Habitat use and activity patterns of ungulates in a tropical rainforest of southern México
Keywords:
Coexistence, habitat use, Maya Forest, resource partitioning, ungulates.Abstract
Baird’s tapir (Tapirella bairdii), white-lipped peccary (Tayassu pecari), and collared peccary (Dicotyles tajacu) sympatrically occur in the Lacandon Forest of Chiapas, México. These species contribute to maintain ecosystem dynamics through herbivory, seed dispersal, and seed predation, constituting important prey for large carnivores and hunters. We analyzed activity patterns and habitat use of the three focal species to assess the degree of temporal and spatial habitat segregation among them in Montes Azules Biosphere Reserve (REBIMA) and surrounding communities. Between February and October 2015 we deployed camera-traps during 8,463 camera-trap days to estimate the presence and activity of tapirs and peccaries in two habitat types: “conserved†(REBIMA), and “transformed†(community forests; AFC). Habitat use and activity patterns of tapirs and peccaries were assessed through logistic regression models. We found that Baird’s tapir was almost exclusively nocturnal with a trend towards crepuscular activity, while both peccary species were diurnal, therefore showing a high daily temporal segregation from the tapir. Both peccary species were similarly active in the two study sites, while tapirs were more active in continuous forest within the protected area. The occurrence of tapirs and white-lipped peccaries depended on the presence and proximity of water sources and roads. Our results suggest that spatial segregation of the habitat allows coexistence of both peccary species in the study area. AFC have potential for maintaining populations of tapirs and peccaries in the Lacandon Forest. Conserving these forests by local communities is essential to ensure the persistence of these mammals.References
ALTRICHTER, M., ET AL. 2012. Range-wide declines of a key Neotropical ecosystem architect, the Near Threatened White-lipped peccary Tayassu pecari. Oryx 46:87–98.
ARCE-PEÑA, N. P., ET AL. 2019. Landscape predictors of rodent dynamics in fragmented rainforests. Biodiversity and Conservation 28:655–669.
ARROYO-ARCE, S., I. THOMSON, C. FERNÁNDEZ, AND R. SALOM-PÉREZ. 2017. Relative abundance and activity patterns of terrestrial mammals in Pacuare Nature Reserve, Costa Rica. Cuadernos de Investigación UNED 9:15–21.
BARTON, K. 2019. MuMIn: Multi-Model Inference. https://CRAN.R-project.org/package = MuMIn. Downloaded on July 20, 2021.
BODMER, R. E. 1991. Strategies of seed dispersal and seed predation in Amazonian ungulates. Biotropica 23:255–261.
BRICEÑO-MÉNDEZ, M., ET AL. 2016. Responses of two sympatric species of peccaries (Tayassu pecari and Pecari tajacu) to hunting in Calakmul, Mexico. Tropical Conservation Science 9:1–11.
BURNHAM, K. P., AND D. R. ANDERSON. 2004. Model Selection and Multimodel Inference: A Practical Information-theoretic Approach. 2nd ed. Springer-Verlag. New York, U.S.A.
CALCAGNO, V. 2019. Glmulti: Model Selection and Multimodel Inference Made Easy. R package version 1.0.7.1. https://CRAN.R-project.org/package=glmulti . Downloaded on July 20, 2021.
CAMINO, M., S. CORTEZ, S. D. MATTEUCCI, AND M. ALTRICHTER. 2017. Experiencia de monitoreo participativo de fauna en el Chaco seco argentino. Maztozoología Neotropical 24:31–46.
CARABIAS, J. J. DE LA MAZA, AND R. CADENA (EDS.). 2015. Conservación y Desarrollo Sustentable en la Selva Lacandona: 25 Años de Actividades y Experiencias. Natura y Ecosistemas Mexicanos. Ciudad de México, México.
CARRARA, E., ET AL. 2015. Impact of landscape composition and configuration on forest specialist and generalist bird species in the fragmented Lacandona rainforest, Mexico. Biological Conservation 184:117–126.
CARREIRA, D. C., ET AL. 2020. A question of size and fear: Competition and predation risk perception among frugivores and predators. Journal of Mammalogy 101:648–657.
CARRILLO-REYNA. N., R. REYNA-HURTADO, AND B. SCHMOOK. 2015. Abundancia relativa y selección de hábitat de Tapirus bairdii en las reservas de Calakmul y Balam kú, Campeche, México. Revista Mexicana de Biodiversidad 86:202–207.
CARTES, J. L., J. THOMPSON, AND A. YANOSKY. 2015. El Chaco paraguayo como uno de los últimos refugios para los mamíferos amenazados del Cono Sur. Paraquaria Natural 3:37–47.
CHALLENGER, A., AND J. SOBERÓN. 2008. Los ecosistemas terrestres. Pp. 87–108 in Capital Natural de México (CONABIO, ed.). Vol. I: Conocimiento Actual de la Biodiversidad. Cmisión Nacional para el Conocimiento y Uso de la Biodiversidad. Ciudad de México, México.
CHÁVEZ, C., ET AL. (EDS.). 2013. Manual de Fototrampeo para Estudio de Fauna Silvestre: El Jaguar en México como Estudio de Caso. Alianza WWF-Telcel, Universidad Nacional Autónoma de México. Ciudad de México, México.
DE LA TORRE, J. A., AND R. A. MEDELLÍN. 2011. Jaguars Panthera onca in the greater Lacandona ecosystem, Chiapas, Mexico: Population estimates and future prospects. Oryx 45:546–553.
DE LA TORRE, J. A., AND M. RIVERO. 2019. Insights on the movements of the jaguar in the tropical forests of southern Mexico. Pp. 217–241 in Movement Ecology of Neotropical Forest Mammals (Reyna-Hurtado, R., and C. A. Chapman, eds.). Springer. Gewerbestasse, Switzerland.
DELLINGER, J. A., ET AL. 2020. Using Mountain lion habitat selection in management. The Journal of Wildlife Management 84:359–371.
DIRZO, R., ET AL. 2014. Defaunation in the Anthropocene. Science 345:401–406.
EISENBERG, J. F. 1989. Mammals of the Neotropics. Vol 1: The Northern Neotropics. University of Chicago Press. Chicago, U.S.A.
ESPINOSA, S., AND J. SALVADOR. 2017. Hunters’ landscape accessibility and daily activity of ungulates in Yasuní Biosphere Reserve, Ecuador. Therya 8:45–52.
FLETCHER, R., AND M. J FORTIN. 2018. Spatial ecology and conservation modeling. Springer International Publishing. Gewerbestasse, Switzerland.
FOERSTER, C. R., AND C. VAUGHAN. 2002. Home range, habitat use and activity of Baird’s tapir in Costa Rica. Biotropica 34:423–437
FREY, S., J. T. FISHER, A. C. BURTON, AND J. P. VOLPE. 2017. Investigating animal activity patterns and temporal niche partitioning using camera-trap data: Challenges and opportunities. Remote Sensing in Ecology and Conservation 3:123–132.
FRYXELL, J. M., A. R. E. SINCLAIR, AND G. CAUGHLEY. 2014. Wildlife Ecology, Conservation, and Management. 3rd ed. Wiley-Blackwell, Oxford, United Kingdom.
GAILLARD, J., ET AL. 2010. Habitat – performance relationships: Finding the right metric at a given spatial scale. Philosophical Transactions of the Royal Society of London 365:2255–2265.
GALETTI, M., R. S. BOVENDORP, AND R. GUEVARA. 2015. Defaunation of large mammals leads to an increase in seed predation in the Atlantic forests. Global Ecology and Conservation 3:824–830.
GALETTI, M., V. B. ZIPPARRO, AND L. P. C. MORELLATO. 1999. Fruiting phenology and frugivory on the palm Euterpe edulis in a lowland Atlantic forest of Brazil. Ecotropica 5:115–122.
GARCíA, E. 2004. Modificaciones al Sistema de Clasificación ClimaÌtica de Köppen. Serie Libros Núm 6. Instituto de Geografía, Universidad Nacional Autónoma de México. Ciudad de México, México.
GARCÍA, M., ET AL. 2016. Tapirus bairdii. In: IUCN 2016. The IUCN Red List of Threatened Species. https://www.iucnredlist.org. Downloaded on April 5, 2021.
GARCIA-ALANIZ, N., E. J. NARANJO, AND F. F. MALLORY. 2010. Human-felid interactions in three mestizo communities of the Selva Lacandona, Chiapas, Mexico: Benefits, conflicts and traditional uses of species. Human Ecology 38:451–457.
GARCÍA-GIL, J.G., AND J. LUGO-HUPB. 1992. Las formas de relieve y los tipos de vegetación en la Selva Lacandona. Pp. 39–49 in Reserva de la Biósfera Montes Azules, Selva Lacandona: Investigación para su Conservación (Vásquez-Sánchez, M. A., and M. A. Ramos-Olmos, eds.). Centro de Estudios para la Conservación de los Recursos Naturales, A. C. Publicaciones Especiales de Ecosfera 1. San Cristóbal de Las Casas, México.
GARMENDIA, A., ET AL. 2013. Landscape and patch attributes impacting medium- and large-sized terrestrial mammals in a fragmented rain forest. Journal of Tropical Ecology 29:331–344.
GARRIDO-GARDUÑO, T., AND E. VÁZQUEZ-DOMÍNGUEZ. 2013. Métodos de análisis genéticos, espaciales y de conectividad en genética del paisaje. Revista Mexicana de Biodiversidad 84:1031–1054.
GAUSE, G. F. (ED.). 1934. The Struggle for Existence in Natural Conditions. Williams and Wilkins. Baltimore, U.S.A.
GIL–FERNÁNDEZ, M., ET AL. 2017. Wild felid species richness affected by a corridor in the Lacandona forest, Mexico. Animal Biodiversity and Conservation 40:115–120.
HUBBELL, S. P. 2001. The Unified Neutral Theory of Biodiversity and Biogeography. Princeton University Press. New Jersey, U.S.A.
JACOMO, A. T. A., ET AL. 2013. White-lipped peccary home-range size in a protected area and farmland in the central Brazilian grasslands. Journal of Mammalogy 94:137–145.
JOHNSON, D. H. 1980. The comparison of usage and availability measurements for evaluating resources preference. Ecology 61:65–71.
KÉRY, M., AND J. A. ROYLE. 2016. Applied Hierarchical Modelling in Ecology: Analysis of Distribution, Abundance and Species Richness in R and BUGS. Vol. 1: Prelude and static models. Academic Press. London, United Kingdom.
KEUROGHLIAN, A., ET AL. 2013. Tayassu pecari. In: The IUCN Red List of Threatened Species 2013. https://www.iucnredlist.org. Downloaded on April 5, 2021.
KEUROGHLIAN, A., D. P. EATON, AND W. S. LONGLAND. 2004. Area use by White-lipped and Collared peccaries (Tayassu pecari and Tayassu tajacu) in a tropical forest fragment. Biological Conservation 120:411–425.
KILTIE, R. A. 1982. Bite force as a basis for niche differentiation between rain forest peccaries (Tayassu tajacu and T. pecari). Biotropica 14:188–195.
KRAUSMAN, P. R., AND M. L. MORRISON. 2016. Another plea for standard terminology. The Journal of Wildlife Management 80:1143–1144.
KRONFELD-SCHOR, N., AND T. DAYAN. 2003. Partitioning of time as an ecological resource. Annual Review of Ecology, Evolution, and Systematics 34:153–181.
LELE, S. R., E. H. MERRILL, J. KEIM, AND M. S. BOYCE. 2013. Selection, use, choice and occupancy: clarifying concepts in resource selection studies. Journal of Animal Ecology 82:1183–1191.
LIMA, M., ET AL. 2019. The paradoxical situation of the White-lipped peccary (Tayassu pecari) in the state of Mato Grosso, Brazil. Perspectives in Ecology and Conservation 17:36–39.
LIRA-TORRES, I., M. BRIONES-SALAS, AND G. SÁNCHEZ-ROJAS. 2014. Abundancia relativa, estructura poblacional, preferencia de hábitat y patrones de actividad del tapir centroamericano Tapirus bairdii (Perissodactyla: Tapiridae), en la selva de Los Chimalapas, Oaxaca, México. Revista de Biología Tropical 62:1407–1419.
LIU, X., ET AL. 2017. Diversity and activity patterns of sympatric animals among four types of forest habitat in Guanyinshan Nature Reserve in the Qinling Mountains, China. Environmental Science and Pollution Research 24:16465–16477.
LIZCANO, D. L., AND J. CAVELIER. 2000. Daily and seasonal activity of the mountain tapir (Tapirus pinchaque) in the Central Andes of Colombia. Journal of Zoology 252:429–435.
LONE, K., ET AL. 2017. Temporal variation in habitat selection breaks the catch-22 of spatially contrasting predation risk from multiple predators. Oikos 126:624–632.
LÃœDECKE, D. 2018. SjPlot: Data Visualization for Statistics in Social Science. R package version 2(1). https://cran.r-project.org/web/packages/sjPlot/index.html. Downloaded on October 12, 2019.
MACKENZIE, D. L., AND J. A. ROYLE. 2005. Designing occupancy studies: general advice and allocating survey effort. Journal of Applied Ecology 42:1105–1114.
MALHI, Y., ET AL. 2016. Megafauna and ecosystem function from the Pleistocene to the Anthropocene. Proceedings of the National Academy of Sciences 113:838–846.
MANDUJANO, S., AND R. REYNA-HURTADO. 2019. Recent studies of peccaries in the Neotropics. Pp. 415–438 in Ecology and Conservation of Tropical Ungulates in Latin America (Gallina, S. ed.). Springer. Cham, Switzerland.
MANLY, B. F., ET AL. 2002. Resource Selection by Animals. Springer. The Netherlands.
MARCH, I.J., AND E.J. NARANJO. 2005. Tapir (Tapirus bairdii). Pp. 496–497, in Los Mamíferos Silvestres de México (Ceballos, G., and G. Oliva. eds.). CONABIO and Fondo de Cultura Económica. Ciudad de México, México.
MATOLA, S., A. D. CUARÓN, AND H. RUBIO-TORGLER. 1997. Conservation status and action plan of Baird’s tapir (Tapirus bairdii). Pp. 29–45, in Tapirs: Status Survey and Conservation Action Plan (Brooks, D., R. Bodmer, and S. Matola, eds.). Gland, Switzerland and Cambridge, United Kingdom.
MAYER, J. J., AND R. M. WETZEL. 1987. Tayassu pecari. Mammalian Species 293:1–7.
MENDES-PONTES, A. R., AND D. J. CHIVERS. 2007. Peccary movements as determinants of the movements of large cats in Brazilian Amazonia. Journal of Zoology 273:257–265.
MEREDITH, M., AND M. RIDOUT. 2017. Overlap: Estimates of Coefficient of Overlapping for Animal Activity Patterns. R package version 0.3.0. Downloaded on October 12, 2019.
MEYER, N. F., ET AL. 2019. Effectiveness of Panama as an intercontinental land bridge for large mammals. Conservation Biology 34:207–219.
MOREIRA-RAMÍREZ, J., ET AL. 2019. Estado de conservación de dos ungulados sociales en Guatemala: Pecarí de labios blancos y pecarí de collar. Pp. 75–96, in Perspectivas de Investigación sobre los Mamíferos Silvestres de Guatemala (Kraker-Castañeda, C., A., P. Calderón, y A. A. Cabrera, eds.). Asociación Guatemalteca de Mastozoólogos. Ciudad de Guatemala, Guatemala.
MORRISON, M. L, B. G. MARCOT, AND R. W. MANNAN. 2006. Wildlife-habitat relationships: concepts and applications. Island Press. Washington D. C., U.S.A.
MUENCH, C., AND M. M. RAMOS. 2016. Can community protected areas conserve biodiversity in human modified tropical landscapes? The case of terrestrial mammals in southern Mexico. Tropical Conservation Science 9:178–202.
NARANJO, E. J. 2002. Population Ecology and Conservation of Ungulates in the Lacandon Forest, Mexico. PhD Dissertation. University of Florida. Gainesville, U.S.A.
NARANJO, E. J. 2008. Uso y conservación de mamíferos en la Selva Lacandona, Chiapas, México. Pp. 675–691 in Avances en el Estudio de los Mamíferos de México II (Lorenzo, C., E. Espinoza, y J. Ortega, eds.). Publicaciones Especiales Volumen II. Asociación Mexicana de Mastozoología, A. C. Ciudad de México, México.
NARANJO, E. J. 2009. Ecology and conservation of Baird’s tapir in Mexico. Tropical Conservation Science 2:140–158.
NARANJO, E. J. 2018. Baird’s tapir ecology and conservation in Mexico revisited. Tropical Conservation Science 11:1–4.
NARANJO, E. J. 2019. Ecology and conservation of ungulates in the Lacandon Forest, Mexico. Pp. 105–115 in Ecology and Conservation of Tropical Ungulates in Latin America (Gallina-Tessaro S, ed.). Springer. Cham, Switzerland.
NARANJO, E. J, S. A. AMADOR, F. A. FALCONI, AND R. A. REYNA. 2015. Distribución, abundancia y amenazas a las poblaciones de tapir centroamericano (Tapirus bairdii) y pecarí de labios blancos (Tayassu pecari) en México. Therya 6:227–249.
NARANJO, E. J., J. LÓPEZ-ACOSTA, AND R. DIRZO. 2010. La cacería en México. Biodiversitas 91:6–10.
NARANJO, E. J., AND E. CRUZ. 1998. Ecología del tapir en la Reserva de la Biósfera La Sepultura. Acta Zoológica Mexicana 73:111–125.
NARANJO, E. J., AND R. E. BODMER. 2007. Source-sink systems of hunted ungulates in the Lacandon Forest, Mexico. Biological Conservation 138:412-420.
O’ FARRILL, G., ET AL. 2014. The potential connectivity of waterhole networks and the effectiveness of a protected area under various drought scenarios. PloS One 9:1–10.
OLIVEIRA-SANTOS, L. G. R., ET AL. 2010. Influence of extrinsic variables on activity and habitat selection of lowland tapirs (Tapirus terrestris) in the coastal sand plain shrub, southern Brazil. Mammalian Biology 75:219–226.
PENNINGTON, T. D., AND J. SARUKHÁN. 2005. Árboles Tropicales de México: Manual para la Identificación de las Principales Especies. 3rd ed. Universidad Nacional Autónoma de México and Fondo de Cultura Económica. Ciudad de México, México.
PIANKA, E. 1983. Evolutionary Ecology. Omega. Barcelona, Spain.
PERES, C. A. 1994. Composition, density, and fruiting phenology of arborescent palms in an Amazonian terra firme forest. Biotropica 26:285–294.
R CORE TEAM. 2019. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. Vienna, Austria. www.R-project.org. Downloaded on October 25, 2019.
REDFORD, K. H., AND J. F. EISENBERG. 1992. Mammals of the Neotropics. Vol. II: The Southern Cone. University of Chicago Press. Chicago, U.S.A.
REYNA-HURTADO, R., E. ROJAS-FLORES, AND G. W. TANNER. 2009. Home range and habitat preferences of White-lipped peccaries (Tayassu pecari) in Calakmul, Campeche, Mexico. Journal of Mammalogy 90:1199–1209.
REYNA-HURTADO, R., I. MARCH, E. NARANJO, AND S. MANDUJANO. 2014. Pecaríes en México. Pp. 377–387 in Ecología y Manejo de Fauna Silvestre en México (Valdez, R., and J. A. Ortega, eds.). Colegio de Postgraduados and New Mexico State University. Texcoco, México.
REYNA-HURTADO, R., AND G. W. TANNER. 2005. Habitat preferences of ungulates in hunted and non-hunted areas in the Calakmul Forest, Campeche, Mexico. Biotropica 37:676–685.
REYNA-HURTADO, R., AND G. W. TANNER. 2007. Ungulate relative abundance in hunted and non-hunted sites in Calakmul Forest (southern Mexico). Biodiversity and Conservation 16:743–756.
ROBINSON, K. F., ET AL. 2016. Structured decision-making as a framework for largeâ€scale wildlife harvest management decisions. Ecosphere 7:12.
ROMERO-BALDERAS, K. G., E. J. NARANJO, H. H. MORALES, AND R. B. NIGH. 2006. Daños ocasionados por vertebrados silvestres al cultivo de maíz en la Selva Lacandona, Chiapas, México. Interciencia 31:276–283.
RZEDOWSKI, J. 1978. Vegetación de México. Limusa. Ciudad de México, México.
SÁNCHEZ-PINZÓN, K., R. REYNA-HURTADO, AND N. F. V. MEYER. 2020. Moon light and the activity patterns of Baird’s tapir in the Calakmul region, Southern Mexico. Therya 11:137–142.
SANDERSON, J. G., AND M. TROLLE. 2005. Monitoring elusive mammals: unattended cameras reveal secrets of some of the world’s wildest places. American Scientist 93:148–155.
SCHAEFER, H. C., W. JETZ, AND K. BÖHNING-GAESE. 2008. Impact of climate change on migratory birds: community reassembly versus adaptation. Global Ecology and Biogeography 17:38–49.
SCHOENER, T. W. 1974. Resource partitioning in ecological communities. Science 185:27–39.
SCHANK, C. J., ET AL. 2017. Using a novel model approach to assess the distribution and conservation status of the endangered Baird’s tapir. Diversity and Distributions 23:1459–1471.
SECRETARÍA DE MEDIO AMBIENTE Y RECURSOS NATURALES (SEMARNAT). 2010. Norma Oficial Mexicana NOM-059-ECOL-2010. Protección ambiental, especies de flora y fauna silvestres de México, categorías de riesgo y especificaciones para su inclusión, exclusión o cambio, y lista de especies en riesgo. Diario Oficial de la Federación. 30 de Diciembre 2010.
SILVAâ€RODRÍGUEZ, E. A., G. R. ORTEGAâ€SOLÍS, AND J. E. JIMÉNEZ. 2010. Conservation and ecological implications of the use of space by chilla foxes and freeâ€ranging dogs in a humanâ€dominated landscape in southern Chile. Austral Ecology 35:765–777.
SILVER, S. 2004. Assessing Jaguar Abundance using Remotely Triggered Cameras. Jaguar Conservation Program, Wildlife Conservation Society. New York, U.S.A.
SOKAL, R. R., AND F. J. ROHLF. 1995. Biometry: The Principles and Practice of Statistics in Biological Research. 3rd ed. WH Freeman. New York, U.S.A.
SOWLS, L. K. 1997. Javelinas and Other Peccaries: Their Biology, Management, and Use. Texas A&M University Press. College Station, U.S.A.
TEJEDA-CRUZ, C., ET AL. 2009. Habitat use of wild ungulates in fragmented landscapes of the Lacandon Forest, southern Mexico. Mammalia 73:211–219.
TERBORGH, J. 1986. Community aspects of frugivory in tropical forest. Pp. 371–384, in Frugivores and Seed Dispersal (Estrada, A., and T. H. Fleming, eds.). W. Junk. Dordrecht, The Netherlands.
THORNTON, D., ET AL. 2020. Precipitous decline of White-lipped peccary populations in Mesoamerica. Biological Conservation 242:1–12.
TOBLER, M. W., ET AL. 2008. An evaluation of camera traps for inventorying large- and medium-sized terrestrial rainforest mammals. Animal Conservation 11:169–178.
VANAK, A. T., AND M. E. GOMPPER. 2009. Dogs Canis familiaris as carnivores: their role and function in intraguild competition. Mammal Review 39:265–283.
WICKHAM, H. 2017. Tidyverse: Easily Install and Load. https://CRAN.R-project.org/package=tidyverse. Downloaded on November 12, 2017.
ZAPATA-RÍOS, G., AND L. C. BRANCH. 2016. Altered activity patterns and reduced abundance of native mammals in sites with feral dogs in the high Andes. Biological Conservation 193:9–16.
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