Abstract
Introduction: Medium and large-sized mammals are threatened globally due to habitat loss and fragmentation. In Costa Rica, forest fragments that remain outside protected areas may serve as a refuge or corridor for these animals. Mammal presence in fragmented landscapes may be influenced by resource availability, which varies greatly in seasonal regions. Objective: To determine the species richness of medium and large-sized mammals in a forest fragment, and to examine if species diversity and detectability varied between the wet and dry season. Methods: We established 26 camera trap stations throughout the Municipal Forest of Atenas (Alajuela, Costa Rica), a 26.4 ha forest fragment that provides water to about 1 800 people. From August 2021 to April 2022, one camera trap was active at each station for 12-21 days throughout each season (dry and wet), for a total of 810 camera trap days. We applied rarefaction and extrapolation curves to characterize mammal’s species diversity and compare it between seasons. Results: We detected 19 species of mammals. The most frequently detected species were the White-nosed Coati (Nasua narica; 0.254 detections/camera trap day), and the Central American Agouti (Dasyprocta punctata; 0.163 detections/camera trap day). We also registered four species considered as endangered in Costa Rica, three felines: Puma concolor, Herpailurus yagouaroundi, Leopardus pardalis, and the Neotropical River Otter, Lontra longicaudis. Seasonality did not affect species diversity, but it influenced dominant species and detectability, which was greater during the wet season. Conclusions: Our study demonstrates how protecting small forest fragments, can help conserve endangered medium and large-sized mammals in human-dominated landscapes.
Objective: We aimed to determine the species richness of medium and large-sized mammals in a forest fragment protected for water production, and to examine if species diversity and detectability varied between the wet and dry season.
Methods: We established 26 camera trap stations throughout the Municipal Forest of Atenas (MFA), a 26-ha forest fragment that provides drinking water to about 1 800 people. From August 2021 to April 2022, one camera trap was active at each station for 12-21 days throughout each season (dry and wet), for a total of 810 camera trap days. We applied rarefaction and extrapolation curves to characterize mammal’s species diversity and compare it between seasons.
Results: We detected 19 species of medium and large-sized mammals. The species with the highest frequency of detections were the White-nosed Coati (Nasua narica; 0.504 detections/camera trap day), and the Central American Agouti (Dasyprocta punctata; 0.377 detections/camera trap day). We also detected four species considered as endangered in Costa Rica, three felines: Puma concolor, Herpailurus yagouaroundi, Leopardus pardalis, and the Neotropical River Otter, Lontra longicaudis. Seasonality did not affect species diversity but influenced the detectability of dominant species.
Discussion: The relatively high richness of mammals observed in the MFA is likely related to the surrounding land use, which is dominated by agroforestry systems (e. g., coffee plantations) and forest patches, that may contribute to animal mobility and serve as refuge in fragmented landscapes.
Conclusions: Our study demonstrates how protecting ecosystem services, such as water, may also help conserving endangered medium and large-sized mammals in fragmented landscapes.
References
Alroy, J. (2017). Effects of habitat disturbance on tropical forest biodiversity. Proceedings of the National Academy of Sciences, 114(23), 6056–6061. https://doi.org/10.1073/pnas.1611855114
Avalos, G., Hoell, K., Gardner, J., Anderson, S., & Lee, C. (2006). Impact of the invasive plant Syzigium jambos (Myrtaceae) on patterns of understory seedling abundance in a tropical premontane forest, Costa Rica. Revista de Biología Tropical, 54(2), 415–421.
Basset, Y., Cizek, L., Cuénoud, P., Didham, R. K., Novotny, V., Ødegaard, F., Roslin, T., Tishechkin, A. K., Schmidl, J., Winchester, N. N., Roubik, D. W., Aberlenc, H. P., Bail, J., Barrios, H., Bridle, J. R., Castaño-Meneses, G., Corbara, B., Curletti, G., Duarte da Rocha, W., … Leponce, M. (2015). Arthropod Distribution in a Tropical Rainforest: Tackling a four dimensional puzzle. PLOS ONE, 10(12), e0144110. https://doi.org/10.1371/journal.pone.0144110
Beca, G., Vancine, M. H., Carvalho, C. S., Pedrosa, F., Alves, R. S. C., Buscariol, D., Peres, C. A., Ribeiro, M. C., & Galetti, M. (2017). High mammal species turnover in forest patches immersed in biofuel plantations. Biological Conservation, 210(2017), 352–359. https://doi.org/10.1016/j.biocon.2017.02.033
Beck-King, H., Helversen, O. von, & Beck-King, R. (1999). Home range, population density, and food resources of Agouti paca (Rodentia: Agoutidae) in Costa Rica: a study using alternative methods. Biotropica, 31(4), 675–685. https://doi.org/10.1111/j.1744-7429.1999.tb00417.x
Bogoni, J. A., Peres, C. A., & Ferraz, K. M. P. M. B. (2020). Extent, intensity and drivers of mammal defaunation: A continental-scale analysis across the Neotropics. Scientific Reports, 10(1), 14750. https://doi.org/10.1038/s41598-020-72010-w
Botelho, A. L. M., Calouro, A. M., Borges, L. H. M., & Chaves, W. A. (2012). Large and medium-sized mammals of the Humaitá Forest Reserve, southwestern Amazonia, state of Acre, Brazil. Check List, 8(6), 1190. https://doi.org/10.15560/8.6.1190
Brassil, E., Burris, B., Godlove, S., Martin, M., Merrow, O., Rectenwald, H., & Rust, M. (2000). Floristic composition, species richness, and vertical structural attributes of El Bosque Municipal de Atenas. School for Field Studies Center for Sustainable Development, Directed Research.
Burgin, C. J., Colella, J. P., Kahn, P. L., & Upham, N. S. (2018). How many species of mammals are there? Journal of Mammalogy, 99(1), 1–14. https://doi.org/10.1093/jmammal/gyx147
Chao, A., Gotelli, N. J., Hsieh, T. C., Sander, E. L., Ma, K. H., Colwell, R. K., & Ellison, A. M. (2014). Rarefaction and extrapolation with Hill numbers: A framework for sampling and estimation in species diversity studies. Ecological Monographs, 84(1), 45–67. https://doi.org/10.1890/13-0133.1
Coulon, A., Cosson, J. F., Angibault, J. M., Cargnelutti, B., Galan, M., Morellet, N., Petit, E., Aulagnier, S., & Hewison, A. J. M. (2004). Landscape connectivity influences gene flow in a roe deer population inhabiting a fragmented landscape: An individual-based approach. Molecular Ecology, 13(9), 2841–2850. https://doi.org/10.1111/j.1365-294X.2004.02253.x
Cove, M. V., Spínola, R. M., Jackson, V. L., Sàenz, J. C., & Chassot, O. (2013). Integrating occupancy modeling and camera-trap data to estimate medium and large mammal detection and richness in a central american biological corridor. Tropical Conservation Science, 6(6), 781–795. https://doi.org/10.1177/194008291300600606
Crooks, K. (2002). Relative sensitivities of mammalian carnivores to habitat fragmentation. Conservation Biology, 16(2), 488–502.
Crooks, K. R., Burdett, C. L., Theobald, D. M., King, S. R. B., Di Marco, M., Rondinini, C., & Boitani, L. (2017). Quantification of habitat fragmentation reveals extinction risk in terrestrial mammals. Proceedings of the National Academy of Sciences, 114(29), 7635–7640. https://doi.org/10.1073/pnas.1705769114
da Silva, N. A. P., Frizzas, M. R., & Oliveira, C. M. de (2011). Seasonality in insect abundance in the “Cerrado” of Goiás State, Brazil. Revista Brasileira de Entomologia, 55(1), 79–87. https://doi.org/10.1590/S0085-56262011000100013
Daily, G. C., Ceballos, G., Pacheco, J., Suzán, G., & Sánchez-Azofeifa, A. (2003). Countryside biogeography of neotropical mammals: conservation opportunities in agricultural landscapes of Costa Rica. Conservation Biology, 17(6), 1814–1826. https://doi.org/10.1111/j.1523-1739.2003.00298.x
Dalecky, A., Chauvet, S., Ringuet, S., Claessens, O., Judas, J., Larue, M., & Cosson, J. F. (2002). Large mammals on small islands: Short term effects of forest fragmentation on the large mammal fauna in french Guiana. Revue d’Ecologie, Terre et Vie, Société Nationale de Protection de La Nature, 8, 145–164.
Darosci, A. A. B., Takahashi, F. S. C., Proença, C. E. B., Soares-Silva, L. H., & Munhoz, C. B. R. (2021). Does spatial and seasonal variability in fleshy-fruited trees affect fruit availability? A case study in gallery forests of Central Brazil. Acta Botanica Brasilica, 35(3), 456–465. https://doi.org/10.1590/0102-33062020abb0279
digiKam Developers Team. (2021). DigiKam. www.digikam.org
Dillon, A., & Kelly, M. J. (2008). Ocelot home range, overlap and density: Comparing radio telemetry with camera trapping. Journal of Zoology, 275(4), 391–398. https://doi.org/10.1111/j.1469-7998.2008.00452.x
Edwards, D. P., Tobias, J. A., Sheil, D., Meijaard, E., & Laurance, W. F. (2014). Maintaining ecosystem function and services in logged tropical forests. Trends in Ecology & Evolution, 29(9), 511–520. https://doi.org/10.1016/j.tree.2014.07.003
Emsens, W. J., Hirsch, B. T., Kays, R., & Jansen, P. A. (2014). Prey refuges as predator hotspots: Ocelot (Leopardus pardalis) attraction to agouti (Dasyprocta punctata) dens. Acta Theriologica, 59(2), 257–262. https://doi.org/10.1007/s13364-013-0159-4
Gargiullo, M. B., Magnuson, B. L., & Kimball, L. D. (2008). A field guide to plants of Costa Rica. Oxford University Press.
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(4), 331–344. https://doi.org/10.1017/S0266467413000370
Häger, A., Fernández Otárola, M., Stuhlmacher, M. F., Acuña Castillo, R., & Contreras Arias, A. (2015). Effects of management and landscape composition on the diversity and structure of tree species assemblages in coffee agroforests. Agriculture, Ecosystems & Environment, 199, 43–51. https://doi.org/10.1016/j.agee.2014.08.022
Haro-Carrión, X., Johnston, J., & Bedoya-Durán, M. J. (2021). Landscape Structure and Seasonality: Effects on Wildlife Species Richness and Occupancy in a Fragmented Dry Forest in Coastal Ecuador. Remote Sensing, 13(18), 3762. https://doi.org/10.3390/rs13183762
Harvey, P. (2022). ExifTool. https://exiftool.org/
Holland, M. B. (2012). Mesoamerican biological corridor. In J. A. Hilty, C. C. Chester, & M. S. Cross (Eds.), Climate and conservation (pp. 56–66). Island Press. https://doi.org/10.5822/978-1-61091-203-7_5
Hsieh, T. C., Ma, K. H., & Chao, A. (2016). iNEXT: An R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods in Ecology and Evolution, 7(12), 1451–1456. https://doi.org/10.1111/2041-210X.12613
Instituto Costarricense de Acueductos y Alcantarillados. (2016). Política Nacional de Agua Potable de Costa Rica 2017–2030 (Comisión Interinstitucional). Instituto Costarricense de Acueductos y Alcantarillados, Costa Rica.
Jost, L. (2006). Entropy and diversity. Oikos, 113(2), 363–375. https://doi.org/10.1111/j.2006.0030-1299.14714.x
Koptur, S. (1983). Flowering phenology and floral biology of Inga (Fabaceae: Mimosoideae). Systematic Botany, 8(4), 354–368.
Lacher, T. E., Davidson, A. D., Fleming, T. H., Gómez-Ruiz, E. P., McCracken, G. F., Owen-Smith, N., Peres, C. A., & Vander-Wall, S. B. (2019). The functional roles of mammals in ecosystems. Journal of Mammalogy, 100(3), 942–964. https://doi.org/10.1093/jmammal/gyy183
McConkey, K. R., Prasad, S., Corlett, R. T., Campos-Arceiz, A., Brodie, J. F., Rogers, H., & Santamaria, L. (2012). Seed dispersal in changing landscapes. Biological Conservation, 146(1), 1–13. https://doi.org/10.1016/j.biocon.2011.09.018
Michalski, F., & Peres, C. A. (2007). Disturbance-mediated mammal persistence and abundance-area relationships in amazonian forest fragments. Conservation Biology, 20(6), 1626–1640. https://doi.org/10.1111/j.1523-1739.2007.00797.x
Ministerio de Ambiente y Energía (2017). Reglamento a la Ley de Conservación de Vida Silvestre, no. N 40548-MINAE, Sistema Nacional de Áreas de Conservación. Ministerio de Ambiente y Energía, Costa Rica.
Morera, C., & Sandoval, L. (2019). Fragmentación y conectividad de la cobertura natural a nivel cantonal en Costa Rica durante los años 2000 y 2015. Revista Geográfica de América Central, 4(61E), 37. https://doi.org/10.15359/rgac.61-4.2
Morera, C., Sandoval, L. F., & Alfaro, L. D. (2021). Ecological corridors in Costa Rica: An evaluation applying landscape structure, fragmentation‐connectivity process, and climate adaptation. Conservation Science and Practice, 3(8), e475. https://doi.org/10.1111/csp2.475
Niedballa, J., Sollmann, R., Courtiol, A., & Wilting, A. (2016). camtrapR: An R package for efficient camera trap data management. Methods in Ecology and Evolution, 7(12), 1457–1462. https://doi.org/10.1111/2041-210X.12600
Patel, C. R., Heiplanmi Rymbai, Patel, N. L., Ahlawat, T. R., Tandel, Y. N., Saravaiya, S. N., Swamy, G. S. K., Nataraja, K. H., & Sabarad, A. (2017). Rose apple (Syzygium jambos (L.) Alston). In S. N. Ghosh, A. Singh, & A. Thakur (Eds.), Underutilized fruit crops: Importance and cultivation (pp. 1235–1242). Jaya Publishing House.
Perfecto, I., & Vandermeer, J. (2008). Biodiversity conservation in tropical agroecosystems. Annals of the New York Academy of Sciences, 1134(1), 173–200. https://doi.org/10.1196/annals.1439.011
Pillay, R., Venter, M., Aragon‐Osejo, J., González‐del‐Pliego, P., Hansen, A. J., Watson, J. E., & Venter, O. (2022). Tropical forests are home to over half of the world’s vertebrate species. Frontiers in Ecology and the Environment, 20(1), 10–15. https://doi.org/10.1002/fee.2420
R Development Core Team. (2022). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. http://www.r-project.org
Ramírez-Fernández, J., Sánchez, R., May-Collado, L., González-Maya, J., & Rodríguez-Herrera, B. (2023). Revised checklist and conservation status of the mammals of Costa Rica. Therya, 14(2), 1–12.
Ripple, W. J., Abernethy, K., Betts, M. G., Chapron, G., Dirzo, R., Galetti, M., Levi, T., Lindsey, P. A., Macdonald, D. W., Machovina, B., Newsome, T. M., Peres, C. A., Wallach, A. D., Wolf, C., & Young, H. (2016). Bushmeat hunting and extinction risk to the world’s mammals. Royal Society Open Science, 3(10), 160498. https://doi.org/10.1098/rsos.160498
Salom-Pérez, R., Corrales-Gutiérrez, D., Araya-Gamboa, D., Espinoza-Muñoz, D., Finegan, B., & Petracca, L. S. (2021). Forest cover mediates large and medium-sized mammal occurrence in a critical link of the Mesoamerican Biological Corridor. PLOS ONE, 16(3), e0249072. https://doi.org/10.1371/journal.pone.0249072
Salom-Pérez, R., Wultsch, C., Adams, J. R., Soto-Fournier, S., Gutiérrez-Espeleta, G. A., & Waits, L. P. (2022). Genetic diversity and population structure for ocelots (Leopardus pardalis) in Costa Rica. Journal of Mammalogy, 103(1), 68–81. https://doi.org/10.1093/jmammal/gyab146
Sampaio, R., Lima, A. P., Magnusson, W. E., & Peres, C. A. (2010). Long-term persistence of midsized to large-bodied mammals in Amazonian landscapes under varying contexts of forest cover. Biodiversity and Conservation, 19(8), 2421–2439. https://doi.org/10.1007/s10531-010-9848-3
Sánchez-Brenes, R. J., & Monge, J. (2021). Períodos de actividad y dieta de Dasyprocta punctata (Gray, 1842) (Rodentia; Dasyproctidae) en agroecosistemas con café, San Ramón, Costa Rica. Acta Zoológica Mexicana, 37, 1–15. https://doi.org/10.21829/azm.2021.3712346
Silva-Forsberg, M. C. (2008). Restauração ecológica e proteção da biodiversidade no sistema de micro-bacias hidrográficas em Atenas, Alajuela, Costa Rica. Revista Amazônica de Ensino de Ciências, 1(1), 98–118.
Sistema Nacional de Áreas de Conservación. (2018). Plan Estratégico 2018-2025 del Programa Nacional de Corredores Biológicos de Costa Rica (Informe Final). Programa Nacional de Corredores Biológicos, Sistema Nacional de Áreas de Conservación, Costa Rica.
Sistema Nacional de Áreas de Conservación. (2022). Control de áreas silvestres protegidas por categoría de manejo, Julio 2002. Sistema Nacional de Áreas de Conservación, Costa Rica. https://www.sinac.go.cr/ES/asp/Paginas/default.aspx
Stan, K., & Sanchez-Azofeifa, A. (2019). Deforestation and secondary growth in Costa Rica along the path of development. Regional Environmental Change, 19(2), 587–597. https://doi.org/10.1007/s10113-018-1432-5
Stoner, K. E., & Timm, R. M. (2011). Seasonally dry tropical forest mammals: adaptations and seasonal patterns. In R. Dirzo, H. S. Young, H. A. Mooney, & G. Ceballos (Eds.), Seasonally Dry Tropical Forests (pp. 85–106). Island Press. https://doi.org/10.5822/978-1-61091-021-7_6
Tabarelli, M., Cardoso da Silva, J. M., & Gascon, C. (2004). Forest fragmentation, synergisms and the impoverishment of neotropical forests. Biodiversity and Conservation, 13(7), 1419–1425. https://doi.org/10.1023/B:BIOC.0000019398.36045.1b
Valenzuela, D., & Ceballos, G. (2000). Habitat selection, home range, and activity of the white-nosed coati (Nasua narica) in a Mexican tropical dry forest. Journal of Mammalogy, 81(3), 810–819.
Valenzuela, D., & Macdonald, D. W. (2002). Home‐range use by white‐nosed coatis (Nasua narica): Limited water and a test of the resource dispersion hypothesis. Journal of Zoology, 258(2), 247–256. https://doi.org/10.1017/S0952836902001358
Vetter, D., Hansbauer, M. M., Végvári, Z., & Storch, I. (2011). Predictors of forest fragmentation sensitivity in Neotropical vertebrates: A quantitative review. Ecography, 34(1), 1–8. https://doi.org/10.1111/j.1600-0587.2010.06453.x
Williams, D. R., Rondinini, C., & Tilman, D. (2022). Global protected areas seem insufficient to safeguard half of the world’s mammals from human-induced extinction. Proceedings of the National Academy of Sciences, 119(24), e2200118119. https://doi.org/10.1073/pnas.2200118119
Wright, S. J., Carrasco, C., Calderón, O., & Paton, S. (1999). The El Nino Southern Oscillation, variable fruit production, and famine in a tropical forest. Ecology, 80(5), 1632. https://doi.org/10.2307/176552
Comments
This work is licensed under a Creative Commons Attribution 4.0 International License.
Copyright (c) 2023 Revista de Biología Tropical