Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-26T14:56:37.985Z Has data issue: false hasContentIssue false
  • English
  • Français

Parent-parent and parent-offspring distances in Spondias radlkoferi seeds suggest long-distance pollen and seed dispersal: evidence from latrines of the spider monkey

Published online by Cambridge University Press:  23 March 2017

Víctor Arroyo-Rodríguez ,
Esther Aguilar-Barajas ,
Arturo González-Zamora ,
Víctor Rocha-Ramírez ,
Antonio González-Rodríguez  and
Ken Oyama
Víctor Arroyo-Rodríguez*
Affiliation:
Instituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad Nacional Autónoma de México, Morelia, Michoacán, Mexico
Esther Aguilar-Barajas
Affiliation:
Escuela Nacional de Estudios Superiores Morelia, Universidad Nacional Autónoma de México, Morelia, Michoacán, Mexico
Arturo González-Zamora
Affiliation:
Instituto de Investigaciones Biológicas, Universidad Veracruzana, Xalapa, Veracruz, Mexico
Víctor Rocha-Ramírez
Affiliation:
Instituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad Nacional Autónoma de México, Morelia, Michoacán, Mexico
Antonio González-Rodríguez
Affiliation:
Instituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad Nacional Autónoma de México, Morelia, Michoacán, Mexico
Ken Oyama
Affiliation:
Instituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad Nacional Autónoma de México, Morelia, Michoacán, Mexico Escuela Nacional de Estudios Superiores Morelia, Universidad Nacional Autónoma de México, Morelia, Michoacán, Mexico
*
*Corresponding author. Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract:

Pollen and seed dispersal are key ecological processes, directly impacting the spatial distribution, abundance and genetic structure of plant populations; yet, pollen- and seed-dispersal distances are poorly known. We used molecular markers to identify the parental origin (n = 152 adult trees) of 177 Spondias radlkoferi (Anacardiaceae) seeds deposited by the spider monkey (Ateles geoffroyi) in latrines located beneath 17 sleeping-trees in two continuous forest sites (CF) and two forest fragments (FF) in the Lacandona rain forest, Mexico. We estimated mean parent-offspring (PO) distances per latrine and, for those seeds (54% of seeds) with more than one candidate parent (i.e. the potential maternal and parental parents), we also estimated parent-parent (PP) distances per latrine, and tested if PO and PP distances differed between forest types. Global PO and PP distances per latrine averaged 682 m (range = 83–1741 m) and 610 m (range = 74–2339 m), respectively, and did not differ significantly between CF and FF. This suggests that pollen dispersal is extensive in both forest types and that long seed dispersal distances (>100 m) are common, thus supporting the hypothesis that the spider monkey is an effective seed disperser of S. radlkoferi in continuous and fragmented forests.

Keywords

Atelesforest fragmentationLacandonaparental analysispollen dispersalseed dispersal effectiveness
Type
Research Article
Information
Journal of Tropical Ecology , Volume 33 , Issue 2 , March 2017 , pp. 95 - 106
Copyright
Copyright © Cambridge University Press 2017 

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

ADLER, G. H. & KIELPINSKI, K. A. 2000. Reproductive phenology of a tropical canopy tree, Spondias mombin. Biotropica 32:686–692.Google Scholar
AGUILAR-BARAJAS, E., SORK, V., GONZÁLEZ-ZAMORA, A., ROCHA-RAMÍREZ, V., ARROYO-RODRÍGUEZ, V. & OYAMA, K. 2014. Isolation and characterization of polymorphic microsatellite loci in Spondias radlkoferi (Anacardiaceae). Applications in Plant Sciences 2:1400079.Google Scholar
ARROYO-RODRÍGUEZ, V. & MANDUJANO, S. 2006. The importance of tropical rain forest fragments to the conservation of plant species diversity in Los Tuxtlas, Mexico. Biodiversity and Conservation 15: 4159–4179.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. Pp. 111–139 in Kowalewski, M., Garber, P. A., Cortés-Ortiz, L., Urbani, B. & Youlatos, D. (eds). Howler monkeys. Developments in Primatology: Progress and Prospects series. Springer, New York.Google Scholar
AURELI, F., SCHAFFNER, C. M., BOESCH, C., BEARDER, S. K., CALL, J., CHAPMAN, C. A., CONNOR, R., DI FIORE, A., DUNBAR, R. I. M., HENZI, P., HOLEKAMP, K., KORSTJENS, A. H., LAYTON, R., LEE, F., LEHMANN, J. MANSON, J. H., RAMOS-FERNANDEZ, G., STRIER, K. B. & VAN SCHAIK, C. P. 2008. Fission-fusion dynamics: new research frameworks. Current Anthropology 49:627–654.Google Scholar
BAWA, K. S. 1990. Plant-pollinator interactions in tropical rain forests. Annual Review of Ecology and Systematics 21:399–422.Google Scholar
BENÍTEZ-MALVIDO, J., GONZÁLEZ-DI PIERRO, A. M., LOMBERA, R., GUILLÉN, S. & ESTRADA, A. 2014. Seed source, seed traits, and frugivore habits: implications for dispersal quality of two sympatric primates. American Journal of Botany 101:970–978.Google Scholar
BUFALO, F. S., GALETTI, M. & CULOT, L. 2016. Seed dispersal by primates and implications for the conservation of a biodiversity hotspot, the Atlantic forest of South America. International Journal of Primatology 37:333–349.Google Scholar
CAIN, M. L., MILLIGAN, B. G. & STRAND, A. E. 2000. Long-distance seed dispersal in plant populations. American Journal of Botany 87:1217–1227.Google Scholar
CAMPBELL, C. J. 2008. Spider monkeys. The biology, behaviour and ecology of the genus Ateles. Cambridge University Press, New York. 410 pp.Google Scholar
CARNEIRO, L. & MARTINS, C. 2012. Africanized honey bees pollinate and preempt the pollen of Spondias mombin (Anacardiaceae) flowers. Apidologie 43:474–486.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.Google 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 44:105–113.Google Scholar
COLLEVATTI, R. G., SCHOEREDER, J. H. & CAMPOS, L. A. O. 2000. Foraging behavior of bee pollinators on the tropical weed Triumfetta semitriloba: flight distance and directionality. Revista Brasileira de Biologia 60:29–37.Google Scholar
CORDEIRO, N. J., NDANGALASI, H. J., MCENTEE, J. P. & HOWE, H. F. 2009. Dispersal limitation and recruitment of an endemic African tree in a fragmented landscape. Ecology 90:1030–1041.CrossRefGoogle Scholar
CRAMER, J. M., MESQUITA, R. C. G. & WILLIAMSON, G. B. 2007. Forest fragmentation differentially affects seed dispersal of large and small-seeded tropical trees. Biological Conservation 137:415–423.CrossRefGoogle Scholar
CUNNINGHAM, S. A. 2000. Depressed pollination in habitat fragments causes low fruit set. Proceedings of the Royal Society of London Series B – Biological Sciences 267:1149–1152.Google Scholar
DEW, J. L. 2008. Spider monkeys as seed dispersers. Pp. 155–182 in Campbell, C. J. (ed.). Spider monkeys. Behaviour, ecology and evolution of the genus Ateles. Cambridge University Press, New York.Google Scholar
DI FIORE, A. & CAMPBELL, C. J. 2007. The Atelines: variation in ecology, behavior, and social organization. Pp. 155–185 in Campbell, C. J., Fuentes, A., MacKinnon, K. C., Panger, M. & Beader, S. K. (eds). Primates in perspective. Oxford University Press, New York.Google Scholar
DICK, C. W., ETCHELECU, G. & AUSTERLITZ, F. 2003. Pollen dispersal of tropical trees (Dinizia excelsa: Fabaceae) by native insects and African honeybees in pristine and fragmented Amazonian rainforest. Molecular Ecology 12:753–764.Google Scholar
DICK, C., HARDY, O., JONES, F. & PETIT, R. 2008. Spatial scales of pollen and seed-mediated gene flow in tropical rain forest trees. Tropical Plant Biology 1:20–33.Google Scholar
GODOY, J. A. & JORDANO, P. 2001. Seed dispersal by animals: exact identification of source trees with endocarp DNA microsatellites. Molecular Ecology 10:2275–2283.Google Scholar
GONZÁLEZ-ZAMORA, A., ARROYO-RODRÍGUEZ, V., CHAVES, O. M., SÁNCHEZ-LOPEZ, 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.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.Google Scholar
GONZÁLEZ-ZAMORA, A., ARROYO-RODRÍGUEZ, V., ESCOBAR, F., RÖS, M., OYAMA, K., IBARRA-MANRÍQUEZ, G., STONER, K. E. & CHAPMAN, C. A. 2014. Contagious deposition of seeds in spider monkeys' sleeping-trees limits effective seed dispersal in fragmented landscapes. PLoS ONE 9:e89346.Google Scholar
GONZÁLEZ-ZAMORA, A., ARROYO-RODRÍGUEZ, V., ESCOBAR, F., OYAMA, K., STONER, K. E. & AURELI, F. 2015. Sleeping-tree fidelity of the spider monkey shapes community-level seed rain patterns in continuous and fragmented rain forests. Journal of Tropical Ecology 31:305–313.Google Scholar
GRAFEN, A. & HAILS, R. 2002. Modern statistics for the life sciences. Oxford University Press, Oxford. 351 pp.Google Scholar
GRIVET, D., SMOUSE, P. E. & SORK, V. L. 2005. A novel approach to an old problem: tracking dispersed seeds. Molecular Ecology 14:3585–3595.CrossRefGoogle Scholar
HOBAN, S. M., SCHLARBAUM, S. E., BROSI, S. L. & ROMERO-SEVERSON, J. 2012. A rare case of natural regeneration in butternut, a threatened forest tree, is parent and space limited. Conservation Genetics 13:1447–1457.Google Scholar
HOWE, H. F. & SMALLWOOD, J. 1982. Ecology of seed dispersal. Annual Review of Ecology and Systematics 13:201–228.Google Scholar
IBARRA- MANRÍQUEZ, G. & OYAMA, K. 1992. Ecological correlates of reproductive traits of Mexican rain forest trees. American Journal of Botany 79:383–394.Google Scholar
JORDANO, P. 2007. Frugivores, seeds and genes: analysing the key elements of seed shadows. Pp. 229–251 in Dennis, A., Green, R., Schupp, E. W. & Wescott, D. (eds). Frugivory and seed dispersal: theory and applications in a changing world. Commonwealth Agricultural Bureau International, Wallingford.Google Scholar
JORDANO, P., FORGET, P.-M., LAMBERT, J. E., BÖHNING-GAESE, K., TRAVESET, A. & WRIGHT, S. J. 2011. Frugivores and seed dispersal: mechanisms and consequences for biodiversity of a key ecological interaction. Biology Letters 7:321–323.Google Scholar
KALINOWSKI, S. T. 2005. HP-Rare: a computer program for performing rarefaction on measures of allelic diversity. Molecular Ecology Notes 5:187–189.Google Scholar
KALINOWSKI, S. T., WAGNER, A. P. & TAPER, M. L. 2006. ML-Relate: a computer program for maximum likelihood estimation of relatedness and relationship. Molecular Ecology Notes 6:576–579.CrossRefGoogle Scholar
LINK, A. & DI FIORE, A. 2006. Seed dispersal by spider monkeys and its importance in the maintenance of Neotropical rainforest diversity. Journal of Tropical Ecology 22:235–246.Google Scholar
MILLAR, M. A., COATES, D. J. & BYRNE, M. 2014. Extensive long-distance pollen dispersal and highly outcrossed mating in historically small and disjunct populations of Acacia woodmaniorum (Fabaceae), a rare banded iron formation endemic. Annals of Botany 114:961–971.Google Scholar
MILTON, K. 1981. Food choice and digestive strategies of two sympatric primate species. American Naturalist 117:496–505.Google Scholar
NADIA, T. L., MACHADO, I. S. & LOPES, A. V. 2007. Polinização de Spondias tuberosa Arruda (Anacardiaceae) e análise da partilha de polinizadores com Ziziphus joazeiro Mart. (Rhamnaceae), espécies frutíferas e endêmicas da Caatinga. Revista Brasileira de Botanica 30:89–100.Google Scholar
PEAKALL, R. & SMOUSE, P. E. 2006. GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6: 288–295.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.Google Scholar
REITER, J., CURIO, E., TACUD, B., URBINA, H. & GERONIMO, F. 2006. Tracking bat-dispersed seeds using fluorescent pigment. Biotropica 38:64–68.Google Scholar
ROBERTSON, A. W., KELLY, D., LADLEY, J. J. & SPARROW, A. D. 1999. Effects of pollinator loss on endemic New Zealand mistletoes (Loranthaceae). Conservation Biology 13:499–508.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.Google Scholar
RUSSO, S. E. & CHAPMAN, C. A. 2011. Primate seed dispersal: Linking behavioral ecology with forest community structure. Pp. 510–525 in Campbell, C. J., Fuentes, A. F., MacKinnon, K. C., Panger, M. & Bearders, S. (eds.). Primates in perspective. Oxford University Press, Oxford.Google Scholar
RUSSO, S. E., PORTNOY, S. & AUGSPURGER, C. K. 2006. Incorporating animal behavior into seed dispersal models: implications for seed shadows and an example for a primate-dispersed tree. Ecology 87:3160–3174.Google Scholar
SAZAN, M. S., BEZERRA, A. D. M. & FREITAS, B. M. 2014. Oil collecting bees and Byrsonima cydoniifolia A. Juss. (Malpighiaceae) interactions: the prevalence of long-distance cross pollination driving reproductive success. Anais da Academia Brasileira de Ciências 86:347–357.Google Scholar
SCHUPP, E. W. 1993. Quantity, quality and the effectiveness of seed dispersal by animals. Vegetatio 107/108:15–29.CrossRefGoogle Scholar
SCHUPP, E. W., MILLERON, T. & RUSSO, S. E. 2002. Dissemination limitation and the origin and maintenance of species-rich tropical forests. Pp. 19–33 in Levey, D. J., Silva, W. R. & Galetti, M. M. (eds.). Seed dispersal and frugivory: ecology, evolution and conservation. CAB International, Wallingford.Google Scholar
STACY, E. A., HAMRICK, J. L., NASON, J. D., HUBBELL, S. P., FOSTER, R. B. & CONDIT, R. 1996. Pollen dispersal in low-density populations of three neotropical tree species. American Naturalist 148:275–298.Google Scholar
TERAKAWA, M., ISAGI, Y., MATSUI, K. & YUMOTO, T. 2009. Microsatellite analysis of the maternal origin of Myrica rubra seeds in the feces of Japanese macaques. Ecological Research 24:663–670.CrossRefGoogle Scholar
VAN OOSTERHOUT, C., HUTCHINSON, W. F., WILLS, D. P. M. & SHIPLEY, R. 2004. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4:535–538.Google Scholar
VELÁZQUEZ-VÁZQUEZ, G., REYNA-HURTADO, R., ARROYO-RODRÍGUEZ, V., CALMÉ, S., LÉGER-DALCOURT, M. & NAVARRETE, D. A. 2015. Sleeping sites of spider monkeys (Ateles geoffroyi) in logged and unlogged tropical forests. International Journal of Primatology 36:1154–1171.Google Scholar
WAGNER, A. P., CREEL, S. & KALINOWSKI, S. T. 2006. Estimating relatedness and relationships using microsatellite loci with null alleles. Heredity 97:336–345.Google Scholar
WALLACE, R. B. 2008. Factors influencing spider monkey habitat use and ranging patterns. Pp. 138–154 in Campbell, C. J. (ed.). Spider monkeys: behavior, ecology and evolution of the genus Ateles. Cambridge University Press, Cambridge.Google Scholar
WEBB, C. J. & BAWA, K. S. 1983. Pollen dispersal by hummingbirds and butterflies: a comparative study of two lowland tropical plants. Evolution 37:1258–1270.Google Scholar
WHEELWRIGHT, N. T. & ORIANS, G. H. 1982. Seed dispersal by animals: contrasts with pollen dispersal, problems of terminology, and constraints on coevolution. American Naturalist 119:402–413.Google Scholar