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Sleeping Sites of Spider Monkeys (Ateles geoffroyi) in Logged and Unlogged Tropical Forests

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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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Bravo, S. P. (2012). The impact of seed dispersal by black and gold howler monkeys on forest regeneration. Ecological Research, 27, 311–321.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Chapman, C. A. (1989). Spider monkey sleeping sites: Use and availability. American Journal of Primatology, 18, 53–60.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Heydon, M. J., & Bulloh, P. (1997). Mousedeer densities in a tropical rainforest: The impact of selective logging. Journal of Applied Ecology, 34, 484–496.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Janzen, D. H. (1970). Herbivores and the number of tree species in tropical forests. American Naturalist, 104, 501–528.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • Milton, K. (1980). The foraging strategy of howler monkeys. New York: Columbia University Press.

    Google Scholar 

  • Mitchell, A. (2005). The ESRI guide to GIS analysis, Vol. 2: Spatial Measurements and Statistics. Redlands: ESRI Press.

    Google Scholar 

  • Nunes, A. (1995). Foraging and ranging patterns in white-bellied spider monkeys. Folia Primatologica, 65, 85–99.

    CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Pozo, W. E. (2005). Caracterización de los dormideros usados por Ateles belzebuth en el parque Nacional Yasuní, Ecuador. Neotropical Primates, 13, 27–34.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • Reichard, U. (1998). Sleeping sites, sleeping places, and presleep behavior of gibbons (Hylobates lar). American Journal of Primatology, 62, 35–62.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • Russo, S. E., Portnoy, S., & Augspurger, C. K. (2006). Incorporating animal behavior into seed dispersal models: Implications for seed shadows. Ecology, 87, 3160–3174.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

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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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Correspondence to Guadalupe Velázquez-Vázquez.

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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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