrix to the movement of C. coimbrai. We used the number of responses of C. coimbrai to playback to estimate the species density in each patch. The density of C. coimbrai was positively related to understory vegetation density, and tree diameter and density, but not to the surrounding landscape composition. The sites with the highest densities were concentrated in the center of the species geographic range and only one of the forest patches may be large enough to host a viable population of C. coimbrai over the long term. Denser understories and larger and closed-spaced trees were related to food availability, and possibly also to predator avoidance, although most predators were extirpated from the region. C. coimbrai tolerate and may even benefit from forest disturbance, depending on how the process has changed the vegetation structure. Our results emphasize the need to enhance the connectivity of the forest patches, particularly in the central portion of the species distribution. Our findings suggest that a whole-range approach is effective to identify the drivers of species density, and priority areas and conservation strategies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alvares, C. A., Stape, J. L., Sentelhas, P. C., de Moraes Gonçalves, J. L., & Sparovek, G. (2013). Köppen's climate classification map for Brazil. Meteorologische Zeitschrift, 22(6), 711–728. https://doi.org/10.1127/0941-2948/2013/0507.

    Article  ADS  Google Scholar 

  • Anderson, J., Cowlishaw, G., & Rowcliffe, J. M. (2007). Effects of forest fragmentation on the abundance of Colobus angolensis palliatus in Kenya’s Coastal Forests. International Journal of Primatology, 28(3), 637–655. https://doi.org/10.1007/s10764-007-9143-7.

    Article  Google Scholar 

  • Arce-Peña, N. P., Arroyo-Rodríguez, V., Dias, P. A., Franch-Pardo, I., & Andresen, E. (2019). Linking changes in landscape structure to population changes of an endangered primate. Landscape Ecology, 34(11), 2687–2701. https://doi.org/10.1007/s10980-019-00914-8.

    Article  Google Scholar 

  • Arroyo-Rodríguez, V., & Dias, P. A. D. (2010). Effects of habitat fragmentation and disturbance on howler monkeys: a review. American Journal of Primatology, 72(1), 1–16. https://doi.org/10.1002/ajp.20753.

    Article  PubMed  Google Scholar 

  • Arroyo-Rodríguez, V., & Fahrig, L. (2014). Why is a landscape perspective important in studies of primates? American Journal of Primatology, 76(10), 901–909. https://doi.org/10.1002/ajp.22282.

    Article  PubMed  Google Scholar 

  • Arroyo-Rodríguez, V., & Mandujano, S. (2006). Forest fragmentation modifies habitat quality for Alouatta palliata. International Journal of Primatology, 27(4), 1079–1096. https://doi.org/10.1007/s10764-006-9061-0.

    Article  Google Scholar 

  • Arroyo-Rodríguez, V., González-Perez, I. M., Garmendia, A., Solà, M., & Estrada, A. (2013). The relative impact of forest patch and landscape attributes on black howler monkey populations in the fragmented Lacandona rainforest, Mexico. Landscape Ecology, 28(9), 1717–1727. https://doi.org/10.1007/s10980-013-9929-2.

    Article  Google Scholar 

  • Barlow, J., Haugaasen, T., & Peres, C. A. (2002). Effects of ground fires on understorey bird assemblages in Amazonian forests. Biological Conservation, 105(2), 157–169. https://doi.org/10.1016/S0006-3207(01)00177-X.

    Article  Google Scholar 

  • Bicca-Marques, J. C., & Heymann, E. W. (2013). Ecology and behavior of titi monkeys (genus Callicebus). In L. M. Veiga, A. A. Barnett, S. F. Ferrari, & M. A. Norconk (Eds.), Evolutionary Biology and Conservation of Titis, Sakis and Uacaris (pp. 196–207). Cambridge University Press.

    Chapter  Google Scholar 

  • Boinski, S. U. E., Kauffman, L., Westoll, A., Stickler, C. M., Cropp, S., & Ehmke, E. (2003). Are Vigilance, Risk from Avian Predators and Group Size Consequences of Habitat Structure? A Comparison of Three Species of Squirrel Monkey (Saimiri oerstedii, S. boliviensis, and S. sciureus). Behaviour, 140, 1421–1467. https://doi.org/10.1163/156853903771980666.

    Article  Google Scholar 

  • Bowman, J., Jaeger, J. A., & Fahrig, L. (2002). Dispersal distance of mammals is proportional to home range size. Ecology, 83(7), 2049–2055. https://doi.org/10.1890/0012-9658(2002)083[2049:DDOMIP]2.0.CO;2.

    Article  Google Scholar 

  • Brazil (2011). Plano de Ação Nacional para Conservação dos Primatas do Nordeste. ICMBio.

    Google Scholar 

  • Brown, J., Mehlman, D., & Stevens, G. (1995). Spatial variation in abundance. Ecology, 76(7), 2028–2043. https://doi.org/10.2307/1941678.

    Article  Google Scholar 

  • Burnham, K. P., & Anderson, D. R. (2002). Model selection and multimodel inference: a practical information-theoretic approach. Springer.

    Google Scholar 

  • Byrne, H., Rylands, A. B., Carneiro, J. C., Alfaro, J. W. L., Bertuol, F., da Silva, M. N., Messias, M., Groves, C. P., Mittermeier, R. A., Farias, I., Hrbek, T., Schneider, H., Sampaio, I., & Boubli, J. P. (2016). Phylogenetic relationships of the New World titi monkeys (Callicebus): first appraisal of taxonomy based on molecular evidence. Frontiers in Zoology, 13(1), 10. https://doi.org/10.1186/s12983-016-0142-4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carretero-Pinzón, X. (2013). Population density and habitat availability of Callicebus ornatus, a Colombian endemic titi monkey. In T. R. Defler, P. R. Stevenson, M. L. Bueno, & D. C. Guzmán-Caro (Eds.), Especies de Primates Colombianos en Peligro de Extinción (pp. 160–169). Asociación Primatológica Colombiana.

    Google Scholar 

  • Cavada, N., Tenan, S., Barelli, C., & Rovero, F. (2019). Effects of anthropogenic disturbance on primate density at the landscape scale. Conservation Biology, 33(4), 873–882. https://doi.org/10.1111/cobi.13269.

    Article  PubMed  Google Scholar 

  • Chagas, R. R. D., & Ferrari, S. F. (2010). Habitat use by Callicebus coimbrai (Primates: Pitheciidae) and sympatric species in the fragmented landscape of the Atlantic Forest of southern Sergipe, Brazil. Zoologia, 27(6), 853–860. https://doi.org/10.1590/S1984-46702010000600003.

    Article  Google Scholar 

  • Chagas, R. R. D., & Ferrari, S. F. (2011). Population parameters of the endangered titi monkey, Callicebus coimbrai Kobayashi and Langguth, 1999, in the fragmented landscape of southern Sergipe, Brazil. Brazilian Journal of Biology, 71(3), 569–575. https://doi.org/10.1590/S1519-69842011000400001.

    Article  CAS  Google Scholar 

  • Chapman, C., Chapman, L., Wangham, R., Hunt, K., Gebo, D., & Gardner, L. (1992). Estimators of fruit abundance of tropical trees. Biotropica, 24(4), 527–531. https://doi.org/10.2307/2389015.

    Article  Google Scholar 

  • Chapman, C. A., Gautier-Hion, A. N. N. I. E., Oates, J. F., & Onderdonk, D. A. (1999). African primate communities: determinants of structure and threats to survival. In J. G. Fleagle, C. H. Janson, & K. E. Reed (Eds.), Primate communities (pp. 1–37). Cambridge University Press. https://doi.org/10.1017/CBO9780511542381.002.

    Chapter  Google Scholar 

  • Chapman, C. A., Bortolamiol, S., Matsuda, I., Omeja, P. A., Paim, F. P., Reyna-Hurtado, R., Sengupta, R., & Valenta, K. (2018). Primate population dynamics: variation in abundance over space and time. Biodiversity and Conservation, 27(5), 1221–1238. https://doi.org/10.1007/s10531-017-1489-3.

    Article  Google Scholar 

  • Cheyne, S. M. (2011). Gibbon locomotion research in the field: problems, possibilities, and benefits for conservation. In K. D’Août & E. E. Vereecke (Eds.), Primate Locomotion: Linking Field and Laboratory Research (pp. 201–213). Springer. https://doi.org/10.1007/978-1-4419-1420-0_11.

    Chapter  Google Scholar 

  • Cisneros-Heredia, D. F., León-Reyes, A., & Seger, S. (2005). Boa constrictor predation on a Titi monkey, Callicebus discolor. Neotropical Primates, 13(3), 11–12. https://doi.org/10.1896/1413-4705.13.3.11.

    Article  Google Scholar 

  • Costa-Araújo, R., Luis Regolin, A., Martello, F., Pedro Souza-Alves, J., Hrbek, T., & Cezar Ribeiro, M. (2021). Occurrence and conservation of the vulnerable titi monkey Callicebus melanochir in fragmented landscapes of the Atlantic forest hotspot. Oryx, 55(6), 916–923. https://doi.org/10.1017/S0030605319001522.

    Article  Google Scholar 

  • Cottam, G., & Curtis, J. T. (1956). The use of distance measures in phytosociological sampling. Ecology, 37(3), 451–460. https://doi.org/10.2307/1930167.

    Article  Google Scholar 

  • Cristóbal-Azkarate, J., Veà, J. J., Asensio, N., & Rodríguez-Luna, E. (2005). Biogeographical and floristic predictors of the presence and abundance of mantled howlers (Alouatta palliata mexicana) in rainforest fragments at Los Tuxtlas, Mexico. American Journal of Primatology, 67(2), 209–222. https://doi.org/10.1002/ajp.20178.

    Article  PubMed  Google Scholar 

  • DeWalt, S. J., Maliakal, S. K., & Denslow, J. S. (2003). Changes in vegetation structure and composition along a tropical forest chronosequence: Implications for wildlife. Forest Ecology and Management, 182(1-3), 139–151. https://doi.org/10.1016/S0378-1127(03)00029-X.

    Article  Google Scholar 

  • Emmons, L. H., Whitney, B. T., & Ross, D. L. (1997). Sounds of Neotropical Rainforest Mammals: An audio field guide. Library of Natural Sounds, Cornell Laboratory of Ornithology.

    Google Scholar 

  • Ewers, R. M., & Didham, R. K. (2006). Confounding factors in the detection of species responses to habitat fragmentation. Biological Reviews, 81(1), 117–142. https://doi.org/10.1017/S1464793105006949.

    Article  PubMed  Google Scholar 

  • Ferrari, S. F. (2009). Predation risk and antipredator strategies. In P. A. Garber, A. Estrada, J. C. Bicca-Marques, E. W. Heymann, & K. B. Strier (Eds.), South American Primates (pp. 251–277). Springer.

    Chapter  Google Scholar 

  • Flesher, K. M. (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. International Journal of Primatology, 36(6), 1172–1197. https://doi.org/10.1007/s10764-015-9884-7.

    Article  Google Scholar 

  • Fortin, M., & Dale, M. (2005). Spatial Analysis: A guide for ecologists. Cambridge University Press.

    Book  Google Scholar 

  • Frankham, R. (2003). Genetics and Conservation Biology. Comptes Rendus Biologies, 326((Supplement 1), 22–29. https://doi.org/10.1016/S1631-0691(03)00023-4.

    Article  Google Scholar 

  • Gabriel, D. N., Gould, L., & Cook, S. (2018). Crowding as a primary source of stress in an endangered fragment-dwelling strepsirrhine primate. Animal Conservation, 21(1), 76–85. https://doi.org/10.1111/acv.12375.

    Article  Google Scholar 

  • Galán-Acedo, C., Arroyo-Rodríguez, V., Cudney-Valenzuela, S. J., & Fahrig, L. (2019). A global assessment of primate responses to landscape structure. Biological Reviews, 94(5), 1605–1618. https://doi.org/10.1111/brv.12517.

    Article  PubMed  Google Scholar 

  • Galán-Acedo, C., Spaan, D., Bicca-Marques, J. C., de Azevedo, R. B., Villalobos, F., & Rosete-Vergés, F. (2021). Regional deforestation drives the impact of forest cover and matrix quality on primate species richness. Biological Conservation, 263, 109338. https://doi.org/10.1016/j.biocon.2021.109338.

    Article  Google Scholar 

  • Gestich, C. C., Caselli, C. B., Nagy-Reis, M. B., Setz, E. Z., & Cunha, R. G. (2017). Estimating primate population densities: The systematic use of playbacks along transects in population surveys. American Journal of Primatology, 79(2), e22586. https://doi.org/10.1002/ajp.22586.

    Article  Google Scholar 

  • Gestich, C. C., Arroyo-Rodríguez, V., Saranholi, B. H., Cunha, R. G., Setz, E. Z., & Ribeiro, M. C. (2021). Forest loss and fragmentation can promote the crowding effect in a forest-specialist primate. Landscape Ecology. https://doi.org/10.1007/s10980-021-01336-1.

  • Gouveia, S. F., Souza-Alves, J. P., de Souza, B. B., Beltrão-Mendes, R., Jerusalinsky, L., & Ferrari, S. F. (2017). Functional planning units for the management of an endangered Brazilian titi monkey. American Journal of Primatology, 79(5), e22637. https://doi.org/10.1002/ajp.22637.

    Article  Google Scholar 

  • Hamard, M., Cheyne, S. M., & Nijman, V. (2010). Vegetation correlates of gibbon density in the peat-swamp forest of the Sabangau catchment, Central Kalimantan, Indonesia. American Journal of Primatology, 72(7), 607–616. https://doi.org/10.1002/ajp.20815.

    Article  PubMed  Google Scholar 

  • Hanya, G., & Chapman, C. A. (2013). Linking feeding ecology and population abundance: a review of food resource limitation on primates. Ecological Research, 28(2), 183–190. https://doi.org/10.1007/s11284-012-1012-y.

    Article  Google Scholar 

  • Hawes, J., Motta, C. D. S., Overal, W. L., Barlow, J., Gardner, T. A., & Peres, C. A. (2009). Diversity and composition of Amazonian moths in primary, secondary and plantation forests. Journal of Tropical Ecology, 25(3), 281–300. https://doi.org/10.1017/S0266467409006038.

    Article  Google Scholar 

  • Heiduck, S. (2002). The use of disturbed and undisturbed forest by masked titi monkeys Callicebus personatus melanochir is proportional to food availability. Oryx, 36(2), 133–139. https://doi.org/10.1017/S0030605302000200.

    Article  Google Scholar 

  • Hendges, C. D., Melo, G. L., Gonçalves, A. S., Cerezer, F. O., & Cáceres, N. C. (2017). Landscape attributes as drivers of the geographical variation in density of Sapajus nigritus Kerr, 1792, a primate endemic to the Atlantic Forest. Acta Oecologica, 84, 57–63. https://doi.org/10.1016/j.actao.2017.08.007.

    Article  ADS  Google Scholar 

  • Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G., & Jarvis, A. (2005). Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology, 25(15), 1965–1978. https://doi.org/10.1002/joc.1276.

    Article  ADS  Google Scholar 

  • Hilário, R. R. (2013). Determinantes ambientais da densidade de Callicebus coimbrai em fragmentos florestais no nordeste brasileiro e implicações para a sua conservação. PhD Dissertation, Universidade Federal da Paraíba.

  • Hilário, R. R., Jerusalinsky, L., Santos, S., Beltrão-Mendes, R., & Ferrari, S. F. (2017). A primate at risk in Northeast Brazil: local extinctions of Coimbra Filho’s titi (Callicebus coimbrai). Primates, 58(2), 343–352. https://doi.org/10.1007/s10329-017-0599-6.

    Article  PubMed  Google Scholar 

  • Irwin, M. T. (2008). Feeding ecology of diademed sifakas (Propithecus diadema) in forest fragments and continuous forest. International Journal of Primatology, 29(1), 95–115. https://doi.org/10.1007/s10764-007-9222-9.

    Article  Google Scholar 

  • Isbell, L. A. (1994). Predation on primates: ecological patterns and evolutionary consequences. Evolutionary Anthropology, 3(2), 61–71. https://doi.org/10.1002/evan.1360030207.

    Article  Google Scholar 

  • Jackson, H. B., & Fahrig, L. (2012). What size is a biologically relevant landscape? Landscape Ecology, 27(7), 929–941. https://doi.org/10.1007/s10980-012-9757-9.

    Article  Google Scholar 

  • Jerusalinsky, L. (2013) Distribuição geográfica e conservação de Callicebus coimbrai Kobayashi & Langguth, 1999 (Primates – Pitheciidae) na Mata Atlântica do nordeste do Brasil. PhD Dissertation, Universidade Federal da Paraíba.

  • Jerusalinsky, L., & Souza-Alves, J. P. (2018). Callicebus comibrai. In ICMBio (Ed.), Livro Vermelho da Fauna Brasileira Ameaçada de Extinção: Volume II - Mamíferos (pp. 287–293).

    Google Scholar 

  • Jerusalinsky, L., Souza-Alves, J. & Ferrari, S. (2020). Callicebus coimbrai. The IUCN Red List of Threatened Species 2020. https://doi.org/10.2305/IUCN.UK.2020-3.RLTS.T39954A17972422.en

  • Kinzey, W. G., & Robinson, J. G. (1983). Intergroup loud calls, range size, and spacing in Callicebus torquatus. American Journal of Physical Anthropology, 60(4), 539–544. https://doi.org/10.1002/ajpa.1330600416.

    Article  CAS  PubMed  Google Scholar 

  • Kulp, J., & Heymann, E. W. (2015). Ranging, activity budget, and diet composition of red titi monkeys (Callicebus cupreus) in primary forest and forest edge. Primates, 56(3), 273–278. https://doi.org/10.1007/s10329-015-0471-5.

    Article  PubMed  PubMed Central  Google Scholar 

  • Luna, A. G., Sanmiguel, R., Di Fiore, A., & Fernandez-Duque, E. (2010). Predation and predation attempts on red titi monkeys (Callicebus discolor) and equatorial sakis (Pithecia aequatorialis) in Amazonian Ecuador. Folia Primatologica, 81(2), 86–95. https://doi.org/10.1159/000314948.

    Article  Google Scholar 

  • MapBiomas. (2019). Projeto MapBiomas – Coleção 5.0 da Série Anual de Mapas de Cobertura e Uso de Solo do Brasil. https://mapbiomas.org/. Accessed 4 Mar 2021.

  • Marsh, L. (2003). Wild zoos: conservation of primates in situ. In L. Marsh (Ed.), Primates in fragments: Ecology and conservation (pp. 365–379). Kluwer Academic/Plenum Publishers.

    Chapter  Google Scholar 

  • Marsh, C., Link, A., King-Bailey, G., & Donati, G. (2016). Effects of fragment and vegetation structure on the population abundance of Ateles hybridus, Alouatta seniculus and Cebus albifrons in Magdalena Valley, Colombia. Folia Primatologica, 87(1), 17–30. https://doi.org/10.1159/000443929.

    Article  Google Scholar 

  • McIntyre, N. E. (1995). Effects of forest patch size on avian diversity. Landscape Ecology, 10(2), 85–99. https://doi.org/10.1007/BF00153826.

    Article  Google Scholar 

  • McRae, B. H. (2006). Isolation by resistance. Evolution, 60(8), 1551–1561. https://doi.org/10.1111/j.0014-3820.2006.tb00500.x.

    Article  PubMed  Google Scholar 

  • McRae, B. H., Dickson, B. G., Keitt, T. H., & Shah, V. B. (2008). Using circuit theory to model connectivity in ecology, evolution, and conservation. Ecology, 89(10), 2712–2724. https://doi.org/10.1890/07-1861.1.

    Article  PubMed  Google Scholar 

  • Morrissey, M. B., & Ruxton, G. D. (2018). Multiple regression is not multiple regressions: the meaning of multiple regression and the non-problem of collinearity. Philosophy, Theory, and Practice in Biology, 10, 3. https://doi.org/10.3998/ptpbio.16039257.0010.003.

    Article  Google Scholar 

  • Oliveira, V. B. D., Linares, A. M., Corrêa, G. L. C., & Chiarello, A. G. (2008). Predation on the black capuchin monkey Cebus nigritus (Primates: Cebidae) by domestic dogs Canis lupus familiaris (Carnivora: Canidae), in the Parque Estadual Serra do Brigadeiro, Minas Gerais, Brazil. Revista Brasileira de Zoologia, 25, 376–378. https://doi.org/10.1590/S0101-81752008000200026.

    Article  Google Scholar 

  • Pinto, N., Lasky, J., Bueno, R., Keitt, T. H., & Galetti, M. (2009). Primate densities in the Atlantic Forest of Southeastern Brazil: The role of habitat quality and anthropogenic disturbance. In P. A. Garber, A. Estrada, J. C. Bicca-Marques, E. K. Heymann, & K. B. Strier (Eds.), South American Primates, Developments in Primatology: Progress and Prospects (pp. 413–431). Springer.

    Chapter  Google Scholar 

  • Pozo-Montuy, G., Serio-Silva, J. C., & Bonilla-Sánchez, Y. M. (2011). Influence of the landscape matrix on the abundance of arboreal primates in fragmented landscapes. Primates, 52(2), 139–147. https://doi.org/10.1007/s10329-010-0231-5.

    Article  PubMed  Google Scholar 

  • Price, E. C., & Piedade, H. M. (2001). Ranging behavior and intraspecific relationships of masked titi monkeys (Callicebus personatus personatus). American Journal of Primatology, 53(2), 87–92. https://doi.org/10.1002/1098-2345(200102)53:2<87::AID-AJP4>3.0.CO;2-P

  • R Core Team (2020). R: A language and environment for statistical computing. R Foundation for Statistical Computing. https://www.R-project.org/. Accessed 29 Feb 2020.

  • Reed, D. H., O'Grady, J. J., Brook, B. W., Ballou, J. D., & Frankham, R. (2003). Estimates of minimum viable population sizes for vertebrates and factors influencing those estimates. Biological Conservation, 113(1), 23–34. https://doi.org/10.1016/S0006-3207(02)00346-4.

    Article  Google Scholar 

  • Rocha, J. G. (2011). Distribuição e densidade de populacões de Callicebus coimbrai Kobayashi & Langguth 1999, na região do Refúgio de Vida Silvestre Mata do Junco, Sergipe. Master’s Dissertation, Federal University of Sergipe

  • Sousa, M. C., Santos, S. S., & Valente, M. C. M. (2008). Distribuição e variação na pelagem de Callicebus coimbrai (Primates, Pitheciidae) nos estados de Sergipe e Bahia, Brasil. Neotropical Primates, 15(2), 54–59. https://doi.org/10.1896/044.015.0208.

    Article  Google Scholar 

  • Souza, C. M., Shimbo, J. Z., Rosa, M. R., Parente, L. L., Alencar, A. A., Rudorff, B. F., Hasenack, H., Matsumoto, M., Ferreira, L. G., Souza-Filho, P. W. M., de Oliveira, S. W., Rocha, W. F., Fonseca, A. V., Marques, C. B., Diniz, C. G., Costa, D., Monteiro, D., Rosa, E. R., Vélez-Martin, E., et al (2020). Reconstructing three decades of land use and land cover changes in Brazilian biomes with Landsat archive and Earth Engine. Remote Sensing, 12(17), 2735. https://doi.org/10.3390/rs12172735.

    Article  ADS  Google Scholar 

  • Souza-Alves, J. P. & Ferrari, S. F. (2012). Unwanted homecoming: an adult male titi (Callicebus coimbrai) returns to its natal group. In International Primatological Society XXIV Congress (p. 661-661), Cancún: International Primatological Society.

  • Souza-alves, J. P., & Fontes, I. P. (2020). Anti-predator behavior of Coimbra-Filho’s titi monkeys (Callicebus coimbrai). Neotropical Primates, 26, 10–16.

    Article  Google Scholar 

  • Souza-Alves, J. P., Fontes, I. P., Chagas, R. R. D., & Ferrari, S. F. (2011). Seasonal versatility in the feeding ecology of a group of titis (Callicebus coimbrai) in the northern Brazilian Atlantic Forest. American Journal of Primatology, 73(12), 1199–1209. https://doi.org/10.1002/ajp.20990.

    Article  PubMed  Google Scholar 

  • Souza-Alves, J. P., Mourthé, Í., Hilário, R. R., Bicca-Marques, J. C., Rehg, J., Gestich, C. C., et al (2019). Terrestrial behavior in titi monkeys (Callicebus, Cheracebus, and Plecturocebus): potential correlates, patterns, and differences between genera. International Journal of Primatology, 40(4-5), 553–572. https://doi.org/10.1007/s10764-019-00105-x.

    Article  Google Scholar 

  • Souza-Alves, J. P., Chagas, R. R. D., Santana, M. M., Boyle, S. A., & Bezerra, B. M. (2021). Food availability, plant diversity, and vegetation structure drive behavioral and ecological variation in Endangered Coimbra-Filho's titi monkeys. American Journal of Primatology, 83, e23237. https://doi.org/10.1002/ajp.23237.

    Article  PubMed  Google Scholar 

  • Sugiura, N. (1978). Further analysis of the data by Akaike's information criterion and the finite corrections. Communications in Statistics - Theory and Methods, 7(1), 13–26. https://doi.org/10.1080/03610927808827599.

    Article  Google Scholar 

  • Tews, J., Brose, U., Grimm, V., Tielbörger, K., Wichmann, M. C., Schwager, M., & Jeltsch, F. (2004). Animal species diversity driven by habitat heterogeneity/diversity: the importance of keystone structures. Journal of Biogeography, 31(1), 79–92. https://doi.org/10.1046/j.0305-0270.2003.00994.x.

    Article  Google Scholar 

  • Traill, L. W., Bradshaw, C. J., & Brook, B. W. (2007). Minimum viable population size: a meta-analysis of 30 years of published estimates. Biological Conservation, 139(1-2), 159–166. https://doi.org/10.1016/j.biocon.2007.06.011.

    Article  Google Scholar 

  • Tscharntke, T., Tylianakis, J. M., Rand, T. A., Didham, R. K., Fahrig, L., Batáry, P., Bengtsson, J., Clough, Y., Crist, T. O., Dormann, C. F., & Ewers, R. M. (2012). Landscape moderation of biodiversity patterns and processes-eight hypotheses. Biological Reviews, 87(3), 661–685. https://doi.org/10.1111/j.1469-185X.2011.00216.x.

    Article  PubMed  Google Scholar 

  • van Kuijk, S. M., García-Suikkanen, C., Tello-Alvarado, J. C., Vermeer, J., & Hill, C. M. (2015). Estimating population density of the San Martin titi monkey (Callicebus oenanthe) in Peru using vocalisations. Folia Primatologica, 86(6), 525–533. https://doi.org/10.1159/000442974.

    Article  Google Scholar 

  • Wagner, T. (2000). Influence of Forest Type and Tree Species on Canopy-Dwelling Beetles in Budongo Forest, Uganda. Biotropica, 32(3), 502–514. https://doi.org/10.1111/j.1744-7429.2000.tb00496.x.

    Article  Google Scholar 

  • Wagner, M., Castro, F., & Stevenson, P. R. (2009). Habitat Characterization and Population Status of the Dusky Titi (Callicebus ornatus) in Fragmented Forests, Meta, Colombia. Neotropical Primates, 16(1), 18–24. https://doi.org/10.1896/044.016.0104.

    Article  Google Scholar 

  • Worman, C. O. D., & Chapman, C. A. (2006). Densities of two frugivorous primates with respect to forest and fragment tree species composition and fruit availability. International Journal of Primatology, 27(1), 203. https://doi.org/10.1007/s10764-005-9007-y.

    Article  Google Scholar 

Download references

Acknowledgments

The authors are grateful to CAPES for graduate stipends to RRH. JPS-A is supported by FACEPE (process: BFP 0149-2.05/19) and SFF by CNPq (process: 310852/2017-0). They thank Copener and the owners of the properties visited during this study. They also thank the Belo Horizonte zoo and Dalia for access to study titi monkey vocalizations. Thanks to Daniela Bitencurti Ruiz-Esparza (in memoriam) for her contributions to this study. We thank the anonymous reviewers for the valuable comments made on previous drafts of this manuscript.

Funding

This study was funded by CNPq (Process: 303994/2011-8)

Author information

Authors and Affiliations

  1. Department of Environment and Development, Federal University of Amapá, Rod. JK, Km 2, Jardim Marco Zero, Macapá, AP, 68.903-419, Brazil

    Renato R. Hilário

  2. Department of Systematics and Ecology, Federal University of Paraíba, João Pessoa, Brazil

    Renato R. Hilário & Stephen F. Ferrari

  3. Department of Zoology, Federal University of Pernambuco, Recife, Brazil

    Bárbara Moraes & João Pedro Souza-Alves

  4. Department of Ecology, Federal University of Sergipe, São Cristóvão, Brazil

    Stephen F. Ferrari

Authors
  1. Renato R. Hilário
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bárbara Moraes
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. João Pedro Souza-Alves
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Stephen F. Ferrari
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

RRH developed the methodological procedures, conducted fieldwork, analyzed the data, and wrote the manuscript. BM and JPSA gathered landscape data, and helped to write the manuscript. SFF provided editorial and academic advice and helped to write the manuscript.

Corresponding author

Correspondence to Renato R. Hilário.

Additional information

Handling Editor: Joanna Setchell

Supplementary Information

ESM 1

(PDF 217 kb)

ESM 2

(PDF 38 kb)

ESM 3

(PDF 47.8 kb)

ESM 4

(PDF 45 kb)

ESM 5

(PNG 729 kb)

High resolution image (TIF 108 kb)

ESM 6

(XLSX 19 kb)

ESM 7

(PDF 49 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hilário, R.R., Moraes, B., Souza-Alves, J.P. et al. The Density of Callicebus coimbrai is Better Predicted by Vegetation Structure Variables than by Surrounding Landscape. Int J Primatol 45, 54–71 (2024). https://doi.org/10.1007/s10764-022-00278-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10764-022-00278-y

Keywords

Search

Navigation