primate frugivory in kibale national park, uganda, and its implications for human use of forest...
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Afr. J. Ecol. 1998, Volume 36, pages 234–240
Primate frugivory in Kibale National Park, Uganda, and itsimplications for human use of forest resources
JOANNA E. LAMBERT
Department of Zoology, University of Florida, Gainesville, U.S.A.
Summary
In an attempt to understand the practical and/or economic implications of primateseed dispersal, it was established which seed species are dispersed by frugivorousprimates in Kibale National Park, Uganda, and which of this sort of species wereused by Ugandan people. A list of fruit species consumed by Kibale primates wascompiled using primary data and by reviewing all known published accounts of theirfruit diet. Primates consume the fruit of 87 Kibale forest tree species; the seeds of11% of these species are destroyed by the primates. The remaining 77 species aredispersed by either one, two, three or all four of the frugivorous Kibale primates.Of these 77 species, 42% have some utility to local Ugandan inhabitants, suggestingthat maintaining populations of primates is important not only for natural forestregeneration, but also for human habitat use. This report illustrates the complexityof the seed dispersal process and suggests links not only between plants and theirdispersers, but also between sets of plants/dispersers and the human populationsthat rely on forest resources.
Key words: conservation, feeding, forest regeneration, seed dispersal
Resume
Afin de comprendre les implications pratiques et/ou economiques de la dispersiondes semences par les primates, on a montre quelles especes de semences sont disperseespar les primates frugivores du Parc National de Kibale, en Ouganda, et quellesespeces parmi celles-la etaient utilisees par les Ougandais. On a etabli une liste desespeces a fruits consommees par les primates, en se servant de donnees de base eten revisant tous les rapports connus publies sur leur regime de frugivores. Lesprimates mangent les fruits de 87 especes d’arbres de la foret de Kibale; les semencesde 11% de ces especes sont detruites par les primates. Les 77 especes restantes sontdispersees par un, deux, trois ou les quatre especes de primates frugivores de Kibale.De ces 77 especes, 42% sont de quelque utilite pour les habitants de la region, cequi signifie que le maintien des populations de primates est important non seulementpour la regeneration naturelle de la foret, mais aussi pour l’utilisation humaine del’habitat. Ce rapport revele d’une part la complexite du processus de dispersion dessemences et, d’autre part, les liens non seulement entre les plantes et ceux qui les
Correspondence: Joanna E. Lambert, Department of Sociology and Anthropology, Southwest MissouriState University, Springfield, Missouri 65804, U.S.A. E-mail: [email protected]
1998 East African Wild Life Society.
Primate frugivory and forest resources 235
dispersent mais aussi entre cet ensemble et les populations humaines qui dependentdes ressources de la foret.
Introduction
The ecological impact of primate seed dispersal continues to be recognized andevaluated in the wild. From this research, it is becoming increasingly evident thatmonkeys and apes are important dispersers for a variety of plant species, in numeroushabitats, and on all continents where primates are found (e.g. Galdikas, 1982; Garber,1986; Chapman, 1989; Wrangham, Chapman & Chapman, 1994; Julliot, 1996;Lambert, 1997). However, despite a recent surge in academic interest in the ecologicalimpact of primates on forest community dynamics, the economic or practicalimplications of primate seed dispersal remain to be demonstrated fully. An exceptionis the recent report by Bakuneeta et al. (1995) which has shown that a large numberof the species whose seeds are dispersed by chimpanzees (Pan troglodytes Blumenbach)in Budongo Forest, Uganda, have some economic or cultural value to people livingin areas surrounding this forest. As suggested by these authors, such data are criticalin the building of sound conservation and management plans for forest habitats.Building on their earlier report, the goal of this paper is to add to the list of humanuses of primate-dispersed tree species, and thereby contribute to our appreciationof the practical implications of primate seed dispersal. This is accomplished bydetermining which seed species are dispersed, rather than destroyed, by frugivorousprimates in Kibale National Park, Uganda, and then evaluating this subset of seedspecies in light of known functions of trees used by Ugandan people.
Methods
An exhaustive list of all fruit species known to be consumed by Kibale primates wascompiled using data collected by the author during 1993 and 1994, and by reviewingall known published accounts of the fruit diet of Kibale forest primates (includingreports in Waser, 1975, 1977; Rudran, 1978; Struhsaker, 1978; Ghiglieri, 1984;Isabirye-Basuta, 1989; Wrangham et al., 1993, 1994; Oliput, 1994; Chapman &Chapman, 1996). Particular attention was paid to the ways in which redtail monkeys(Cercopithecus ascanius Audebert), blue monkeys (Cercopithecus mitis Wolf), grey-cheeked mangabeys (Cercocebus albigena Lydekker) and chimpanzees were observedand are reported to process fruit and handle seeds. Seed-handling behaviour wascategorized as either spit, swallow or destroy; seeds that were either spat out orswallowed were considered to have been dispersed by the primates, whereas thoseseeds that were destroyed by the primates were considered dead and therefore notdispersed. Dung was also collected opportunistically during 1993–94 and sieved forseeds, which were then identified using the Makerere University Biological FieldStation seed collection. From direct field observations, dung samples and publishedaccounts, a list of seed-handling techniques by these four frugivorous primates wascompiled and evaluated to determine whether seed species were dispersed or destroyedduring feeding. The human use of plant species whose seeds are dispersed by Kibaleprimates was then evaluated by examining reports published in Katende, Birnie &Tengnas (1995).
East African Wild Life Society, Afr. J. Ecol., 36, 234–240
236 Joanna E. LambertTa
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East African Wild Life Society, Afr. J. Ecol., 36, 234–240
Primate frugivory and forest resources 237Te
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East African Wild Life Society, Afr. J. Ecol., 36, 234–240
238 Joanna E. Lambert
Results
During 1993–94, frugivorous primates were observed to consume the fruit of 39Kibale forest tree species. Published accounts added another 48 species to this list.Of this set of 87 fruit species, 10 (11%) were destroyed by the primates, either becauseseeds were broken open and the endosperm purposely consumed, or because seedswere broken open in the process of consuming fruit pulp. The remaining 77 specieswere dispersed by either one, two, three or all four of the frugivorous primate speciesof Kibale. This dispersal either took place via swallowing the seeds and defaecatingthem out some distance away from the parent tree, or, in the case of the cer-copithecines, through cheek-pouching fruit and spitting out unwanted seeds somedistance away from where fruits were removed.
Of the 77 fruiting forest tree species that are dispersed by Kibale primates, 32(42%) were found to have some utility to local Ugandan inhabitants. Table 1 outlinesthe subset of species that are both dispersed by primates and have some economic/cultural value. The categories employed here are those of Katende et al. (1995), andinclude ‘Wood‘, ‘Food‘, ‘Fodder’, ‘Environmental’ and ‘Other’ uses. By far the mostcommon use of these 77 seed species was ‘Wood’ use; indeed, 29 of these species(91%) are used for either firewood, timber, charcoal, furniture, posts, carvings orutensils. The next most common use was ‘Environmental’, with 25 (78%) of thesespecies being used for purposes such as shade, soil conservation and mulch. Fifteen(47%) of the tree species have resources that fall under the category of ‘Food‘,including medicine, six (19%) are used for ‘Fodder’ and nine (28%) are used forvarious ‘Other’ purposes, including both functional and ceremonial uses.
Discussion
A total of 216 species of forest trees are reported to occur in Kibale (Hamilton,1981; Howard, 1991). Of these forest trees, more than a third (77/216=37%) haveseeds that are dispersed by the four primate species discussed here. Clearly, manyseeds are moved by these frugivores. For example, Lambert (1997) has reportedthat, in a single day, Kibale monkeys can disperse the seeds of up to≈33, 800 fruitskm−2 and chimpanzees up to 1400 fruits km−2 − a large number of fruits whichmay have ecological consequences for forest regeneration dynamics and tree speciesreproduction. In a recent review, Chapman (1995) pointed out that larger-bodiedmammals, such as primates, may be particularly important seed dispersers, and thatit is these same animals that are often most vulnerable to hunting or habitat loss.Although the primates of Kibale National Park are protected, most primates arenot. In fact, 90% of African primates live outside protected areas, and only anaverage of 3.2% of African closed-canopy forests are protected in parks or reserves(IUCN, 1985; Rose & Ammann, 1997). A decline in frugivorous primate populationsmay have deleterious consequences for forest regeneration and/or tree species com-position. Indeed, in an evaluation of seedling recruitment in the protected Kibaleforest interior with intact primate populations, compared with that in forest fragmentswhere primate populations have been severely reduced, Chapman & Onderdonk(1998) found that the fragments had lower seedling density and fewer species ofseedlings than the forest. This suggests a cost of losing primates which extendsbeyond the loss of the animals themselves.
East African Wild Life Society, Afr. J. Ecol., 36, 234–240
Primate frugivory and forest resources 239
In addition to the ecological importance of seed dispersal, many primate-dispersedplant species have some economic and/or cultural value to Ugandan people. Thissuggests that maintaining populations of primates is important not only for naturalforest regeneration, but also for human habitat use. Protection of primates and theseed dispersal system outside protected areas is particularly relevant in this context,since it is in these areas where primates are most at risk, and also where people areallowed to exploit forest resources. Bakuneeta et al. (1995) suggest that forestmanagement schemes should strive to ensure that some portion of mature stems ofimportant human-used trees remain untouched during logging plans. Indeed, theprotection of primate populations to ensure successful movement of seeds (par-ticularly those demonstrated to recruit successfully after primate dispersal), as wellas an informed logging regime, are of critical importance not only in preservingnatural processes of forest regeneration, but also to help protect natural resourcesused by humans. This report illustrates the complexity of the seed dispersal dynamic,and indicates links not only between the plant species and the dispersers themselves,but also between sets of plants/dispersers and the human populations that rely onforest, forest edge, and forest fragment habitats. The conservation of primate speciesis a critically important goal in itself, but in working to ensure their protection, weprotect indirectly the seed dispersal of important human resources as well.
Acknowledgements
For permission to work in Uganda, I thank the Office of the President, the UgandaNational Council for Science and Technology, and the Uganda Forestry Department.I thank Gilbert Isabirye-Basuta and John Kasenene for facilitating my work andfor allowing me to conduct research at the Makerere University Biological FieldStation. This study was supported in part by a Makerere University Grant forBiological Research, a Sigma Xi Grant-in-Aid of Research, a University of IllinoisGraduate School Fellowship, and a University of Illinois Thesis Support Grant. Iwould like to thank Stephen Wooten and Daphne Onderdonk for their insightfuland critical comments on this paper, and Colin Chapman for guidance and supportin the study of conservation and seed dispersal.
References
B, C., J, K., P, R. & R, V. (1995) Human uses of tree species whoseseeds are dispersed by chimpanzees in the Budongo Forest, Uganda. Afr. J. Ecol. 33, 276–278.
C, C.A. (1989) Primate seed dispersal: the fate of dispersed seeds. Biotropica 21, 148– 154.C, C.A. (1995) Primate seed dispersal: coevolution and conservation implications. Evol. Anthropol.
4, 74–82.C, C.A. & C, L.J. (1996) Frugivory and the fate of dispersed and non-dispersed seeds of
six African tree species. J. trop. Ecol. 12, 491–504.C, C.A. & O, D. (1998) Forests without primates: primate/plant codependency. Am.
J. Primatol. 45, 127–141.G, B.M. (1982) Orang utans as seed dispersers at Tanjung Puting, Central Kalimantan: implications
for conservation. In: The Orang Utan: its Biology and Conservation (Ed. L.E.M. Boer). W. JunkPublishers, The Hague.
G, P.A. (1986) The ecology of seed dispersal in two species of Callitrichid primates (Saguinus mystaxand Saguinus fuscicollis). Am. J. Primatol. 10, 155–170.
East African Wild Life Society, Afr. J. Ecol., 36, 234–240
240 Joanna E. Lambert
G, M. (1984) The Chimpanzees of Kibale Forest. Columbia University Press, New York.H, A. (1981) A Field Guide to Uganda Forest Trees. Kampala, Makerere University Press,
Kampala.H, P.C. (1991) Nature Conservation in Uganda’s Tropical Forest Reserves. The IUCN Tropical
Forest Programme, Cambridge.I-B, G. (1989) Feeding ecology of chimpanzees in the Kibale Forest, Uganda. In: Under-
standing Chimpanzees (Eds P.N. Heltne and L. Marquardt). Harvard University Press, Cambridge.I (1985) United Nations List of National Parks and Protected Areas. IUCN, Gland, Switzerland.J, C. (1996) Seed dispersal by red howling monkeys (Alouatta seniculus) in the tropical rainforest
of French Guiana. Int. J. Primatol. 17, 239–258.K, A.B., B, A. & T, B. (1995) Useful Trees and Shrubs for Uganda. Regional Soil
Conservation Unit, Nairobi, Kenya.L, J.E. (1997) Digestive Strategies, Fruit Processing, and Seed Dispersal in the Chimpanzees (Pan
troglodytes) and Redtail Monkeys (Cercopithecus ascanius) of Kibale National Park, Uganda. PhDDissertation. University of Illinois, Urbana-Champaign.
O, W. (1994) Ranging Patterns of the Grey-Cheeked Mangabey (Cercocebus albigena) with SpecialReferences to Food Finding and Food Availability in Kibale National Park. MSc. Thesis. MakerereUniversity, Kampala, Uganda.
R, A.L. & A, K. (1997) The African primate bushmeat crisis (abstract). Am. J. Primatol. 42,89–90.
R, R. (1978) Socioecology of the Blue Monkeys of the Kibale Forest, Uganda. SmithsonianContribution to Zoology 249. Smithsonian Institution Press, Washington, DC.
S, T.T. (1978) Food habits of five monkey species in the Kibale Forest, Uganda. In: RecentAdvances in Primatology (Vol. 2): Conservation (Eds D.J. Chivers and J. Herbert). Academic Press,London.
W, P.M. (1975) Monthly variation in feeding and activity patterns of the mangabey, Cercocebusalbigena (Lydekker). E. Afr. Wildl. J. 13, 249–263.
W, P.M. (1977) Mangabey feeding, movements, and group size. In: Primate Ecology. (Ed. T.H.Clutton-Brock). Academic Press, London.
W, R.W., C, C.A. & C, L.J. (1994) Seed dispersal by forest chimpanzees inUganda. J. trop. Ecol. 10, 355–368.
W, R.W., C, N.L., E, G., O, J., H, K.D., H, M.D. & C, A.P.(1993) The value of figs to chimpanzees. Int. J. Primatol. 14, 243–256.
(Manuscript accepted 1 October 1997)
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