Abstract
Selective logging can have negative effects on biodiversity and on key ecological processes such as seed dispersal and forest regeneration. Yet, the effect that timber extraction has on animal behavior and habitat use is poorly known. We tested whether the density, distribution, and composition of sleeping sites used by spider monkeys (Ateles geoffroyi) differed between two logged and two unlogged forest sites in the Calakmul region, southeastern Mexico. We recorded a total of 74 sleeping sites (0.11 sleeping sites/ha). The density of sleeping sites did not differ between forest conditions. Most (97%) sleeping sites were located in medium-stature semievergreen forest, and only 3% in low-stature seasonally inundated forest. In three of four sites, the number of sleeping sites in core areas was significantly greater than expected by chance, showing an aggregated spatial distribution, particularly in areas containing a greater density of feeding trees. About half (51%) of the sleeping sites were composed of a single large tree (mean ± SD diameter at breast height, 42.2 ± 21.9 cm) from a small number of tree species, such as Lonchocarpus castelloi, Bucida buceras, and Lysiloma latisiliquum. These results suggest that the current level of timber extraction seems to have no effect on the density, distribution, and composition of sleeping sites. Nevertheless, because the species that were selected as sleeping trees are subject to timber extraction, the availability of sleeping sites is expected to decrease in coming decades, potentially modifying the habitat use of this primate species.
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References
Anderson, J. R. (1998). Sleep, sleeping sites, and sleep-related activities: Awakening to their significance. American Journal of Primatology, 46, 63–75.
Aquino, R., & Encarnación, F. (1986). Characteristics and use of sleeping sites in Aotus (Cebidae: Primates) in the Amazon Lowlands of Peru. American Journal of Primatology, 11, 319–331.
Ariyanti, N. S., Bos, M. M., Kartawinata, K., Tjitrosoedirdjo, S. S., Guhardja, E., & Gradstein, S. R. (2008). Bryophytes on tree trunks in natural forests, selectively logged forests and cacao agroforests in Central Sulawesi, Indonesia. Biological Conservation, 141, 2516–2527.
Arroyo-Rodríguez, V., Andresen, E., Bravo, S. P., & Stevenson, P. R. (2015). Seed dispersal by howler monkeys: Current knowledge, conservation implications, and future directions. In M. Kowalewski, P. A. Garber, L. Cortés-Ortiz, B. Urbani, & D. Youlatos (Eds.), Howler monkeys: Behavior, ecology and conservation (pp. 111–139). New York: Springer Science+Business Media.
Asensio, N., Lusseau, D., Schaffner, C. M., & Aureli, F. (2012a). Spider monkeys use high-quality core areas in a tropical dry forest. Journal of Zoology, 287, 250–258.
Asensio, N., Schaffner, C. M., & Aureli, F. (2012b). Variability in core areas of spider monkeys (Ateles geoffroyi) in a tropical dry forest in Costa Rica. Primates, 53, 147–156.
Asner, G. P., Knapp, D. E., Broadbent, E. N., Oliveira, P. J. C., Keller, M., & Silva, J. N. (2005). Selective logging in the Brazilian Amazon. Science, 310, 480–481.
Asner, G. P., Rudel, T. K., Aide, T. M., Defries, R., & Emerson, R. (2009). A contemporary assessment of change in humid tropical forests. Conservation Biology, 23, 1386–1395.
Aureli, F., & Schaffner, C. M. (2008). Social interactions, social relationships and the social system of spider monkeys. In C. J. Campbell (Ed.), Spider monkeys: Behavior, ecology and evolution of the genus Ateles (pp. 236–265). New York: Cambridge University Press.
Berry, N. J., Phillips, O. L., Lewis, S. L., Hill, J. K., Edwards, D. P., Tawatao, N. B., et al. (2010). The high value of logged tropical forests: Lessons from northern Borneo. Biodiversity and Conservation, 19, 985–997.
Beyer, H. L. (2004). Hawth’s analysis tools for ArcGIS. http://www.spatialecology.com/htools (Accessed September 15, 2014).
Bicknell, J. E., Struebig, M. J., & Davies, Z. G. (2015). Reconciling timber extraction with biodiversity conservation in tropical forests using reduced-impact logging. Journal of Applied Ecology, 52, 379–388.
Bolland, L. P., Dren, A. P., & Vergara-Tenorio, C. (2006). Analysis of a natural resources management system in the Calakmul Biosphere Reserve. Landscape and Urban Planning, 74, 223–241.
Bravo, S. P. (2012). The impact of seed dispersal by black and gold howler monkeys on forest regeneration. Ecological Research, 27, 311–321.
Brown, K. A., & Gurevitch, J. (2004). Long-term impacts of logging on forest diversity in Madagascar. Proceedings of the National Academy of Sciences of the USA, 101, 6045–6049.
Byers, C. R., Steinhorst, R. K., & Krausman, P. R. (1984). Clarification of a technique for analysis of utilization-availability data. Journal of Wildlife Management, 48, 1050–1053.
Chapman, C. A. (1987). Patch use and patch depletion by the spider and howling monkeys of Santa Rosa National Park, Costa Rica. Behaviour, 105, 99–116.
Chapman, C. A. (1989). Spider monkey sleeping sites: Use and availability. American Journal of Primatology, 18, 53–60.
Chapman, C. A., Balcom, S. R., Gillespie, T. R., Skorupa, J. P., & Struhsaker, T. T. (2000). Long-term effects of logging on African primate communities: A 28-year comparison from Kibale National Park, Uganda. Conservation Biology, 14, 207–217.
Chapman, C. A., Chapman, L. J., & McLaughlin, R. L. (1989). Multiple central place foraging by spider monkeys: Travel consequences of using many sleeping sites. Oecologia, 79, 506–511.
Chaves, O. M., Stoner, K. E., Arroyo-Rodríguez, V., & Estrada, A. (2011). Effectiveness of spider monkeys (Ateles geoffroyi vellerosus) as seed dispersers in continuous and fragmented rainforests in southern Mexico. International Journal of Primatology, 32, 177–192.
Connell, J. H. (1971). On the role of natural enemies in preventing competitive exclusion in some marine animals and in rainforest trees. In P. J. den Boer & D. R. Gradwell (Eds.), Dynamics of populations (pp. 298–313). Wageningen: Center for Agricultural Publishing and Documentation.
Cui, L. W., Quan, R. C., & Xiao, W. (2006). Sleeping sites of black-and-white snub-nosed monkeys (Rhinopithecus bieti) at Baima Snow Mountain, China. Journal of Zoology, 270, 192–198.
de Winter, J. C. F. (2013). Using the Student’s t-test with extremely small sample sizes. Practical Assessment, Research & Evaluation, 18. http://pareonline.net/getvn.asp?v=18&n=10.
Di Bitetti, M. S., Luengos Vidal, E. M., Baldovino, M. C., & Benesovsky, V. (2000). Sleeping site preferences in tufted capuchin monkeys (Cebus apella nigritus). American Journal of Primatology, 274, 257–274.
Di Fiore, A., Link, A., & Dew, J. L. (2008). Diets of wild spider monkeys. In C. J. Campbell (Ed.), Spider monkeys: Behavior, ecology and evolution of the genus Ateles (pp. 81–137). New York: Cambridge University Press.
Fredericksen, N. J., & Fredericksen, T. S. (2002). Terrestrial wildlife responses to logging and fire in a Bolivian tropical humid forest. Biodiversity and Conservation, 11, 27–38.
FSC (Forest Stewardship Council A.C.) (1996). FSC principles and criteria for forest stewardship. FSC-STD-01-001 (version 4-0) EN. https://ic.fsc.org/principles-and-criteria.34.htm (Accessed October 6, 2015).
García, G., Palacio-Prieto, J. L., & Ortíz-Pérez, M. A. (2002). Reconocimiento geomorfológico e hidrográfico de la Reserva de la Biosfera de Calakmul, México. Investigaciones Geográficas, 48, 7–23.
González-Zamora, A., Arroyo-Rodríguez, V., Chaves, O. M., Sánchez-López, S., Stoner, K. E., & Riba-Hernández, P. (2009). Diet of spider monkeys (Ateles geoffroyi) in Mesoamerica: Current knowledge and future directions. American Journal of Primatology, 71, 8–20.
González-Zamora, A., Arroyo-Rodríguez, V., Escobar, F., Oyama, K., Aureli, F., & Stoner, K. E. (2015). Sleeping tree fidelity of the spider monkeys shapes community-level seed rain patterns in continuous and fragmented rain forests. Journal of Tropical Ecology, 31, 305–313.
González-Zamora, A., Arroyo-Rodríguez, V., Escobar, F., Rös, M., Oyama, K., Ibarra-Manríquez, G., et al. (2014). Contagious deposition of seeds in spider monkeys sleeping trees limits effective seed dispersal in fragmented landscapes. PLoS ONE, 9, e89346.
González-Zamora, A., Arroyo-Rodríguez, V., Oyama, K., Sork, V., Chapman, C. A., & Stoner, K. E. (2012). Sleeping sites and latrines of spider monkeys in continuous and fragmented rainforests: implications for seed dispersal and forest regeneration. PLoS ONE, 7, e46852.
Gutiérrez-Granados, G., & Dirzo, R. (2010). Indirect effects of timber extraction on plant recruitment and diversity via reductions in abundance of frugivorous spider monkeys. Journal of Tropical Ecology, 26, 45–52.
Heydon, M. J., & Bulloh, P. (1997). Mousedeer densities in a tropical rainforest: The impact of selective logging. Journal of Applied Ecology, 34, 484–496.
Heymann, E. W. (1995). Sleeping habits of tamarins, Saguinus mystax and Saguinus fuscicollis (Mammalia: Primates: Callitrichidae), in north-eastern Peru. Journal of Zoology, 237, 211–226.
Janzen, D. H. (1970). Herbivores and the number of tree species in tropical forests. American Naturalist, 104, 501–528.
Johns, A. D. (1992). Effects of “selective” timber extraction on rain forest structure and composition and some consequences for frugivores and folivores. Biotropica, 20, 31–37.
Kernohan, B. J., Gitzen, R. A., & Millspaugh, J. J. (2001). Analysis of animal space use and movement. In J. J. Millspaugh & J. M. Marzluff (Eds.), Radio tracking and animal populations (pp. 125–166). San Diego: Academic Press.
Malhi, Y., Gardner, T. A., Goldsmith, G. R., Silman, M. R., & Zelazowski, P. (2014). Tropical forests in the Anthropocene. Annual Review of Environmental Resources, 39, 125–159.
Manly, B. F., McDonald, L. L., Thomas, D. L., McDonald, T. L., & Erickson, W. P. (2002). Resource selection by animals: Statistical design and analysis for field studies. Norwell: Kluwer Academic.
Mendes-Pontes, A. R., & Lira, S. M. (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.
Milton, K. (1980). The foraging strategy of howler monkeys. New York: Columbia University Press.
Mitchell, A. (2005). The ESRI guide to GIS analysis, Vol. 2: Spatial Measurements and Statistics. Redlands: ESRI Press.
Nunes, A. (1995). Foraging and ranging patterns in white-bellied spider monkeys. Folia Primatologica, 65, 85–99.
Plumptre, A. J., & Reynolds, V. (1994). The effect of selective logging on the primate populations in the budongo Forest Reserve, Uganda. Journal of Applied Ecology, 31, 631–641.
Pozo, W. E. (2005). Caracterización de los dormideros usados por Ateles belzebuth en el parque Nacional Yasuní, Ecuador. Neotropical Primates, 13, 27–34.
Putz, F. E., Blate, G. M., Redford, K. H., Fimbel, R., & Robinson, J. (2001). Tropical forest management and conservation of biodiversity: An overview. Conservation Biology, 15, 7–20.
Ramos-Fernández, G., Smith-Aguilar, S. E., Schaffner, C. M., Vick, L. G., & Aureli, F. (2013). Site fidelity in space use by spider monkeys (Ateles geoffroyi) in the Yucatan Peninsula, Mexico. PLoS ONE, 8, e62813.
Ramos-Fernández, G., & Wallace, R. B. (2008). Spider monkey conservation in the twenty-first century: Recognizing risks and opportunities. In J. C. Campbell (Ed.), Spider monkeys. The biology, behavior and ecology of the genus Ateles (pp. 351–372). New York: Cambridge University Press.
Reichard, U. (1998). Sleeping sites, sleeping places, and presleep behavior of gibbons (Hylobates lar). American Journal of Primatology, 62, 35–62.
Reyna-Hurtado, R., Rojas-Flores, E., & Tanner, G. W. (2009). Home range and habitat preferences of white-lipped peccary groups (Tayassu pecari) in a seasonal tropical forest of the Yucatan Peninsula, Mexico. Journal of Mammalogy, 90, 1199–1209.
Russo, S. E., & Augspurger, C. K. (2004). Aggregated seed dispersal by spider monkeys limits recruitment to clumped patterns in Virola calophylla. Ecology Letters, 7, 1058–1067.
Russo, S. E., & Chapman, C. A. (2011). Primate seed dispersal: Linking behavioral ecology with forest community structure. In C. J. Campbell, A. F. Fuentes, K. C. MacKinnon, M. Panger, & S. Bearders (Eds.), Primates in perspective (pp. 523–534). Oxford: Oxford University Press.
Russo, S. E., Portnoy, S., & Augspurger, C. K. (2006). Incorporating animal behavior into seed dispersal models: Implications for seed shadows. Ecology, 87, 3160–3174.
Smith, A. C., Knogge, C., Huck, M., Löttker, P., Buchanan-Smith, H. M., & Heymann, E. W. (2007). Long-term patterns of sleeping site use in wild saddleback (Saguinus fuscicollis) and mustached tamarins (S. mystax): Effects of foraging, thermoregulation, predation, and resource defense constraints. American Journal of Physical Anthropology, 134, 340–353.
Snook, L. K. (2003). Regeneration, growth, and sustainability of mahogany in Mexico's Yucatán forests. In A. E. Lugo, J. C. Figueroa Colón, & M. Alayón (Eds.), Big-leaf mahogany: Genetics, ecology, and management (pp. 169–192). New York: Springer.
Teichroeb, J. A., Holmes, J. A., & Sicotte, P. (2012). Use of sleeping trees by ursine colobus monkeys (Colobus vellerosus) demonstrates the importance of nearby food. Primates, 53, 287–296.
Vester, H. F. M., Lawrence, D., Eastman, J. R., Turner, B. L., II, Calmé, S., Pozo, C., et al. (2007). Land change in the southern Yucatan and Calakmul Biosphere Reserve: Effects on habitat and biodiversity. Ecological Applications, 17, 989–1003.
Weisstein, E. W. (2005). Moore neighborhood. MathWorld-A Wolfram Web Resource. http://mathworld.wolfram.com/MooreNeighborhood.html (Accessed September 15, 2015).
Youlatos, D. (2002). Positional behavior of black spider monkeys (Ateles paniscus) in French Guiana. International Journal of Primatology, 23, 1071–1093.
Acknowledgments
We thank Joanna M. Setchell and two anonymous reviewers for their insightful comments on an earlier version of the manuscript, and F. J. W. Parsons for his linguistic revision. A special thank you is extended to those who helped with field work, including J. Taylor, R. Escalante, N. Arias, G. Domínguez, H. Marshall, M. Lafrenière, C. Martineau, F. Beaulieu, L. Gaillard, M. Chénier, and S. Côté-Bourgoin. We thank the authorities of the Nuevo Becal ejido for allowing us to carry out this study. G. Velázquez-Vázquez obtained an MSc scholarship from the Consejo Nacional de Ciencia y Tecnología, CONACYT and an internship from the Ecology Department of the University of Sherbrooke. ECOSUR and the University of Sherbrooke provided the funding required for the field work.
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Velázquez-Vázquez, G., Reyna-Hurtado, R., Arroyo-Rodríguez, V. et al. Sleeping Sites of Spider Monkeys (Ateles geoffroyi) in Logged and Unlogged Tropical Forests. Int J Primatol 36, 1154–1171 (2015). https://doi.org/10.1007/s10764-015-9883-8
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DOI: https://doi.org/10.1007/s10764-015-9883-8