Hostname: page-component-7c8c6479df-5xszh Total loading time: 0 Render date: 2024-03-29T18:51:22.727Z Has data issue: false hasContentIssue false

Upward movement of buried seeds: another ecological role of dung beetles promoting seedling establishment

Published online by Cambridge University Press:  01 August 2014

Carolina Santos-Heredia*
Affiliation:
Centro de Investigaciones en Ecosistemas, Universidad Nacional Autónoma de México, Antigua Carretera a Pátzcuaro No. 8701, Ex-Hacienda de San José de la Huerta, CP 58090, Morelia, Michoacán, México Posgrado en Ciencias Biológicas, Universidad Nacional Autónoma de México, Av. Ciudad Universitaria 3000, C.P. 04360, Coyoacán, Distrito Federal, México
Ellen Andresen
Affiliation:
Centro de Investigaciones en Ecosistemas, Universidad Nacional Autónoma de México, Antigua Carretera a Pátzcuaro No. 8701, Ex-Hacienda de San José de la Huerta, CP 58090, Morelia, Michoacán, México
*
1Corresponding author. Email: macasahe@gmail.com

Abstract:

Dung beetles are known to perform important ecological functions, such as secondary seed dispersal of vertebrate-defecated seeds. We found that dung beetles also move buried seeds upwards, with positive consequences for seedling establishment. In the Lacandon rain forest of southern Mexico we conducted field experiments to address three questions: (1) What proportions of different-sized seeds buried by dung beetles are exhumed by them? (2) Does upward relocation of seeds caused by dung beetle activity promote seedling establishment? (3) Does recurrent beetle activity increase seedling establishment? Using 4-mm, 8-mm and 12-mm beads as seed mimics, embedded in howler-monkey dung, we found that 2–6% of buried beads were later exhumed by beetles, with smaller beads exhumed more often. In small plots (N = 100) where beetles were allowed to bury dung and seed rain was excluded, seedling establishment was over three times higher compared with plots without beetle activity. In plots (N = 8) where we placed dung on four occasions in 1 mo, seedling establishment was more than twice as high compared with plots with single-time dung placement. We believe that our findings open up interesting research opportunities to help further elucidate this newly discovered ecological function of dung beetles.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2014 

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

ANDRESEN, E. 2001. Effects of dung presence, dung amount, and secondary dispersal by dung beetles on the fate of Micropholis guyanensis (Sapotaceae) seeds in Central Amazonia. Journal of Tropical Ecology 17:6178.CrossRefGoogle Scholar
ANDRESEN, E. 2002. Dung beetles in a Central Amazonian rainforest and their ecological role as secondary seed dispersers. Ecological Entomology 27:257270.CrossRefGoogle Scholar
ANDRESEN, E. & FEER, F. 2005. The role of dung beetles as secondary seed dispersers and their effect on plant regeneration in tropical rainforests. Pp. 331349 in Forget, P.-M., Lambert, J., Hulme, P. & Vander Wall, S. B. (eds). Seed fate: predation, dispersal and seedling establishment. CABI Publishing, Wallingford.CrossRefGoogle Scholar
ANDRESEN, E. & LEVEY, D. J. 2004. Effects of dung and seed size on secondary dispersal, seed predation, and seedling establishment of rain forest trees. Oecologia 139:145154.CrossRefGoogle ScholarPubMed
BEATTIE, A. J. & CULVER, D. C. 1982. Inhumation: how ants and other invertebrates help seeds. Nature 297:627.CrossRefGoogle ScholarPubMed
BRAGA, R. F., KORASAKI, V., ANDRESEN, E. & LOUZADA, J. 2013. Dung beetle community and functions along a habitat-disturbance gradient in the Amazon: a rapid assessment of ecological functions associated to biodiversity. PLOS ONE 8 (2): e57786. doi:10.1371/journal.pone.0057786.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
CRAWLEY, M. J. 2000. Seed predators and plant population dynamics. Pp. 167182 in Fenner, M. (ed.). Seeds: the ecology of regeneration in plant communities. CABI Publishing, Wallingford.CrossRefGoogle Scholar
CRAWLEY, M. J. 2007. The R book. Wiley & Sons, Chichester. 942 pp.CrossRefGoogle Scholar
CULOT, L., HUYNEN, M.-C., GÉRARD, P. & HEYMANN, E. W. 2009. Short-term post-dispersal fate of seeds defecated by two small primate species (Saguinus mystax and Saguinus fuscicollis) in the Amazonian forest of Peru. Journal of Tropical Ecology 25:229238.CrossRefGoogle Scholar
DALLING, J. W. 2005. The fate of seed banks: factors influencing seed survival for light-demanding species in moist tropical forests. Pp. 3144 in Forget, P.-M., Lambert, J., Hulme, P. & Vander Wall, S. B. (eds). Seed fate: predation, dispersal and seedling establishment. CABI Publishing, Wallingford.CrossRefGoogle Scholar
DALLING, J. W., SWAINE, M. D. & GARWOOD, N. C. 1994. Effect of soil depth on seedling emergence in tropical soil seed-bank investigations. Functional Ecology 9:119121.CrossRefGoogle Scholar
DALLING, J. W., DAVIS, A. S., SCHUTTE, B. J. & ARNOLD, A. E. 2011. Seed survival in soil: interacting effects of predation, dormancy and the soil microbial community. Journal of Ecology 99:89–95.CrossRefGoogle Scholar
DANGLES, O., CARPIO, C. & WOODWARD, G. 2012. Size-dependent species removal impairs ecosystem functioning in a large-scale tropical field experiment. Ecology 93:26152625.CrossRefGoogle Scholar
DONATH, T. W. & ECKSTEIN, R. L. 2012. Litter effects on seedling establishment interact with seed position and earthworm activity. Plant Biology 14:163170.CrossRefGoogle ScholarPubMed
FEER, F., PONGE, J. F., JOUARD, S. & GOMEZ, D. 2013. Monkey and dung beetle activities influence soil seed bank structure. Ecological Research 28:93–102.CrossRefGoogle Scholar
FENNER, M. 2000. Seeds: the ecology of regeneration in plant communities. (Second edition). CABI Publishing, Wallingford. 410 pp.CrossRefGoogle Scholar
FRAGOSO, J. M. V., SILVIUS, K. M. & CORREA, J. A. 2003. Long-distance seed dispersal by tapirs increases seed survival and aggregates tropical trees. Ecology 84:19982006.CrossRefGoogle Scholar
GARWOOD, N. C. 1989. Tropical soil seed banks: a review. Pp. 149209 in Leck, M. A., Parker, V. T. & Simpson, R. L. (eds). Ecology of soil seed banks. Academic Press, San Diego.CrossRefGoogle 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 (10):e46852. doi:10.1371/journal.pone.0046852.CrossRefGoogle ScholarPubMed
GRANT, J. D. 1983. The activities of earthworms and the fate of seeds. Pp. 107122 in Satchell, J. E. (ed). Earthworm ecology from Darwin to vermiculture. Chapman and Hall, London.CrossRefGoogle Scholar
HOLDRIDGE, L. R. 1967. Life zone ecology. Tropical Science Center, San José. 206 pp.Google Scholar
HULME, P. E. 2002. Seed-eaters: dispersal, destruction and demography. Pp. 257273 in Levey, D. J., Silva, W. R. & Galetti, M. (eds.). Seed dispersal and frugivory: ecology, evolution and conservation. CABI Publishing, Wallingford.Google Scholar
IRWIN, M. T., SAMONDS, K. E., RAHARISON, J. L. & WRIGHT, P. C. 2004. Lemur latrines: observations of latrine behavior in wild primates and possible ecological significance. Journal of Mammalogy 85:420427.2.0.CO;2>CrossRefGoogle Scholar
LAWSON, C. R., MANN, D. J. & LEWIS, O. T. 2012. Dung beetles reduce clustering of tropical tree seedlings. Biotropica 44:271275.CrossRefGoogle Scholar
MARTHEWS, T. R., MULLINS, C. E., DALLING, J. W. & BURSLEM, D. F. 2008. Burial and secondary dispersal of small seeds in a tropical forest. Journal of Tropical Ecology 24:595605.CrossRefGoogle Scholar
MEDELLÍN, R. A. 1994. Mammal diversity and conservation in the Selva Lacandona, Chiapas, Mexico. Conservation Biology 8:780–799.CrossRefGoogle Scholar
NICHOLS, E., SPECTOR, S., LOUZADA, J., LARSEN, T., AMEZQUITA, S., FAVILA, M.E. & TSR NETWORK. 2008. Ecological functions and ecosystem services provided by Scarabaeinae dung beetles. Biological Conservation 141:14611474.CrossRefGoogle Scholar
PEARSON, T. R. H., BURSLEM, D. F., MULLINS, C. E. & DALLING, J. W. 2002. Germination ecology of neotropical pioneers: interacting effects of environmental conditions and seed size. Ecology 83:2798–2807.CrossRefGoogle Scholar
POUVELLE, S., JOUARD, S., FEER, F., TULLY, T. & PONGE, J.-F. 2009. The latrine effect: impact of howler monkeys on the distribution of small seeds in a tropical rain-forest soil. Journal of Tropical Ecology 25:239248.CrossRefGoogle Scholar
PUTZ, F. E. & APPANAH, S. 1987. Buried seeds, newly dispersed seeds, and the dynamics of a lowland forest in Malaysia. Biotropica 19:326333.CrossRefGoogle Scholar
RUSSO, S. E. & AUGSPURGER, C. K. 2004. Aggregated seed dispersal by spider monkeys limits recruitment to clumped patterns in Virola calophylla. Ecology Letters 7:10581067.CrossRefGoogle Scholar
SANTOS-HEREDIA, C., ANDRESEN, E. & ZÁRATE, D. A. 2010. Secondary seed dispersal by dung beetles in a Colombian rain forest: effects of dung type and defecation pattern on seed fate. Journal of Tropical Ecology 26:355364.CrossRefGoogle Scholar
SIMPSON, R. L., LECK, M. A. & PARKER, V. T. 1989. Seed banks: general concepts and methodological issues. Pp. 38 in Leck, M. A., Parker, V. T. & Simpson, R. L. (eds). Ecology of soil seed banks. Academic Press, San Diego.CrossRefGoogle Scholar
SKOGLUND, J. 1992. The role of seed banks in vegetation dynamics and restoration of dry tropical ecosystems. Journal of Vegetation Science 3:357360.CrossRefGoogle Scholar
THOMPSON, K. 2000. The functional ecology of soil seed banks. Pp. 215235 in Fenner, M. (ed.). Seeds: the ecology of regeneration in plant communities. CABI Publishing, Wallingford.CrossRefGoogle Scholar
VANDER WALL, S. B., FORGET, P.-M., LAMBERT, J. & HULME, P. 2005. Seed fate pathways: filling the gap between parent and offspring. Pp. 18 in Forget, P.-M., Lambert, J., Hulme, P. & Vander Wall, S. B. (eds). Seed fate: predation, dispersal and seedling establishment. CABI Publishing, Wallingford.Google Scholar
WANG, Y., JIANG, D., TOSHIO, O. & ZHOU, Q. 2013. Recent advances in soil seed bank research. Contemporary Problems of Ecology 6:520524.CrossRefGoogle Scholar