Abstract
Seed dispersal by frugivores in tropical rain forests is important for maintaining viable tree populations. Over the years, vertebrate assemblages in tropical forests have been altered by anthropogenic disturbances, leading to concerns about the ability of remnant vertebrates to substitute for the lost or declining vertebrate populations. We compared vertebrate composition and frugivore visitation rates as an indirect measure of rate of seed dispersal in three tropical rain forests in Uganda, namely Mabira, Budongo and Kibale Forests. Mabira is highly disturbed, Kibale is little and Budongo is intermediate. The aim was to determine whether vertebrate assemblages in differentially disturbed forests had comparable abilities to disperse seeds and whether tree species were equally vulnerable to loss of seed dispersers. Assemblages of forest generalist species were similar in all forests, but specialists were less abundant in the heavily disturbed forest. Remnant frugivores in the heavily disturbed forest were mainly small-bodied species that spat seeds beneath fruiting trees compared to large-bodied species observed in the less disturbed forests that ingested and carried away the seeds. We postulate that the quantity of seeds dispersed in heavily disturbed forests is much reduced due to low visitation rates of frugivores and the absence of large frugivores that consume large quantities of fruit. The quality of seed dispersal is affected as well by the distance over which seeds are moved. Assessment of vulnerability of trees shows no evidence for disperser substitution for trees producing large fruits. Fruit trees with low nutritional contents and digestibility were least visited in frugivore-impoverished forests. The loss of large specialist frugivores is likely to affect recruitment of many trees, especially of species that cannot establish beneath adult conspecifics.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Babweteera F, Savill P, Brown N (2007) Balanites wilsoniana: regeneration with and without elephants. Biol Conserv 134:40–47. doi:10.1016/j.biocon.2006.08.002
Bas JM, Pons P, Gomez C (2006) Exclusive frugivory and seed dispersal of Rhamnus alaternus in the bird breeding season. Plant Ecol 183:77–89. doi:10.1007/s11258-005-9008-0
Basuta IG, Kasenene JM (1987) Small rodent populations in selectively felled and mature tracts of Kibale Forest, Uganda. Biotropica 19:260–266. doi:10.2307/2388345
Bennun L, Dranzoa C, Pomeroy D (1996) The forest birds of Kenya and Uganda. J East Afr Nat Hist 85:23–48. doi:10.2982/0012-8317(1996)85[23:TFBOKA]2.0.CO;2
Bollen A, Van Elsacker L, Ganzhorn JU (2004) Relations between fruits and disperser assemblages in a Malagasy littoral forest: a community-level approach. J Trop Ecol 20:599–612. doi:10.1017/S0266467404001853
Carbone C et al (2001) The use of photographic rates to estimate densities of tigers and other cryptic mammals. Anim Conserv 4:75–79. doi:10.1017/S1367943001001081
Chapman LJ, Chapman CA, Wrangham RW (1992) Balanites wilsoniana—elephant dependent dispersal. J Trop Ecol 8:275–283
Chapman CA, Wrangham RW, Chapman LJ, Kennard DK, Zanne AE (1999) Fruit and flower phenology at two sites in Kibale National Park, Uganda. J Trop Ecol 15:189–211. doi:10.1017/S0266467499000759
Clarke KR (1993) Nonparametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143. doi:10.1111/j.1442-9993.1993.tb00438.x
Colwell RK (2005) EstimateS: statistical estimation of species richness and shared species from samples. V 7.5
Colwell RK, Coddington JA (1994) Estimating terrestrial biodiversity through extrapolation. Philos Trans R Soc Lond B Biol Sci 345:101–118. doi:10.1098/rstb.1994.0091
Cordeiro NJ, Howe HF (2001) Low recruitment of trees dispersed by animals in African forest fragments. Conserv Biol 15:1733–1741. doi:10.1046/j.1523-1739.2001.99579.x
Corlett RT (1996) Characteristics of vertebrate-dispersed fruits in Hong Kong. J Trop Ecol 12:819–833
da Silva JMC, Tabarelli M (2000) Tree species impoverishment and the future flora of the Atlantic forest of northeast Brazil. Nature 404:72–74. doi:10.1038/35003563
Dranzoa C (1998) The avifauna 23 years after logging in Kibale National park, Uganda. Biodivers Conserv 7:777–797. doi:10.1023/A:1008892419940
Fa JE, Ryan SF, Bell DJ (2005) Hunting vulnerability, ecological characteristics and harvest rates of bushmeat species in afrotropical forests. Biol Conserv 121:167–176. doi:10.1016/j.biocon.2004.04.016
Fenner M, Thompson K (2005) The ecology of seeds. Cambridge University Press, Cambridge
Fleming TH (1979) Do tropical frugivores compete for food? Am Zool 19:1157–1172
Forget PM (1990) Seed-dispersal of Vouacapoua americana (Caesalpiniaceae) by caviomorph rodents in French Guiana. J Trop Ecol 6:459–468
French AR, Smith TB (2005) Importance of body size in determining dominance hierarchies among diverse tropical frugivores. Biotropica 37:96–101
Fry CH, Keith S (2004) The birds of Africa, vol VII. Christopher Helm, London
Fry CH, Keith S, Urban EK (1988) The birds of Africa, vol III. Academic Press, London
Fry CH, Keith S, Urban EK (2000) The birds of Africa, vol VI. Academic Press, London
Gautier-Hion A et al (1985) Fruit characters as a basis of fruit choice and seed dispersal in a tropical forest vertebrate community. Oecologia 65:324–337. doi:10.1007/BF00378906
Githiru M, Lens L, Bennur LA, Ogol C (2002) Effects of site and fruit size on the composition of avian frugivore assemblages in a fragmented Afrotropical forest. Oikos 96:320–330. doi:10.1034/j.1600-0706.2002.960214.x
Hamilton A (1991) A field guide to Uganda forest trees. Makerere University Printery, Kampala
Hardesty BD, Hubbell SP, Bermingham E (2006) Genetic evidence of frequent long-distance recruitment in a vertebrate-dispersed tree. Ecol Lett 9:516–525. doi:10.1111/j.1461-0248.2006.00897.x
Howard PC (1991) Nature conservation in Uganda’s tropical forest reserves. IUCN, Gland
Howe HF, Miriti MN (2000) No question: seed dispersal matters. Trends Ecol Evol 15:434–436. doi:10.1016/S0169-5347(00)01965-0
Howe HF, Smallwood J (1982) Ecology of seed dispersal. Annu Rev Ecol Syst 13:201–228. doi:10.1146/annurev.es.13.110182.001221
Hulme PE (1998) Post-dispersal seed predation and seed bank persistence. Seed Sci Res 8:513–519. doi:10.1017/S0960258500004487
Karani P, Kiwanuka LS, Sizomu-Kagolo ME (1997) Forest management plan for Budongo Forest Reserve July 1997–June 2007. Uganda Forest Department, Kampala
Kasenene JM (1987) The influence of mechanised selective logging, felling intensity and gap size on the vegetation of tropical moist forest reserve, Uganda. PhD Dissertation, Michigan State University, USA
Keith S, Urban EK, Fry CH (1992) The birds of Africa, vol IV. Academic Press, London
Kingdon J (1997) The Kingdon guide to African mammals. Academic Press, London
Laidlaw RK (2000) Effects of habitat disturbance and protected areas on mammals of peninsular Malaysia. Conserv Biol 14:1639–1648. doi:10.1046/j.1523-1739.2000.99073.x
Lambert JE (1998) Primate digestion: interactions among anatomy, physiology, and feeding ecology. Evol Anthropol 7:8–20. doi:10.1002/(SICI)1520-6505(1998)7:1<8::AID-EVAN3>3.0.CO;2-C
Lambert JE (1999) Seed handling in chimpanzees (Pan troglodytes) and red tail monkeys (Cercopithecus ascanius): implications for understanding hominoid and cercopithecine fruit-processing strategies and seed dispersal. Am J Phys Anthropol 109:365–386. doi:10.1002/(SICI)1096-8644(199907)109:3<365::AID-AJPA6>3.0.CO;2-Q
Laurance WF (1998) Forest fragmentation: another perspective. Trends Ecol Evol 13:75. doi:10.1016/S0169-5347(97)01310-4
MacArthur RH, Diamond JM, Karr JR (1972) Density compensation in island faunas. Ecology 53:330–342. doi:10.2307/1934090
Manasse RS, Howe HF (1983) Competition for dispersal agents among tropical trees: influences of neighbors. Oecologia 59:185–190. doi:10.1007/BF00378836
Manga TT, Fondoun JM, Kengue J, Thiengang C (2000) Chemical composition of Ricinodendron heudelontii: an indigenous fruit tree in southern Cameroon. Afr Crop Sci J 8:195–201
Moles AT, Westoby M (2006) Seed size and plant strategy across the whole life cycle. Oikos 113:91–105. doi:10.1111/j.0030-1299.2006.14194.x
Palmer MW (1990) The estimation of species richness by extrapolation. Ecology 71:1195–1198. doi:10.2307/1937387
Pimm SL, Jones HL, Diamond J (1988) On the risk of extinction. Am Nat 132:757–785. doi:10.1086/284889
Plumptre AJ (1996) Changes following 60 years of selective timber harvesting in the Budongo Forest Reserve, Uganda. For Ecol Manage 89:101–113. doi:10.1016/S0378-1127(96)03854-6
Plumptre A, Cox D (2006) Counting primates for conservation: primate surveys in Uganda. Primates 47:65–73. doi:10.1007/s10329-005-0146-8
Plumptre AJ, Reynolds V (1994) The effect of selective logging on the primate populations in the Budongo Forest Reserve, Uganda. J Appl Ecol 31:631–641. doi:10.2307/2404154
Plumptre A, Reynolds V, Bakuneeta C (1994) The contribution of fruit eating primates to seed dispersal and natural regeneration after selective logging. Final report to ODA. R4738. Budongo Forest Project, Oxford
Saracco JF, Collazo JA, Groom MJ, Carlo TA (2005) Crop size and fruit neighborhood effects on bird visitation to fruiting Schefflera morototoni trees in Puerto Rico. Biotropica 37:81–87
Seaby RMH, Henderson PA (2004) Community Analysis Package. 3.0. Pisces Conservation Ltd
Silveira L, Jacomo ATA, Diniz-Filho JAF (2003) Camera trap, line transect census and track surveys: a comparative evaluation. Biol Conserv 114:351–355. doi:10.1016/S0006-3207(03)00063-6
Stanford A (2000) Rodent ecology and seed predation in logged and unlogged forest, Uganda. DPhil Dissertation, University of Bristol
Urban EK, Fry CH, Keith S (1986) The birds of Africa, vol II. Academic Press, London
Urban EK, Fry CH, Keith S (1997) The birds of Africa, vol V. Academic Press, London
Westman WE, Strong LL, Wilco BA (1989) Tropical deforestation and species endangerment: the role of remote sensing. Landsc Ecol 3:97–109. doi:10.1007/BF00131173
Acknowledgments
This research was supported by an International Foundation for Science (IFS) grant. We are grateful to G. Erickson and E. Orijabo, who assisted with the field work. Permission to conduct this research was kindly granted by Uganda National Council for Science and Technology, Uganda Wildlife Authority and National Forestry Authority.
Author information
Authors and Affiliations
Corresponding author
Appendix
Appendix
See Table 5.
Rights and permissions
About this article
Cite this article
Babweteera, F., Brown, N. Can remnant frugivore species effectively disperse tree seeds in secondary tropical rain forests?. Biodivers Conserv 18, 1611–1627 (2009). https://doi.org/10.1007/s10531-008-9546-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10531-008-9546-6