Effect of fragmentation and landscape composition on the presence of Ateles fusciceps in Colombia

Authors

DOI:

https://doi.org/10.62015/np.2024.v30.788

Keywords:

Connectivity, Human impact, Conservation, Landscape

Abstract

Habitat fragmentation, associated with biodiversity loss and declining populations of wild species, negatively impacts essential ecological resources for primates, such as food and reproduction. Fragmentation and changes in landscape composition affect the structural connectivity of the landscape and represent a significant threat to the Colombian black headed spider monkey (Ateles fusciceps rufiventris), one of the most threatened primates due to its susceptibility to deforestation and hunting. Its conservation status is not yet updated and its responses to landscape disturbance are still unknown. This study aims to assess how landscape fragmentation and composition influence the presence of A. f. rufiventris in Colombia. We carried out analyses on 23 localities with potential habitat for A. f. rufiventris in Colombia. This was done to evaluate how different landscape composition characteristics, such as the type and amount of habitat and connectivity between fragments, influence the presence and behavior of the subspecies. To this end, data on the presence of the species were collected and the composition of the landscape was characterized using fragmentation metrics analysis. The presence of A. f. rufiventris was confirmed at 52% (n=12) of the assessed localities. Our results revealed that areas with larger area of mature forest and less human disturbance have a higher probability of A. f. rufiventris presence. In addition, proximity to human settlements affects the presence of A. f. rufiventris negatively. Although habitat fragmentation did not show a significant relationship with the presence of A. f. rufiventris, it is essential to mitigate its effects through the protection and restoration of existing forests, as well as the implementation of biocorridors that favor ecological connectivity and an increase in the proportion of forests in the landscape. It is also a priority to develop programs aimed at improving the structure and composition of the landscape in the face of expanding human activities.

References

Altrichter, M. y Carbonell, F. 2013. Efectos de la cacería en la Reserva Indígena Talamanca Bribrí-Cabécar e importancia del parque internacional La Amistad, Costa Rica. R. Lat. Conserv. 3(2): 38–47.

Aquino, R., Cornejo, F. M., Pezo, E. y Heymann, E. W. 2012. Distribution and abundance of white-fronted spider monkeys, Ateles belzebuth (Atelidae), and threats to their survival in Peruvian Amazonia. Folia Primatol. 84(1): 1–10.

Arroyo-Rodríguez, V. y Mandujano, S. 2006. Forest fragmentation modifies habitat quality for Alouatta palliata. Int. J. Primatol. 27: 1079–1096. https://doi.org/10.1007/s10764-006-9061-0

Arroyo-Rodríguez, V. y Mandujano, S. 2009. Conceptualization and measurement of habitat fragmentation from the primates’ perspective. Int. J. Primatol. 30: 497–514. https://doi.org/10.1007/s10764-009-9355-0

Arroyo-Rodríguez, V. y Dias, P. 2010. Effects of habitat fragmentation and disturbance on howler monkeys: a review. Am. J. Primatol. 72(1): 1–16. https://doi.org/10.1002/ajp.20753

Arroyo-Rodríguez, V. et. al. 2017. Spider monkeys in human-modified landscapes: the importance of the matrix. Trop. Conserv. Sci. 10: 1940082917719788. https://doi.org/10.1177/1940082917719788

Arroyo‐Rodríguez, V. et al. 2021. Preserving 40% forest cover is a valuable and well‐supported conservation guideline: reply to Banks‐Leite et al. Ecol. Lett. 24(5): 1114–1116. https://doi.org/10.1111/ele.13689

Asensio, N., Schaffner, C. M. y Aureli, F. 2012. Variability in core areas of spider monkeys (Ateles geoffroyi) in a tropical dry forest in Costa Rica. Primates 53: 147–56. https://doi.org/10.1007/s10329-011-0288-9

Asensio, N., Murillo-Chacon, E., Schaffner, C. M. y Aureli, F. 2017. The effect of roads on spider monkeys’ home range and mobility in a heterogeneous regenerating forest. Biotropica 49(4): 546–554. https://doi.org/10.1111/btp.12441

Aureli, F. et al. 2008. Fission-fusion dynamics: new research frameworks. Curr. Anthropol. 49(4): 627–654. https://doi.org/10.1086/586708

Benchimol, M. y Peres, C. A. 2013. Anthropogenic modulators of species–area relationships in Neotropical primates: a continental‐scale analysis of fragmented forest landscapes. Divers. Distrib. 19(11): 1339–1352. https://doi.org/10.1111/ddi.12111

Bersacola, E., Hill, C.M. y Hockings, K.J. 2021. Chimpanzees balance resources and risk in an anthropogenic landscape of fear. Sci. Rep. 11: 4569. https://doi.org/10.1038/s41598-021-83852-3

Bonilla, N. S. 2021. Especies de interés especial cerro Tacarcuna-Chocó, en el marco del proyecto Colombia BIO (v1.5) [Dataset/Checklist]. Instituto de Investigaciones Ambientales del Pacífico John Von Neumann - IIAP. https://doi.org/10.15472/ahkz3n

Campbell, C. J. 2000. The reproductive biology of black-handed spider monkeys (Ateles geoffroy): integrating behavior and endocrinology. Doctorate thesis, University of California–Berkeley, Berkeley, CA, EUA.

Campbell, C. J. y Gibson, K. N. 2008. Spider monkey reproduction and sexual behavior. En: Spider monkeys: Behavior, Ecology and Evolution of the Genus Ateles, C. J. Campbell (ed.), pp.266–287. Cambridge University Press, New York, NY.

Cervera, L. y Griffith, D. 2016. New Population and Range Extension of the Critically Endangered Ecuadorian Brown-Headed Spider Monkey (Ateles fusciceps fusciceps) in Western Ecuador. Trop. Conserv. Sci. 9: 167–77. https://doi.org/10.1177/19400829160090010

Chaves, O. M., Stoner, K. E. y Arroyo‐Rodríguez, V. 2012. Differences in diet between spider monkey groups living in forest fragments and continuous forest in Mexico. Biotropica 44(1): 105–113. https://doi.org/10.1111/j.1744-7429.2011.00766.x

Clerici, N., Salazar, C., Pardo‐Díaz, C., Jiggins, C. D., Richardson, J. E. y Linares, M. 2019. Peace in Colombia is a critical moment for Neotropical connectivity and conservation: save the northern Andes–Amazon biodiversity bridge. Conserv. Lett. 12(1) : e12594. https://doi.org/10.1111/conl.12594

Correa-Ayram, C. A., Mendoza, M. E. y López Granados, E. 2014. Análisis del cambio en la conectividad estructural del paisaje (1975-2008) de la cuenca del lago Cuitzeo, Michoacán, México. Rev. Geogr. Norte Gd. 59: 7–23. http://dx.doi.org/10.4067/S0718-34022014000300002

Correa-Ayram, C., Etter, A., Díaz-Timoté, J., Buriticá, S. R., Ramírez, W. y Corzo, G. 2020. Spatiotemporal evaluation of the human footprint in Colombia: Four decades of anthropic impact in highly biodiverse ecosystems. Ecol. Indic. 117: 106630. https://doi.org/10.1016/j.ecolind.2020.106630

Cowlishaw, G. y Dunbar, R. 2000. Primate conservation biology. University of Chicago Press, Chicago.

Daskalova, G. N., Myers-Smith, I. H., Bjorkman, A. D., Blowes, S. A., Supp, S. R., Magurran, A. E. y Dornelas, M. 2020 Landscape-scale forest loss as a catalyst of population and biodiversity change. Science 368: 1341–1347. https://doi.org/10.1126/science.aba1289

Dew, J. L. 2005. Foraging, food choice, and food processing by sympatric ripe-fruit specialists: Lagothrix lagotricha poeppigii and Ateles belzebuth belzebuth. Int. J. Primatol. 26: 1107–1135. https://doi.org/10.1007/s10764-005-6461-5

Di Bitetti, M. S., Paviolo, A. y De Angelo, C. 2014. Camera trap photographic rates on roads vs. off roads: location does matter. Mastozool. Neotrop. 27(1): 37–46.

Di Fiore, A. y Campbell, C. J. 2007. The atelines: variation in ecology, behavior and social organization. En: Primates in Perspective, C. J. Campbell, A. Fuentes, K. C. MacKinnon, M. Panger y S. K. Beader (eds.), pp.155–185. Oxford University Press, New York, NY.

Di Fiore, A., Link, A. y Dew, J. L. 2008. Diets of wild spider monkeys. En: Spider monkeys: Behavior, ecology and evolution of the genus Ateles. C. J. Campbell (ed.), pp.81–137. Cambridge University Press, Cambridge.

Dunn, J. C., Cristóbal-Azkarate, J. y Vea, J. J. 2009. Differences in diet and activity pattern between two groups of Alouatta palliata associated with the availability of big trees and fruit of top food taxa. Am. J. Primatol. 71: 654–662. https://doi.org/10.1002/ajp.20700

ESRI (2020). ArcGIS Desktop (Version 10.5). Environmental Systems Research Institute.

Estrada, A. et al. 2017. Impending extinction crisis of the world’s primates: why primates matter. Sci. Adv. 3(1): e1600946. https://doi.org/10.1126/sciadv.1600946

Etter, A., McAlpine, C., Wilson, K., Phinn, S. y Possingham, H. 2006. Regional patterns of agricultural land use and deforestation in Colombia. Agric. Ecosyst. Environ. 114: 369–86. https://doi.org/10.1016/j.agee.2005.11.013

Fagua, J. C., Baggio, J. A. y Ramsey, R. D. 2019. Drivers of forest cover changes in the Chocó‐Darien Global Ecoregion of South America. Ecosphere 10(3): e02648. https://doi.org/10.1002/ecs2.2648

Fahrig, L. 2003. Effects of habitat fragmentation on biodiversity. Annu. Rev. Ecol. Evol. Syst. 34(1): 487–515. https://doi.org/10.1146/annurev.ecolsys.34.011802.132419

Fahrig, L. 2017. Ecological responses to habitat fragmentation per se. Annu. Rev. Ecol. Evol. Syst. 48:1–23. https://doi.org/10.1146/annurev-ecolsys-110316-022612

Fletcher, Jr., R. J. et al. 2018. Is habitat fragmentation good for biodiversity? Biol. Conserv. 226: 9–15.

Fedigan, L. M., Fedigan, L, Chapman, C. y Glander, K. 1988. Spider monkey home ranges: A comparison of radio telemetry and direct observation. Am. J. Primatol. 16: 19–29. https://doi.org/10.1002/ajp.1350160104

Galán-Acedo, C., Arroyo-Rodríguez, V., Estrada, A. y Ramos-Fernández, G. 2018. Forest cover and matrix functionality drive the abundance and reproductive success of an endangered primate in two fragmented rainforests. Landsc. Ecol. 34(1): 147–15. https://doi:10.1007/s10980-018-0753-6

Galán-Acedo, C., Arroyo-Rodríguez V., Andresen E. y Arasa-Gisbert, R. 2019a. Ecological traits of the world’s primates. Sci. Data 6: 55. https://doi.org/10.1038/s41597-019-0059-9

Galán-Acedo, C., Arroyo-Rodríguez, V. y Cudney-Valenzuela, S. J. 2019b. A global assessment of primate responses to landscape structure. Biol. Rev. 94(5): 1605–1618. https://doi.org/10.1111/brv.12517

Galán-Acedo, C., Arroyo-Rodríguez, V. y Chapman, C. A. 2021. Beyond patch size: the impact of regional context and habitat quality on three endangered primates. Perspect. Ecol. Conserv. 19(2): 207–215. https://doi.org/10.1016/j.pecon.2021.02.004

Galán-Acedo, C., Verde Arregoitia, L. D., Arasa-Gisbert, R., Auliz-Ortiz, D., Saldívar-Burrola, L. L., Gouveia, S.F., Correia, I., Rosete-Vergés, F. A., Dinnage, R. y Villalobos, F. 2024. Global primary predictors of extinction risk in primates. Proc. R. Soc. B: Biol. Sci. 291(2032). https://doi.org/10.1098/rspb.2024.1905

Gómez, L., Suárez, C., Trujillo, A., Bravo, A. M., Rojas, V., Hernandez, N. y Vargas, M. C. 2014. Landscape management in Chocó-Darién priority watersheds. WWF-Colombia, Bogotá.

Gorresen, P. M. y Willig, M. R. 2004. Landscape Responses of Bats to Habitat Fragmentation in Atlantic Forest of Paraguay. J. Mammal. 85: 688–97. https://doi.org/10.1644/BWG-125

Haddad, N. M. et al. 2015. Habitat fragmentation and its lasting impact on Earth’s ecosystems. Sci. Adv. 1:e1500052. https://doi.org/10.1126/sciadv.1500052

Harcourt, A. H. y Doherty, D. A. 2005. Species-area relationships of primates in tropical forest fragments: a global analysis. J. Appl. Ecol. 42: 630–637. https://doi.org/10.1111/j.1365-2664.2005.01037.x

Hernández-Jaramillo, A., Shanee, S. y Serio-Silva, J. C. 2024. Range-wide distribution survey, habitat modeling, and characterization of conservation threats to the Colombian Black Spider Monkey (Ateles fusciceps rufiventris) in Colombia. Intl. J. Primatol. 46(1): 96–121. https://doi.org/10.1007/s10764-024-00457-z

Hill, J. L. y Curran, P. J. 2003. Area, shape and isolation of tropical forest fragments: effects on tree species diversity and implications for conservation. J. Biogeogr. 30(9): 1391–1403.

IDEAM. 2017. Mapas continentales, costeros y marinos de Colombia (MEC), escala 1:100.000. Instituto de Hidrología, Meteorología y Estudios Ambientales.

IUCN. 2019. Guidelines for using the IUCN Red List categories and criteria. Version 14. Prepared by the Standards and Petitions Committee.

Jackson, H. B. y Fahrig, L. 2015. Are ecologists conducting research at the optimal scale? Glob. Ecol. Biogeogr. 24(1): 52–63. https://doi.org/10.1111/geb.12233

Klein, L. L. y Klein, D. B., 1977. Feeding behaviour of the Colombian spider monkey. En: Primate Ecology: Studies of Feeding and Ranging Behaviour in Lemurs, Monkeys and Apes, T. H. Clutton-Brock (ed.), pp.153–181, Academic Press, London.

Klingbeil, B. T. y Willig, M. R. 2009. Guild-specific responses of bats to landscape composition and configuration in fragmented Amazonian rainforest. J. Appl. Ecol. 46: 203–13.

Link, A., De Luna, A. G., Alfonso, F., Giraldo-Beltran, P. y Ramirez, F. 2010. Initial effects of fragmentation on the density of three Neotropical primate species in two lowland forests of Colombia. Endanger. Species Res. 13: 41–50.

McGarigal, K. y Marks, B. J. 1994. FRAGSTATS: spatial pattern analysis program for quantifying landscape structure. Version 2.0. Forest Science Department, Oregon State University, Corvallis.

McGarigal, K., Sam, A. C., Maile, C. N. y Eduard, E. 2002. FRAGSTATS: spatial pattern analysis program for categorical maps. University of Massachusetts, Amherst. Website: fragstats.org

Mancini, G., Benítez-López, A., Di Marco, M., Pacifici, M., Rondinini, C. y Santini, L. 2023. Synergistic effects of habitat fragmentation and hunting on the extinction risk of neotropical primates. Biodivers. Conserv. 32(8): 2655–2669.

Marsh, L. K. 2003. Primates in fragments: Ecology and Conservation. Kluwer Academic/Plenum Publishers, New York, NY.

Marsh, L. K., Chapman, C. A., Arroyo-Rodríguez, V., Cobden, A. K., Dunn, J. C., Gabriel, D., Ghai, R., Nijman, V., Reyna-Hurtado, R., Serio-Silva, J. C. y Wasserman, M. D. 2013. En: Primates in Fragments 10 Years Later: Once and Future Goals, L. K. Marsh y C. A. Chapman (eds.), pp.505–525. Springer, New York, NY.

Marsh, L. K. y Chapman, C. A. 2013. Primates in Fragments: Complexity and Resilience. Springer, New York, NY.

Marsh, C., Link, A., King-Bailey, G. y 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 Primatol. 87: 17–30.

Marsh, C. W., Johns, A. D. y Ayres, J. M. 1987. Effects of habitat disturbance on rain forest primates. En: Primate Conservation in the Tropical Rain Forest, W. Y. Brockelman, R. Ali, C. W. Marsh y R. A. Mittermeier (eds.), pp.83–108. AR Liss, New York, N.Y.

Mateucci, S. D. y Silva, M. 2005. Selección de métricas de configuración espacial para la regionalización de un territorio antropizado. GeoFocus 5: 180–202.

Miguet, P., Jackson, H. B., Jackson, N. D., Martin, A. E. y Fahrig, L. 2016. What determines the spatial extent of landscape effects on species? Landsc. Ecol. 31(6): 1177–1194. https://doi.org/10.1007/s10980-015-0314-1

Moscoso, P. 2010. Estado poblacional del mono araña de cabeza café (Ateles fusciceps) en el noroccidente del Ecuador, con notas ecológicas de una relación interespecífica con Alouatta palliata. Tesis de Licenciatura en Ciencias, Pontificia Universidad Católica del Ecuador, Quito, Ecuador.

Myers, N., Mittermeier, R. A., Mittermeier, C. G., Da Fonseca, G. A. y Kent, J. 2000. Biodiversity hotspots for conservation priorities. Nature 403: 853–58. https://doi.org/10.1038/35002501

Negret, P. J., James, A., Braczkowski, A., Maron, M. y Watson, E. M. 2017. Need for conservation planning in postconflict Colombia. Conserv. Biol. 31: 499–500. https://doi.org/10.1111/cobi.12935

Newing, H., Eagle, C., Puri, R. K. y Watson, C. W. 2011. Conducting research in conservation. Routledge, Oxfordshire, Oxford.

Ordóñez-Gómez, J. D., Arroyo-Rodríguez, V., Nicasio-Arzeta, S. y Cristóbal-Azkarate, J. 2014. Which is the appropriate scale to assess the impact of landscape spatial configuration on the diet and behavior of spider monkeys? Am. J. Primatol. 77(1): 56–65. https://doi.org/10.1002/ajp.22310

Patton, M. 2002. Qualitative research y evaluation methods (3rd edition). Sage, Thousand Oaks, Canada. Peck, M., Thorn, J., Mariscal, A., Baird, A., Tirira, D. y Kniveton, D. 2011. Focusing conservation efforts for the Critically Endangered Brown-headed spider monkey (Ateles fusciceps) using remote sensing, modeling, and playback survey methods. Int. J. Primatol. 32: 134–48.

Peres, C. A. 1990. Effects of hunting on western Amazonian primate communities. Biol. Conserv. 54: 47–59.

Peres, C. A. 2001. Synergistic effects of subsistence hunting and habitat fragmentation on Amazonian forest vertebrates. Conserv. Biol. 15(6): 1490–1505. https://doi.org/10.1046/j.1523-1739.2001.01089.x

Peres, C. A., Emilio, T., Schietti, J., Desmoulière, S. J. y Levi, T. 2016. Dispersal limitation induces long-term biomass collapse in overhunted Amazonian forests. Proc. Natl. Acad. Sci., U.S.A. 113(4): 892–897. ttps://doi.org/10.1073/pnas.1516525113

Pérez-Peña, P. E. et al. 2018. Impacto de factores antropogénicos en la abundancia de primates al norte de la Amazonía peruana. En: La primatología en Latinoamérica 2, B. Urbani, M. Kowalewski, R. G. T. Cunha, S. de la Torre S y L. Cortés-Ortiz (eds.), pp.597–610. Instituto Venezolano de Investigaciones Cientícas (IVIC), Caracas, Venezuela.

Pozo, R. W. E. 2001. Social behavior and diet of the spider monkey, Ateles belzebuth, in the Yasuni National Park, Ecuador. Neotrop. Primates 9: 74.

Ramos-Fernández, G. y Wallace, R. B. 2008. Spider monkey conservation in the twenty-first century: recognizing risks and opportunities. En: Spider monkeys: Behavior, Ecology and Evolution of the Genus Ateles, C. J. Campbell (ed.), pp.351–76. Cambridge University Press, Cambridge. http://doi.org/10.1017/CBO9780511721915.013

Rangel-Ch, O. J. y Arellano-P., H. 2004. Clima del Chocó biogeográfico/Costa pacífica de Colombia. En: Colombia Diversidad Biótica. IV. El Chocó Biogeográfico/Costa Pacífica, J. O. Rangel-Ch (ed). pp.39–82. Instituto de Ciencias Naturales-Conservación Internacional, Bogotá, Colombia.

Ravetta, A. L. y Ferrari, S. F. 2009. Geographic distribution and population characteristics of the endangered white-fronted spider monkey (Ateles marginatus) on the lower Tapajós River in central Brazilian Amazonia. Primates 50: 261–268. https://doi.org/10.1007/s10329-009-0146-1

R Core Team. 2024. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

Rimbach, R., Link, A., Heistermann, M., Gómez-Posada, C., Galvis, N. y Heymann, E. W. 2013. Effects of logging, hunting, and forest fragment size on physiological stress levels of two sympatric ateline primates in Colombia. Conserv. Physiol. 1: 1–11. https://doi.org/10.1093/conphys/cot031

Rybicki, J. y Hanski, I. 2013. Species–area relationships and extinction caused by habitat loss and fragmentation. Ecol. Lett. 16: 27–38. https://doi.org/10.1111/ele.12065

Rylands, A. B. y Keuroghlian, A. 1988. Primate populations in continuous forest and forest fragments in Central Amazonia. Acta Amaz. 18(3–4): 291–307. https://doi.org/10.1590/1809-43921988183307

Saldívar-Burrola, L. L., Martínez-Ruíz, M., Arroyo-Rodríguez, V., Villalobos, F., Dias, P. A., López-Barrera, F. y Arasa-Gisbert, R. 2022. Can secondary forests mitigate the negative effect of old-growth forest loss on biodiversity? A landscape-scale assessment of two endangered primates. Landsc. Ecol. 37(12): 3223–3238. https://doi.org/10.1007/s10980-022-01532-7

Saura, S. y Martínez-Millán, J. 2001. Sensitivity of Landscape Pattern Metrics to Map Spatial Extent. Photogramm. Eng. Remote Sens. 67(9): 1027–1036.

Shimooka, Y. et al. 2008. Demography and group composition of Ateles. En: Spider Monkeys: Behavior, Ecology and Evolution of the Genus Ateles, C. J. Campbell (ed.), pp.329–348. Cambridge University Press, Cambridge.

Sorensen, T. C. y Fedigan, L. M. 2000. Distribution of three monkey species along a gradient of regenerating tropical dry forest, Biol. Conserv. 92: 227–240.

Suarez, S. A. 2006. Diet and travel costs for spider monkeys in a nonseasonal, hyperdiverse environment. Int. J. Primatol. 27: 411–436. https://doi.org/10.1007/s10764-006-9023-6

Symington, M. M. 1990. Fission-fusion social organization in Ateles and Pan. Int. J. Primatol. 11: 47–61. https://doi.org/10.1007/BF02193695

Terborgh, J. 1986. Community aspects of frugivory in tropical forests. En: Frugivores and seed dispersal, A. Estrada y T. H. Fleming (eds.), pp.371–384. Springer Netherlands, Dordrecht.

Tójar, J. 2006. Investigación cualitativa. Comprender y actuar. La Muralla, Madrid.

Turner, M. G., Gardner, R. H. y O’Neill, R. V. 2001. Landscape Ecology in Theory and Practice: Pattern and Process. Springer. https://doi.org/10.1007/978-1-4939-2794-4

Wallace, R. B. 2006. Seasonal variations in black‐faced black spider monkey (Ateles chamek) habitat use and ranging behavior in a southern Amazonian tropical forest. Am. J. Primatol. 68(4): 313–332. https://doi.org/10.1002/ajp.2022

Wallace, R. B. 2008. Factors influencing spider monkey habitat use and ranging patterns. En: Spider Monkeys: Behavior, Ecology and Evolution of the Genus Ateles, C. J. Campbell (ed.), pp.138–54. Cambridge University Press, Cambridge.

Downloads

Additional Files

Published

2024-12-01

Data Availability Statement

The complete datasets used are available from the lead author upon reasonable request.

Issue

Section

Articles

How to Cite

Alma Hernandez, Serio-Silva, J. C., & Shanee, S. (2024). Effect of fragmentation and landscape composition on the presence of Ateles fusciceps in Colombia. Neotropical Primates, 30(2). https://doi.org/10.62015/np.2024.v30.788