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Soil disturbance by vertebrates alters seed predation, movement and germination in an African rain forest

Published online by Cambridge University Press:  30 September 2011

Amy E. Dunham*
Affiliation:
Ecology and Evolutionary Biology Department, Stony Brook University, Stony Brook, NY 11794, USA

Abstract:

Biopedturbation, or animal-caused soil disturbance, may be important for development and maintenance of small-scale heterogeneity in ecosystems with the potential to alter seed mortality and recruitment. However, its role in tropical forests has been largely ignored. This study explored effects of vertebrate biopedturbation on seed (1) microsite heterogeneity, (2) predation and (3) germination in a West African rain forest. Exclosure experiments were used to study how biopedturbation altered burial and movements of seeds of four common canopy species. Effect of seed burial on removal by seed predators was also examined. Germination of the dominant canopy species (Raphia palma-pinus) in swamp forest was tested within artificial disturbances mimicking that of a locally common but endangered mammal, the Liberian mongoose (Liberiictis kuhni), which was estimated to turn over the entire forest floor in this habitat in c. 8 mo. Seed exposure to biopedturbation for 20 d (n = 80) led to an overall 6.5-fold increase in small-scale horizontal movement and increased probability of burial (6–52% higher), varying by species. Burial effectively eliminated seed removal for all four species (n = 160) by seed predators over 20 d. Germination of Raphia palma-pinus seeds (n = 100) was enhanced by 17.5% on average over 4 mo in simulated disturbances. Results suggest biopedturbation may be important for seedling recruitment and that loss of species with this functional role could have underappreciated yet important impacts on tropical plant communities.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2011

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References

LITERATURE CITED

ASHTON, D. H. & BASSETT, O. D. 1997. The effects of foraging by the superb lyrebird (Menura novae-hollandiae) in Eucalyptus regnans forests at Beenak, Victoria. Australian Journal of Ecology 22:383394.CrossRefGoogle Scholar
BENITEZ-MALVIDO, J. & KOSSMANN-FERRAZ, I. D. 1999. Litter cover variability affects seedling performance and herbivory. Biotropica 31:598606.CrossRefGoogle Scholar
BORCHERT, M. I., DAVIS, F. W., MICHAELSEN, J. & OYLER, L. D. 1989. Interactions of factors affecting seedling recruitment of blue oak (Quercus douglasii) in California. Ecology 70:389404.CrossRefGoogle Scholar
BRASHARES, J. S., ARCESE, P., SAM, M. K., COPPOLILLO, P. B., SINCLAIR, A. R. E. & BALMFORD, A. 2004. Bushmeat hunting, wildlife declines, and fish supply in West Africa. Science 306:1180.CrossRefGoogle ScholarPubMed
BREYTENBACH, G. J. & SKINNER, J. D. 1982. Diet, feeding and habitat utilization by bushpigs Potamochoerus porcus Linnaeus. South African Journal of Wildlife Research 12:17.Google Scholar
BUSTAMANTE, R. O. & SIMONETTI, J. 2000. Seed predation and seedling recruitment in plants: the effect of the distance between parents. Plant Ecology 147:173183.CrossRefGoogle Scholar
CERABOLINI, B., CERIANI, R. M., CACCIANIGA, M., DE ANDREIS, R. & RAIMONDI, B. 2003. Seed size, shape and persistence in soil: a test on Italian flora from Alps to Mediterranean coasts. Seed Science Research 13:7585.CrossRefGoogle Scholar
CHAMBERS, J. C. & MACMAHON, J. A. 1994. A day in the life of a seed: movements and fates of seeds and their implications for natural and managed systems. Annual Review of Ecology and Systematics 25:263292.CrossRefGoogle Scholar
CHAPMAN, C. A. & CHAPMAN, L. J. 1996. Frugivory and the fate of dispersed and non-dispersed seeds of six African tree species. Journal of Tropical Ecology 12:491504.CrossRefGoogle Scholar
CHRISTIAN, C. E. & STANTON, M. L. 2004. Cryptic consequences of a dispersal mutualism: seed burial, elaiosome removal, and seed-bank dynamics. Ecology 85:11011110.CrossRefGoogle Scholar
CINTRA, R. 1997. Leaf litter effects on seed and seedling predation of the palm Astrocaryum murumuru and in the legume tree Dipteryx micrantha in Amazonia forest. Journal of Tropical Ecology 13:709725.CrossRefGoogle Scholar
CLARK, C. J., POULSEN, J. R., BOLKER, B. M., CONNOR, E. F. & PARKER, V. T. 2005. Comparative seed shadows of bird-, monkey and wind-dispersed trees. Ecology 86:26842694.CrossRefGoogle Scholar
CLARK, D. B. & CLARK, D. A. 1985. Seedling dynamics of a tropical tree: Impacts of herbivory and meristem damage. Ecology 66:18841892.CrossRefGoogle 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. Centre for Agricultural Publishing and Documentation. PUDOC, Wageningen.Google Scholar
CORDEIRO, N. J. & HOWE, H. F. 2001. Low recruitment of trees dispersed by animals in African forest fragments. Conservation Biology 15:17331741.CrossRefGoogle Scholar
DALLING, J. W., SWAINE, M. D. & GARWOOD, N. C. 1997. Soil seed bank community dynamics in seasonally moist lowland tropical forest, Panama. Journal of Tropical Ecology 13:659680.CrossRefGoogle Scholar
DUNHAM, A. E. 2004. Herpestidae; mongooses & fossa. Pp. 347358 in Grzimek, B., Schlager, N., Olendorf, M. & McDade, C. (eds.). Grzimek's animal life encyclopedia. (Second edition). Volume 14. Thomson Gale, New York.Google Scholar
DUNHAM, A. E. 2008. Above and below ground impacts of terrestrial mammals and birds in a tropical forest. Oikos 117:571579.CrossRefGoogle Scholar
ELDRIDGE, D. J. & JAMES, A. I. 2009. Soil-disturbance by native animals plays a critical role in maintaining healthy Australian landscapes. Ecological Management and Restoration 10:S27S34.CrossRefGoogle Scholar
GARCIA-GUZMAN, G. & BENITEZ-MALVIDO, J. 2003. Effect of litter on the incidence of leaf-fungal pathogens and herbivory in seedlings of the tropical tree, Nectandra ambigens. Journal of Tropical Ecology 19:171177.CrossRefGoogle Scholar
GARCIA-ORTH, X. & MARTINEZ-RAMOS, M. 2008. Seed dynamics of early and late successional tree species in tropical abandoned pastures: seed burial as a way of evading predation. Restoration Ecology 16:435443.CrossRefGoogle Scholar
GREEN, P. T. 1999. Seed germination in Chrysophyllum sp. nov., a large-seeded rainforest species in north Queensland: effects of seed size, litter depth and seed position. Australian Journal of Ecology 24:608613.CrossRefGoogle Scholar
GRUBB, P. J. 1977. The maintenance of species-richness in plant communities: the importance of the regeneration niche. Biological Review 52:107145.CrossRefGoogle Scholar
GUZMAN-GRAJALES, S. M. & WALKER, L. R. 1991. Differential seedling responses to litter after hurricane Hugo in the Luquillo Experimental Forest, Puerto Rico. Biotropica 23:407413.CrossRefGoogle Scholar
HULME, P. E. 1998. Post-dispersal seed predation and seed bank persistence. Seed Science Research 8:513519.CrossRefGoogle Scholar
HULME, P. E. & BORELLI, T. 1999. Variability in post-dispersal seed predation in deciduous woodland: relative importance of location, seed species, burial and density. Plant Ecology 145:149156.CrossRefGoogle Scholar
JANZEN, D. H. 1970. Herbivores and the number of tree species in tropical forests. American Naturalist 104:501528.CrossRefGoogle Scholar
JEFFREY, S. 2009. How Liberia uses wildlife. Oryx 14:168173.CrossRefGoogle Scholar
JONES, C. G., LAWTON, J. H. & SHACHAK, M. 1994. Organisms as ecosystem engineers. Oikos 69:373386.CrossRefGoogle Scholar
JORDANO, P., GARCÍA, C., GODOY, J. A. & GARCÍA-CASTAÑO, J. L. 2007. Differential contribution of frugivores to complex seed dispersal patterns. Proceedings of the National Academy of Sciences USA 104:32783282.CrossRefGoogle ScholarPubMed
KONÉ, I., LAMBERT, J. E., REFISCH, J. & BAKAYOKO, A. 2008. Primate seed dispersal and its potential role in maintaining useful tree species in the Taï region, Côte-d'Ivoire: implications for the conservation of forest fragments. Tropical Conservation Science 1:293306.CrossRefGoogle Scholar
LAWTON, J. H. 1994. What do species do in ecosystems? Oikos 71:367374.CrossRefGoogle Scholar
LOPEZ, L. & TERBORGH, J. 2007. Seed predation and seedling herbivory as factors in tree recruitment failure on predator-free forested islands. Journal of Tropical Ecology 23:129137.CrossRefGoogle Scholar
MARI, L., CASAGRANDI, R., GATTO, M., AVGAR, T. & NATHAN, R. 2008. Movement strategies of seed predators as determinants of plant recruitment patterns. American Naturalist 172:694711.CrossRefGoogle ScholarPubMed
MARTIN, G. 2003. The role of small ground-foraging mammals in topsoil health and biodiversity: implications to management and restoration. Ecological Management and Restoration 4:114119.CrossRefGoogle Scholar
MOLOFSKY, J. & AUGSPURGER, C. K. 1992. The effect of leaf litter on early seedling establishment in a tropical forest. Ecology 73:6877.CrossRefGoogle Scholar
NILSON, M. E. & HJALTEN, J. 2003. Covering pine-seeds immediately after seeding: effects on seedling emergence and on mortality through seed-predation. Forest Ecology and Management 176:449457.CrossRefGoogle Scholar
ODUOR, A. M. O., GÓMEZ, J. M. & STRAUSS, S. Y. 2010. Exotic vertebrate and invertebrate herbivores differ in their impacts on native and exotic plants: a meta-analysis. Biological Invasions 12:407419.CrossRefGoogle Scholar
POULSEN, J. R., CLARK, C. J., CONNOR, E. F. & SMITH, T. B. 2002. Differential resource use by primates and hornbills: Implications for seed dispersal. Ecology 83:228240.CrossRefGoogle Scholar
REICHMAN, O. J. 1984. Spatial and temporal variation of seed distributions in Sonoran Desert soils. Journal of Biogeography 11:111.CrossRefGoogle Scholar
SEKERCIOGLU, Ç. H., EHRLICH, P. R., DAILY, G. C., AYGEN, D., GOEHRING, D. & SANDI, R. F. 2001. Disappearance of insectivorous birds from tropical forest fragments. Proceedings of the National Academy of Sciences USA 99:263267.CrossRefGoogle Scholar
SHULTZ, S. 2002. Population density, breeding chronology and diet of crowned eagles Stephanoaetus coronatus in Taï National Park, Ivory Coast. Ibis 144:135138.CrossRefGoogle Scholar
SILMAN, M. R., TERBORGH, J. W. & KILTIE, R. A. 2003. Population regulation of a dominant-rain forest tree by a major seed-predator. Ecology 84:431438.CrossRefGoogle Scholar
SOKAL, R. R. & ROHLF, F. J. 1995. Biometry: The principles and practice of statistics in biological research. Freeman and Company, New York. 880 pp.Google Scholar
TAYLOR, M. & DUNHAM, A. E. in press. Liberian mongoose, Liberiictis kuhni. in Kingdon, J. & Butynski, T. (eds.). The mammals of Africa. Volume 4. (Order Carnivora, Pinnipedia, Pholidota, Tubulidentata, Hyracoidea, Proboscidea, Sirenia, Perissodactyla). Academic Press, Amsterdam.Google Scholar
TAYLOR, M. E. 1992. New records of two species of rare viverrids from Liberia. Oryx 26:103106.CrossRefGoogle Scholar
THEIMER, T. C. & GEHRING, C. A. 1999. Effects of litter-disturbing bird species on tree seedling germination and survival in an Australian tropical rain forest. Journal of Tropical Ecology 15:737749.CrossRefGoogle Scholar
THOMPSON, K., JALILI, A., HODGSON, J. G., HAMZEH'EE, B., ASRI, Y., SHAW, S., SHIRVANY, A., YAZDANI, S., KHOSHNEVIS, M. & ZARRINKAMAR, F. 2001. Seed size, shape and persistence in the soil in an Iranian flora. Seed Science Research 11:345355.Google Scholar
UNEP 2007. World Heritage Sites: Taï National Park. UNEP, World Conservation Monitoring Center, Protected Areas Programme Report, Cambridge. 9 pp.Google Scholar
WRIGHT, J. P. & JONES, C. G. 2006. The concept of organisms as ecosystem engineers ten years on: progress, limitations, and challenges. Bioscience 56:203209.CrossRefGoogle Scholar