Hostname: page-component-848d4c4894-hfldf Total loading time: 0 Render date: 2024-06-11T23:12:12.140Z Has data issue: false hasContentIssue false

Sleeping-tree fidelity of the spider monkey shapes community-level seed-rain patterns in continuous and fragmented rain forests

Published online by Cambridge University Press:  08 June 2015

Arturo González-Zamora*
Affiliation:
División de Posgrado, Instituto de Ecología A.C., Xalapa, Veracruz, Mexico
Víctor Arroyo-Rodríguez
Affiliation:
Instituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad Nacional Autónoma de México, Morelia, Michoacán, Mexico
Federico Escobar
Affiliation:
Red de Ecoetología, Instituto de Ecología A.C., Xalapa, Veracruz, Mexico
Ken Oyama
Affiliation:
Instituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad Nacional Autónoma de México, Morelia, Michoacán, Mexico Escuela Nacional de Estudios Superiores, Universidad Nacional Autónoma de México, Morelia, Michoacán, Mexico
Filippo Aureli
Affiliation:
Instituto de Neuroetología, Universidad Veracruzana, Xalapa, Mexico, and Research Centre in Evolutionary Anthropology and Palaeoecology, Liverpool John Moores University, Liverpool, UK
Kathryn E. Stoner
Affiliation:
Department of Fish, Wildlife, and Conservation Ecology, New Mexico State University, Las Cruces, New Mexico, USA
*
1Corresponding author. Email: toztlan@yahoo.com.mx

Abstract:

Repeated use of sleeping trees (STs) by frugivores promotes the deposition and aggregation of copious amounts of seed, thus having key implications for seed dispersal and forest regeneration. Seed-rain patterns produced by this behaviour likely depend on the frequency of use of these sites, yet this hypothesis has been poorly tested. We evaluated community-level seed-rain patterns produced by the spider monkey (Ateles geoffroyi) over 13 mo in latrines located beneath 60 STs in the Lacandona rain forest, Mexico. Because this primate is increasingly ‘forced’ to inhabit fragmented landscapes, we tested whether sleeping-tree fidelity (STF) differed among sites and between continuous and fragmented forests. We also tested whether seed-rain patterns were associated with STF within each site and forest type. STF was highly variable among STs (average = 7 mo, range = 1–12 mo), but did not differ among study sites or forest types. STF was positively associated with seed abundance, species diversity and species turnover. Nevertheless, STF tended to be negatively related to seed community evenness. These results are likely due to the most frequently used STs being in areas with greater food density. Our results demonstrate that site fidelity shapes community-level seed-rain patterns and thus has key ecological implications.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

LITERATURE CITED

ANDERSON, J. R. 1984. Ethology and ecology of sleep in monkeys and apes. Advances in the Study of Behavior 14:166–229.Google Scholar
ANDERSON, J. R. 2000. Sleep-related behavioural adaptations in free ranging anthropoid primates. Sleep Medicine Reviews 4:355373.CrossRefGoogle ScholarPubMed
ARIZPE, L., PAZ, F. & VELÁZQUEZ, M. 1993. Cultura y cambio global: percepciones sociales sobre la deforestación en la Selva Lacandona. Pp. 6989 in Miguel, A. P. (ed.). La selva Lacandona: tierra de nadie, tierra de todos. Centro Regional de Investigaciones Multidisciplinarias, Universidad Nacional Autónoma de México, Mexico City.Google Scholar
ARROYO-RODRÍGUEZ, V. & MANDUJANO, S. 2006. Forest fragmentation modifies habitat quality for Alouatta palliata. International Journal of Primatology 27:10791096.CrossRefGoogle 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. Pp. 111139 in Kowalewski, M., Garber, P. A., Cortés-Ortiz, L., Urbani, B. & Youlatos, D. (eds.). Howler monkeys: behavior, ecology and conservation. Springer, New York.CrossRefGoogle Scholar
ASENSIO, N., SCHAFFNER, C. M. & AURELI, F. 2012a. Variability in core areas of spider monkeys (Ateles geoffroyi) in a tropical dry forest in Costa Rica. Primates 53:147156.CrossRefGoogle Scholar
ASENSIO, N., LUSSEAU, D., SCHAFFNER, C. M. & AURELI, F. 2012b. Spider monkeys use high-quality core areas in a tropical dry forest. Journal of Zoology 287:250258.CrossRefGoogle Scholar
BÖRGER, L., DALZIEL, B. D. & FRYXELL, J. M. 2008. Are there general mechanisms of animal home range behaviour? A review and prospects for future research. Ecology Letters 11:637650.CrossRefGoogle ScholarPubMed
BRAVO, S. P. 2012. The impact of seed dispersal by black and gold howler monkeys on forest regeneration. Ecological Research 27:311321.CrossRefGoogle Scholar
BUENO, R. S., GUEVARA, R., RIBEIRO, M. C., CULOT, L., BUFALO, F. S. & GALETTI, M. 2013. Functional redundancy and complementarities of seed dispersal by the last Neotropical megafrugivores. PLoS ONE 8:e56252.CrossRefGoogle ScholarPubMed
CHAPMAN, C. A. 1988. Patterns of foraging and range use by three species of Neotropical primates. Primates 29:177194.CrossRefGoogle Scholar
CHAPMAN, C. A. 1989. Spider monkey sleeping sites: use and availability. American Journal of Primatology 18:5360.CrossRefGoogle ScholarPubMed
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 79:506511.CrossRefGoogle ScholarPubMed
CHAPMAN, C. A., CHAPMAN, L. J., WRANGHAM, R., HUNT, K., GEBO, D. & GARDNER, L. 1992. Estimators of fruit abundance of tropical trees. Biotropica 24:527531.CrossRefGoogle Scholar
CHAPMAN, C. A., WRANGHAM, R. W. & CHAPMAN, L. J. 1995. Ecological constraints on group size: an analysis of spider monkey and chimpanzee subgroups. Behavioral Ecology and Sociobiology 36:5970.CrossRefGoogle Scholar
CHAO, A. & JOST, L. 2012. Coverage-based rarefaction and extrapolation: standardizing samples by completeness rather than size. Ecology 93:25332547.CrossRefGoogle ScholarPubMed
CHAO, A., CHIU, C. H. & HSIEH, T. 2012. Proposing a resolution to debates on diversity partitioning. Ecology 93:20372051.CrossRefGoogle ScholarPubMed
CHAVES, O. M., STONER, K. E. & ARROYO-RODRÍGUEZ, V. 2011. Effectiveness of spider monkeys (Ateles geoffroyi vellerosus) as seed dispersers in continuous and fragmented rainforests in southern Mexico. International Journal of Primatology 32:177192.CrossRefGoogle Scholar
CHAVES, O. M., STONER, K. E. & ARROYO-RODRÍGUEZ, V. 2012. Differences in diet between spider monkey groups living in forest fragments and continuous forest in Lacandona, Mexico. Biotropica 44:105113.CrossRefGoogle Scholar
CRAWLEY, M. 2002. Statistical computing: an introduction to data analysis using S-Plus. John Wiley & Sons, Chichester. 772 pp.Google Scholar
CONNELL, J. H. 1971. On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. Pp. 298312 in den Boer, P. J. & Gradwell, G. R. (eds.). Dynamics of populations. Center for Agricultural Publication and Documentation, Wageningen.Google Scholar
DEW, J. L. 2008. Spider monkeys as seed dispersers. Pp. 155182 in Campbell, C. J. (ed.). Spider monkeys. The biology, behavior and ecology of the genus Ateles. Cambridge University Press, New York.CrossRefGoogle Scholar
EIGENBROD, F., HECNAR, S. J. & FAHRIG, L. 2011. Sub-optimal study design has major impacts on landscape-scale inference. Biological Conservation 144:298305.CrossRefGoogle Scholar
DI FIORE, A. & SUAREZ, S. A. 2007. Route-based travel and shared routes in sympatric spider and woolly monkeys: cognitive and evolutionary implications. Animal Cognition 10:317–329.CrossRefGoogle ScholarPubMed
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 71:820.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
GONZÁLEZ-ZAMORA, A., ARROYO-RODRÍGUEZ, V., ESCOBAR, F., RÖS, M., OYAMA, K., IBARRA-MANRÍQUEZ, G. & STONER, K. E. 2014. Contagious deposition of seeds in spider monkeys’ sleeping trees limits effective seed dispersal in fragmented landscapes. PLoS ONE 9 (2): e89346.CrossRefGoogle ScholarPubMed
HERNÁNDEZ-RUEDAS, M. A., ARROYO-RODRÍGUEZ, V., MEAVE, J. A., MARTÍNEZ-RAMOS, M., IBARRA-MANRÍQUEZ, I., MARTÍNEZ, E., JAMANGAPE, J., MELO, F. P. L. & SANTOS, B. A. 2014. Conserving tropical tree diversity and forest structure: the value of small rainforest patches in moderately-managed landscapes. PLoS ONE 9 (6):e98931.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
IBARRA-MANRÍQUEZ, G. & CORNEJO-TENORIO, G. 2010. Diversidad de frutos de los árboles del bosque tropical perennifolio de México. Acta Botánica Mexicana 90:51104.CrossRefGoogle Scholar
JANSON, C. H. 1983. Adaptation of fruit morphology to dispersal agents in a Neotropical forest. Science 219:187189.CrossRefGoogle Scholar
JANZEN, D. H. 1970. Herbivores and the number of tree species in tropical forests. American Naturalist 104:501528.CrossRefGoogle Scholar
JORDANO, P. 1992. Fruits and frugivory. Pp. 105156 in Fenner, M. (ed.). Seeds: the ecology of regeneration in plant communities. CAB International, Wallingford.Google Scholar
JORDANO, P. & SCHUPP, E. W. 2000. Seed disperser effectiveness: the quantity component and patterns of seed rain for Prunus mahaleb. Ecological Monographs 70:591615.CrossRefGoogle Scholar
JOST, L. 2006. Entropy and diversity. Oikos 113:363375.CrossRefGoogle Scholar
JOST, L. 2007. Partitioning diversity into independent alpha and beta components. Ecology 88:24272439.CrossRefGoogle ScholarPubMed
JOST, L. 2010. The relation between evenness and diversity. Diversity 2:207232.CrossRefGoogle Scholar
LINK, A., GALVIS, N., MARQUEZ, M., GUERRERO, J., SOLANO, C. & STEVENSON, P. R. 2012. Diet of the critically endangered brown spider monkey (Ateles hybridus) in an inter-Andean lowland rainforest in Colombia. American Journal of Primatology 74:10971105.CrossRefGoogle Scholar
MILTON, K. 1980. The foraging strategy of howler monkeys: a study in primate economics. Columbia University Press, New York. 165 pp.Google Scholar
MORA, F. 2008. Caracterización de la cobertura forestal en el Corredor Biológico Mesoamericano-México: patrones espaciales en la pérdida y fragmentación de bosques. Pp. 55–83 in Comisión Nacional para el Conocimiento y Uso de la Biodiversidad (CONABIO). Importancia del capital ecológico de la región Corredor Biológico Mesoamericano-México. Centro de Investigación en Geografía y Geomática, CentroGEO, Mexico City.Google Scholar
MYERS, N., MITTERMEIER, R. A., MITTERMEIER, C. G., DA FONSECA, G. A. & KENT, J. 2000. Biodiversity hotspots for conservation priorities. Nature 403:853858.CrossRefGoogle ScholarPubMed
NUNES, A. 1998. Diet and feeding ecology of Ateles belzebuth at Maracá ecological station, Roraima, Brasil. Folia Primatologica 69:6176.CrossRefGoogle Scholar
PONTES, A. R. & SOARES, M. 2005. Sleeping sites of common marmosets (Callithrix jacchus) in defaunated urban forest fragments: a strategy to maximize food intake. Journal of Zoology 26:5563.CrossRefGoogle Scholar
RAMOS-FERNÁNDEZ, G. & WALLACE, R. B. 2008. Spider monkey conservation in the twenty-first century: recognizing risks and opportunities. Pp. 351372 in Campbell, J. C. (ed.). Spider monkeys. The biology, behavior and ecology of the genus Ateles. Cambridge University Press, New York.CrossRefGoogle Scholar
RAMOS-FERNÁNDEZ, G., MATEOS, J. L., MIRAMONTES, O., LARRALDE, H., COCHO, G. & AYALA-OROZCO, B. 2004. Lévy walk patterns in the foraging movements of spider monkeys (Ateles geoffroyi). Behavioral Ecology and Sociobiology 55:223230.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.CrossRefGoogle ScholarPubMed
REICHARD, U. 1998. Sleeping sites, sleeping places, and presleep behavior of gibbons (Hylobates lar). American Journal of Primatology 46:3562.3.0.CO;2-W>CrossRefGoogle ScholarPubMed
ROGERS, M. E., VOYSEY, B. C., MCDONALD, K. E., PARNELL, R. J. & TUTIN, C. E. G. 1998. Lowland gorillas and seed dispersal: the importance of nest sites. American Journal of Primatology 45:4568.3.0.CO;2-W>CrossRefGoogle ScholarPubMed
RUSSO, S. E. & AUGSPURGER, C. K. 2004. Aggregated seed dispersal by spider monkeys limits recruitment to clumped patterns in Virola calophylla. Ecology Letters 7:10581067.CrossRefGoogle Scholar
RUSSO, S. E., CAMPBELL, C. J., DEW, L., STEVENSON, P. R. & SUAREZ, S. A. 2005. A multi-forest comparison of dietary preferences and seed dispersal by Ateles spp. International Journal of Primatology 26:10171037.CrossRefGoogle Scholar
RUSSO, S. E., PORTNOY, S. & AUGSPURGER, C. K. 2006. Incorporating animal behavior into seed dispersal models: implications for seed shadows. Ecology 87:31603174.CrossRefGoogle ScholarPubMed
SCHUPP, E. W. 1993. Quantity, quality and the effectiveness of seed dispersal by animals. Vegetatio 107:1529.CrossRefGoogle Scholar
SCHUPP, E. W., JORDANO, P. & GÓMEZ, J. M. 2010. Seed dispersal effectiveness revisited: a conceptual review. New Phytologist 188:333353.CrossRefGoogle ScholarPubMed
SIGG, H. & STOLBA, A. 1981. Home range use and daily march in a hamadryas baboon troop. Folia Primatologica 36:40–75.CrossRefGoogle Scholar
SILVA JÚNIOR, W. M., MEIRA-NETO, J. A. A., DA SILVA FLÁVIA, M. C., RODRIGUES DE MELO, F., SANTANA MOREIRA, L., FERREIRA BARBOSA, E., DIAS, L. G. & SILVA PERES, C. A. 2009. Habitat quality of the woolly spider monkey. Folia Primatologica 80:295308.CrossRefGoogle ScholarPubMed
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). American Journal of Physical Anthropology 134:340–353.CrossRefGoogle ScholarPubMed
STEVENSON, P. R. 2000. Seed dispersal by woolly monkeys (Lagothrix lagothricha) at Tinigua National Park, Colombia: dispersal distance, germination rates, and dispersal quantity. American Journal of Primatology 50:275–289.3.0.CO;2-K>CrossRefGoogle ScholarPubMed
STONER, K. E., RIBA-HERNÁNDEZ, P., VULINEC, K. & LAMBERT, J. E. 2007. The role of mammals in creating and modifying seedshadows in tropical forests and some possible consequences of their elimination. Biotropica 39:316327.CrossRefGoogle Scholar
SUAREZ, S. A. 2003. Spatio-temporal foraging skills of white-bellied spider monkeys (Ateles belzebuth belzebuth) in the Yasuni National Park, Ecuador. Doctoral dissertation, State University of New York at Stony Brook, Stony Brook.Google Scholar
SUAREZ, S. A., KARRO, J., KIPER, J., FARLER, D., MCELROY, B., ROGERS, B. C., STOCKWELL, B. & TAYLOR, Y. 2014. A comparison of computer‐generated and naturally occurring foraging patterns in route‐network‐constrained spider monkeys. American Journal of Primatology 76:460–471.CrossRefGoogle ScholarPubMed
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 53:287296.CrossRefGoogle ScholarPubMed
TUOMISTO, H. 2010. A diversity of beta diversities: straightening up a concept gone awry. Part 1. Defining beta diversity as a function of alpha and gamma diversity. Ecography 33:222.CrossRefGoogle Scholar
VALERO, A. & BYRNE, R. W. 2007. Spider monkey ranging patterns in Mexican subtropical forest: do travel routes reflect planning? Animal Cognition 10:305315.CrossRefGoogle ScholarPubMed
WALLACE, R. B. 2008. Towing the party line: territoriality, risky boundaries and male group size in spider monkey fission–fusion societies. American Journal of Primatology 70:271281.CrossRefGoogle ScholarPubMed
WANG, B. C. & SMITH, T. B. 2002. Closing the seed dispersal loop. Trends in Ecology and Evolution 17:379385.CrossRefGoogle Scholar
WENNY, D. G. 2001. Advantages of seed dispersal: a re-evaluation of directed dispersal. Evolutionary Ecology Research 3:5174.Google Scholar