Body Size, Population Metabolism, and Habitat Specialization Among Large African Herbivores

Vol. 133, No. 5 The American Naturalist May 1989

BODY SIZE, POPULATION METABOLISM, AND HABITAT SPECIALIZATION AMONG LARGE AFRICAN HERBIVORES

Large species generallyoccur at lower populationdensities than small species but,being larger, use moreenergy per individual.The balance betweenpopulation density and energy use per individual determineshow evenly communityre- sources are shared by species of differentsize. Analyses of large data sets, coveringa wide range of body sizes, have foundthat population metabolism (the product of population densityand energyuse per individual)scales eitherneu- trally(Damuth 1981, 1987) or negatively(Peters 1983) withbody mass. However, differentscaling relationshipsmay occur in certaincommunities within specific biogeographicregions. Brown and Maurer (1986) foundthat population metabolism scales positivelywith body mass amongNorth American land birds,granivo- rous desert rodents,marine fishes, and perennialdesert plants. A comprehensive studyof the relationshipsbetween mammalianpopulation density and body mass (Peters and Raelson 1984) indicates thatpopulation metabolism scales positively withbody mass among "smaller tropical" herbivores(cxM026), "larger tropical" herbivores(cx M045), and "largertropical" carnivores-omnivores(cxM028) but not among North American species (herbivores, cxM009; carnivores-omnivores, xMm-0.39) We presentresults confirming that among Africansavanna herbivores,population metabolismscales positivelywith body mass. That is, largerspecies use a disproportionatelylarger share of local resources. We also presenta hypothesisto explain this, on the basis of patternsof habitatuse. We analyzed census data for mammalianherbivores (-4 kg) from11 African nationalparks or wildlifereserves within the savanna biome. Areas variedfrom 75 km2to 19,500km2. Population metabolism was calculated as the productof mean populationdensity, mean individualbody mass, and mass-specificmetabolic rate (assumed to scale as M-0.25; Kleiber 1961). The combineddata fromthese parks show thatpopulation metabolism increases significantlywith body mass (table 1). However, a tendencyto undercountsmaller species could have influencedthis result.Hence, we also examined ungulatepopulations estimated for the Umfolozi Game Reserve in South Africa, where aerial census data were corrected with intensiveground-based counts. A similarrelationship between population metabolism and body mass was found.Finally, we consideredthe highestlocal densities reportedfrom specific studies in areas favored by each species. Our analysis (table 1) shows that,among large herbivorousspecies in Africansavanna ecosystems, population metabolismincreases approximatelyin relationto M045s. This relationshipis confirmedby Damuth's (1987) data, in which populationmetabo-

Am. Nat. 1989. Vol. 133, pp. 736-740. ? 1989 by The Universityof Chicago. 0003-0147/89/3305-0015$02.00.All rightsreserved.

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TABLE 1

RELATIONSHIPS BETWEEN POPULATION METABOLISM AND BODY MASS FOR LARGE AFRICAN HERBIVORES

REGRESSION STATISTICS RESEARCH AREA BODY-MASS SCALE AREA* (km2) RANGE (kg) b SE a r n

Savanna 11 conservation areas 65,000 10-2100 0.40 0.16 0.84 0.65 25 biome (combined) Regional Umfolozi Game Reserve, 450 20-1350 0.51 0.21 0.85 0.72 13 S. Africa (1970) Local Various single-species 4-2100 0.46 0.14 1.75 0.73 25 studies

NOTE.-Statistics are for the relationship between population metabolism (E) and body mass (M) according to the least-squares-regression equation log E = a + b(log M); SE, standard error of the slope b; r, correlation coefficient; n, number of species. * Sources listed in Owen-Smith 1988.

lism among large Africanherbivores (- 10 kg) in grasslandand savanna regions scales in relation to M0-43(Damuth, unpubl. data). Thus, a 10-foldincrease in species body mass would be associated with an almost threefoldincrease in resource use. Brown and Maurer suggestedseveral advantages of large body size thatmay result in large species' dominatingresource allocation, includingdominance in interspecificaggression, better predator evasion, and enhancedability to use low- qualityfoods. However, aggressivecompetition for food is rare or absent among ungulate species, which instead frequentlyassociate together,deriving mutual benefitsin terms of predator avoidance (Jarman 1974; Sinclair 1985). In fact, feedingby largerspecies may even enhance food availabilityfor smaller ungulate species (Vesey-Fitzgerald 1960; Bell 1971). Furthermore,diminished predation levels occur only amongthe verylargest species, exceedingabout 1000kg in body mass (Owen-Smith1988). Among large herbivores,enhanced tolerancefor low- qualityfoods (Bell 1971; Jarman1974) arises fromthe allometryof the metabolic rate-gut capacity relationship(Demment and van Soest 1985). We propose that thisrelationship also enables largerspecies to spread moreevenly through ecosystems by feedingproductively in habitatsthat are less suitablefor smaller species. We compared patternsof habitatuse by three species of browsingruminant: steenbok (Raphicerus campestris); kudu (Tragelaphus strepsiceros);and giraffe (Giraffa camelopardalis). These species were selected because of their large differencesin body mass (11 kg, 180 kg, and 800 kg, respectively)together with theirsimilarities in food resource base (foliage of woody plants and forbs) and distribution(coexisting in most Africansavanna regions). Comparativehabitat use was investigatedusing data froma 3-year study conducted in the central KrugerNational Park, South Africa(du Toit 1988). For each species, proportional use of each of the 14 habitattypes (vegetational communities) in the 160-km2study area was calculated as ni Puil = p Pai Pai

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0.95- x G

0.90-

H' 0.85- x K

0.80-

x S

I ~~~I I 10 100 1000 M (kg)

FIG. 1.-Diversityof habitat use (H') versusbody mass (M) forthree species of browsing ruminant:S, steenbok;K, kudu,G, giraffe.Axes are logarithmic(data from du Toit 1988). wherepui is the proportionof the studypopulation using the ith habitatwhen all habitats are equalized by area; ni is the mean annual numberof study-animal sightingsin the ith habitat(using randomtransect counts for steenbokand radio telemetryfor kudu and giraffe);and Pai is theproportion of the studyarea actually covered by the ith habitat.The Shannon-Wienerindex H' (Shannon and Weaver 1949; Pielou 1977) was used to indicatediversity of habitatuse: H' = - I Puilog Pui The total numberof sightingsrecorded per species was 349 forsteenbok, 4508 for kudu, and 883 forgiraffe. The results(fig. 1) show thatalthough all threespecies occurredthroughout the studyarea, steenbokwere concentratedin a narrowerrange of habitatsthan kudu, whichin turnwere less evenly distributedthan giraffe. Although our quantitative data are limitedto threespecies, our findingsare supportedby patternsof habitat use reportedfor other ungulate species in the KrugerNational Park (Pienaar 1963; Smithers1983). For example, klipspringer(Oreotragus oreotragus) and bushbuck (Tragelaphus scriptus) are both small ruminants(11 kg and 30 kg) with specific habitatrequirements; klipspringer are restrictedto rockyoutcrops and bushbuck to riparianthickets. Such habitatspecificity is not shown by any largerungulate. For African savanna herbivores, we propose that wider feeding tolerance among larger species leads to the use of a wider range of habitatpatches and, hence, to a moreeven use of environmentalresources. Wider habitat use by larger species could apply to other primaryconsumers as a consequence of increased dietarytolerance for either a widerrange in nutritionalquality or a widerrange of food-itemsizes (May and MacArthur 1972; Schoener 1974). A similarpattern could be expected among secondaryconsumers as a reflectionof the tendencyfor predatorand prey sizes to be related (Rosenzweig 1966; Peters 1983).

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Diversityin habitatuse by large species is, however,limited by the diversityof available habitats.Hence, our hypothesisapplies to ecosystemswith high spatial heterogeneity,or patchiness, and this is expected to decrease with increasing latitudeas a consequence of the latitudinalgradient in ecological diversity(see Brown and Gibson 1983). The abilityof largerspecies to feed in a widerrange of habitats, togetherwith the increased habitat diversityin tropical ecosystems, could explain a differencebetween the resultsof Peters and Raelson (1984) and those of Damuth (1987). Petersand Raelson's resultsshow thatpopulation metabolism scales positively with body mass among mammalianherbivores in the tropics, but not if North American data are included. In contrast,Damuth's results indicate that the scaling of population metabolismin the tropics is not significantlydifferent from the global pattern.This could be because Damuth based his studyon "ecological" densities,referring to the area of habitatactually used by the animals in all cases, whereas Peters and Raelson used "crude" densities over larger areas that include some (perhaps less productive)patches unoccupied by some (perhaps smaller) species.

ACKNOWLEDGMENTS Constructivereviews of the manuscriptwere made by J. H. Brown,J. Damuth, M. L. Rosenzweig, A. R. E. Sinclair,and an anonymousreviewer. The Council for Scientificand IndustrialResearch, South AfricanNature Foundation, Na- tionalParks Board, and Universityof the Witwatersrandprovided research funds and assistance.

LITERATURE CITED

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Pienaar, U. de V. 1963. The large mammals of the Kruger National Park-their distributionand present-daystatus. Koedoe 6:1-37. Rosenzweig, M. L. 1966. Communitystructure in sympatricCarnivora. J. Mammal. 47:602-612. Schoener, T. W. 1974. Resource partitioningin ecological communities.Science (Wash., D.C.) 185:27-39. Shannon, C. E., and W. Weaver. 1949. The mathematicaltheory of communication.University of Illinois Press, Urbana. Sinclair, A. R. E. 1985. Does interspecificcompetition or predation shape the African ungulate community?J. Anim. Ecol. 54:899-918. Smithers,R. H. N. 1983. The mammals of the southernAfrican subregion. University of Pretoria, Pretoria,South Africa. Vesey-Fitzgerald,D. F. 1960. Grazing succession among East Africangame animals. J. Mammal. 41:161-172.

JOHAN T. DU TOIT* NORMAN OWEN-SMITH RESOURCE ECOLOGY GROUP DEPARTMENT OF ZOOLOGY UNIVERSITY OF THE WITWATERSRAND P.O. WITS 2050 SOUTH AFRICA SubmittedApril 8, 1988; Revised July18, 1988; Accepted October 23, 1988

*Presentaddress: Departmentof Range Science, Utah State University,Logan, Utah 84322-5230.

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