the role of mammals as ecosystem...

ALCES VOL. 39, 2003 SINCLAIR – MAMMALS AS ECOSYSTEM LANDSCAPERS

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THE ROLE OF MAMMALS AS ECOSYSTEM LANDSCAPERS

A. R. E. Sinclair

Centre for Biodiversity Research, 6270 University Boulevard, University of British Columbia,Vancouver, BC, Canada V6T 1Z4

ABSTRACT: The role of mammals in ecosystems is to modify vegetation structure, alter pathwaysof nutrients, and thereby change species composition. Their large-scale structuring effects makelarge mammals ‘ecological landscapers’. Through this they influence ecosystem function andbiodiversity. Landscaping effects occur when mammals are regulated by food, rather than bypredators. This condition is constrained by four factors: when (1) body size is large enough to avoidpredators; (2) populations adopt large scale migration behaviour because predators are unable tofollow them; (3) in multispecies communities (savanna, grasslands) with a range of predator and preysizes, only the largest species can avoid predation because they subsidize predators that regulatesmaller prey species; and (4) in single predator-prey systems (tundra, desert, boreal, and temperateforests), ecological conditions determine whether or not predators regulate prey. The structuringrole of mammals in maintaining species diversity is evident not just in vegetation, but also in birds,other mammals, and invertebrates. This role makes them prime candidates as ‘umbrella species’ forconservation. Protection of large mammal species and their habitats also conserves a large part ofthe remaining community. It also means that such mammals become the ‘indicator species’ for thehealth of the ecosystem.

ALCES VOL. 39: 161-176 (2003)

Key words: biodiversity, ecological landscapers, ecosystem function, mammals

In terrestrial ecosystems, plants formthe basis of all communities, in terms of bothstructure and function. The abiotic environ-ment sets the particular form of structure,with cold and dry climates having slow andintermittent flow of resources. The struc-ture moves from single layer lichens in theAntarctic through arctic tundra to complexrainforests of the tropics. Thus, plantsdetermine the niche possibilities of animals.

To what extent do mammals alter thebasic structure of communities set by plants?Because all animals in terrestrial systemsdepend directly or indirectly on plants, theymust to some degree alter plant structure,rates of flow, and species composition.Mammals, even at their most abundant, arenumerically insignificant in comparison tosuch groups as birds and reptiles, not tomention insects, protozoa, and protists.

Nevertheless, mammals impact plant struc-ture and function to a greater extent, rela-tive to their abundance, than any otheranimal group. Mammals are “ecologicallandscapers”.

Because mammals change the physicaland biotic landscape, they can affect eco-system function (Hurlbert 1997, Paine 2000).This impact leads naturally to the conserva-tion issues of umbrella species and indicatorspecies (Landres et al. 1988). Can mam-mals act as umbrella species purely be-cause of their large scale structuring andfunctional effects so that in protecting themthey also protect most other species? Canthey also act as surrogates for other groupsso that easily detectable trends in mammalsreflect similar trends in other less obviousgroups?

MAMMALS AS ECOSYSTEM LANDSCAPERS – SINCLAIR ALCES VOL. 39, 2003

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MAMMALS AS ECOLOGICALLANDSCAPERS

‘Ecological engineers’ are species thatchange the physical state of the biotic orabiotic environment in which they live, andthereby, alter the flow of resources to otherspecies (Jones et al. 1994, 1997). Thus, inmarine environments corals create theirown local environment as well as large-scale habitats for other species. Perhaps,termites create similar households on a lo-cal scale in terrestrial systems.

However, such ‘engineering’ operateson relatively local scales. There are alsoprocesses that take place on much largerscales (landscapes, watersheds, biomes)and determine not only physical structure,but also function and species composition ofwhole ecosystems. An example of onesuch process is fire, which in savanna biomesof Africa, Australia, and South Americachanges plant succession from a ‘firelessclimax’ to a ‘fire disclimax’. In savanna,fire typically impedes the succession oftrees and promotes grassland and fire toler-ant herbs (Frost 1985a). Fire operates as aprobability function on a biome scale, while

individual fire events occur at least at land-scape scales.

Mammals can have analogous effectsto fire in savanna systems (Hobbs 1996,Sala et al. 1996). One could even describea ‘mammal disclimax’ where plant succes-sion is held in a different state as a result ofthe restructuring imposed by mammals.Thus, mammals act as ecological landscap-ers. Such impacts are evident in mostterrestrial biomes where mammals are abun-dant.

Boreal and Taiga ForestsThe boreal forests of Canada are domi-

nated by a few species of conifer trees, inparticular the white spruce (Picea glauca).The dominant mammal there is the snow-shoe hare (Lepus americanus) that de-pends largely on woody shrubs such aswillow (Salix spp.) and birch (Betula spp.)during winter. Every 10 years hares reachhigh numbers and at those times they eat allof the terminal shoots of small white sprucewithin their reach (usually up to 120 cm)(Fig. 1). The slow growing spruce then takeabout 10 years to recover from this brows-

Fig. 1. The frequency of snowshoe hare browse heights on terminal shoots of small white spruce,Yukon, Canada. Hares can prevent trees from growing above about 1 m for several decades.


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ing, develop a new shoot, and add another10 cm in height, only to have this browsedoff at the next peak. Thus, a tree, 50 cmhigh, may take 50-80 years to reach theescape height, and some of them never doso and die. In contrast, trees protectedfrom browsing grow at an accelerating rateand can escape within 10 years. The borealforest is subject to fires from lighteningstrikes and so a mosaic is formed of patchesat different ages since a fire occurred. Theeffect of hares is to keep these patches inan open state for a century or more, creat-ing a landscape suitable for other plants thatlike open areas (many herbs and shrubs)and indirectly promoting their own foodsupply (Krebs et al. 2001.). Furthermore,experiments have shown that hare numbersdecline because of a combination of lack offood and an increase in predators. Experi-mental increase in rate of food supply plusremoval of predators kept hare numbershigh for an extended period. The inferenceis that under these conditions hares couldprevent forest regeneration altogether.There are similar browsing effects by moose(Alces alces) on aspen and other species atIsle Royale, U.S.A. (Risenhoover andMaass 1987, Pastor et al. 1988, McInnes etal. 1992, Pastor and Naiman 1992), and onbirch in Scandinavia (Danell et al. 1985,Danell and Bergstrom 1989, Danell et al.1994). Moose abundance influences thedensity of trees and hence composition ofthe habitats, but these effects also dependon the abiotic conditions and composition ofother vegetation. In general, a forest withmany moose is different structurally fromone without them.

In both Banff National Park, Canada,and Yellowstone National Park, USA, elk(Cervus elaphus) browsed juvenile treesof aspen and willow (Salix spp.) so inten-sively that they changed the landscape froma dense conifer and aspen woodland to anopen parkland (grassland with scattered

mature trees), and maintained it thus for 40years (Houston 1982,White 2001).

Temperate WoodlandThe deciduous hardwood forests of

North America are the home of white-taileddeer (Odocoileus virginianus) (McSheaet al. 1997). The preferred habitat of thesedeer is young forest, regenerating after fire(or logging). In these conditions deer canreach numbers that prevent forests fromregenerating, holding them in an open shrubstate (Schmitz and Sinclair 1997). Deer canmaintain this state while inhibiting hemlock(Tsuga canadensis) regeneration and ex-tirpating rare herbaceous plants (Alversonand Waller 1997). Without deer, forestsproceed to dense hardwood forests withabundant infrastructure in the shrub layerthat forms the nesting habitat for rare birdssuch as the Kentucky warbler (Oporornisformosus) (McShea and Rappole 1997). Inessence, there are two woodland states andwhich state prevails is determined by theabundance of deer.

Tropical ForestTropical forests, at least in the Holocene,

have been far less subject to major structur-ing forces of mammals. In both Africa andAsia, elephant species inhabit the forestsbut their large-scale impact (as opposed tolocal feeding effects) remains unknown.This is a subject that needs research forconservation reasons. I will refer later tothe paleohistorical effects of megaherb-ivores in forests.

Mammals, however, do influence thedistribution of trees in tropical forests and,thereby, the species diversity of tropicaltrees. In turn, the dispersion of trees influ-ences the extraordinary diversity of insectsthat live in these trees (Janzen 1970). Mam-mals such as bush pig (Potamochoerusporcus) and duiker (Cephalophus,Sylvicapra) species in African lowland for-


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est, and peccaries (Pecari, Tayassu), deer,pacas(Agouti spp.), agoutis (Dasyproctaspp.), and rats in New World tropical for-ests concentrate on fruit under parent trees,removing most of them, and transporting afew to other areas. We can see the effectof mammals by examining tree distributionsin areas where mammals have been re-moved. Thus, in tropical forests of CostaRica disturbed by agriculture, mammals areat low density from hunting. The undispersedseeds of the tree, Cassia grandi, are athigh density and suffer unusually high mor-tality from bruchid beetles (Janzen 1971).Similarly, tropical islands often lack thelarge vertebrates found on the mainland,and tree population structure differs mark-edly. In Puerto Rican forests, trees such asTrophis (Moraceae) have dense stands ofyoung trees under the canopy not seen inthe Costa Rican mainland where seeds areremoved by native rodents and birds (Janzen1970).

SavannaSavannas are grasslands with scattered

trees in the tropics and subtropics, typical ofAfrica and Australia, but with some repre-sentation in southern Asia and SouthAmerica. They intergrade with broad-leavedevergreen dry woodlands, particularly the‘mopane’ woodland of southern Africa andeucalypt woodland of Australia. Largemammals in Africa impose substantial struc-tural impacts in these biomes. In southernAfrica, heavy grazing of grasses by ungu-lates (monocot feeders) alters the balanceof water relations between the tree compo-nent and the herb layer so that trees andshrubs become dominant. In turn browsingungulates (dicot feeders) such as impala(Aepyceros melampus), greater kudu(Tragelaphus strepsiceros), and giraffe(Giraffa cemlopardalis) benefit and theirnumbers increase (Walker 1985, Owen-Smith 1988).

Fire is required to change the tree domi-nated vegetation state back to a grasslandstate. This was demonstrated in the Acaciasavanna of the Serengeti-Mara ecosystem,East Africa (Norton-Griffiths 1979). Be-tween 1890 and 1950 Acacia and relatedtrees dominated the vegetation. A 20-yearperiod (1950s, 1960s) of severe burning,where 80 % of the system was burnt eachyear, resulted in virtually no tree seedlingsescaping fire. Eventually senescence ofmature trees, expedited only to a minordegree by African elephants (Loxodontaafricana), resulted in a grassland state. Itis in this grassland state that elephantsplayed their major structuring role (Dublinet al. 1990, Dublin 1995). Elephants, bysystematically browsing tree seedlings, wereable to prevent regeneration of the treesand so hold the vegetation in a grasslandstate. Later, in the 1980s, elephants wereremoved by poachers and trees regener-ated in abundance forming dense thickets(fire having been reduced through grazingby wildebeest, Connochaetes taurinus;Sinclair 1995). Thus, it was the combinationof browsing by elephants and grazing bywildebeest that determined which of thetwo vegetation states, savanna or grass-land, persisted (Sinclair and Krebs 2002,Fig. 2). The return of savanna has resultedin an increase in impala.

Elephants as a structuring force were tobe seen in another area of East Africa, theTsavo National Park, Kenya. In the period1850 – 1900, the ivory trade in East Africadecimated elephant populations and nonewere to be found in the Tsavo of the 1890s(Patterson 1907). Furthermore, the Afri-can tribe that lived around Tsavo, theWakamba, were traditional elephant hunt-ers and kept numbers low in their areaduring 1900 – 1949. The vegetation withoutelephants was dense shrubland with scat-tered trees. It was sufficiently dense thathunters had to crawl along tunnels made by


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black rhino (Diceros bicornis) (Patterson1907). In 1949, Tsavo National Park wasformed and it contained few elephants anddense vegetation. Elephants, now releasedfrom hunting, increased rapidly with theabundant food supply. They reduced theshrub and tree densities in inverse propor-tion to the distance from water. The popu-lation increase ceased with an initial die-offdue to starvation (Corfield 1973) and hassince stabilized. In the presence of el-ephants the landscape is a mosaic of opengrassland, shrubland, and savanna. Thischange in vegetation structure led to de-clines of browsers such as gerenuck(Litocranius walleri), lesser kudu(Tragelaphus imberbis), and giraffe andan increase in grazers such as zebra (Equusburchelli) and buffalo (Syncerus caffer)(Parker 1983, Owen-Smith 1988).

Giraffe also structure savanna vegeta-tion through two effects. One effect is by

keeping small trees at a low height (1 – 2 m)through constant browsing (Pellew 1981,1983). This height makes small trees vul-nerable to fire, whose effects can reach upto 3 m. When a browsed tree in this heightrange experiences a hot fire, all its aboveground biomass is killed, and it must regrowfrom the rootstock (Dublin 1986). Thus,giraffe indirectly reduce the density of treesand maintain a more open vegetation struc-ture. Furthermore, abundant low level treeseedlings benefit other browsers such asgreater kudu and impala (Owen-Smith1988). The second effect of browsing is onmature trees that escape the fire window.These trees can be sculptured into a varietyof shapes beginning with a ‘top’ shape,broad at the base and with a narrow centralpole that giraffe cannot reach. This shapegrows into an hourglass form as the centralpole spreads out above the reach of giraffe.Eventually, the tree forms the characteris-tic flat top or umbrella top. This phenotypeis the direct result of giraffe browsing, for intheir absence we see trees with branchesthat droop down to the ground, formingdense thickets. These differences in treemorphology determine their suitability asnest sites for birds.

GrasslandsMammals play a major role in structur-

ing grasslands, especially wet grasslandsand swamps, in temperate and tropical re-gions. The treeless eastern Serengeti plainsare composed of short height grasses suchas Andropogon greenwayi andSporobolus spicatus. They also support alarge number of small herbaceous dicots.The structure and species composition ofthese plains is maintained by near continu-ous grazing from the large herds of migra-tory wildebeest and zebra (McNaughtonand Sabuni 1988). When wildebeest num-bers were reduced to 20 % of the presentday population, as a result of rinderpest

Fig.2. Savanna trees in Serengeti can exist in twostates with the same density of elephants. Ahigh tree density in the 1950s (squares) wasreduced by fires in the 1960s (triangles)through the inhibition of seedlings. The re-sulting low tree density was maintained byelephant browsing of seedlings (circles). Onlywhen elephants were removed by poaching(1980s) was the high tree density state re-stored (data from Dublin et al. 1990, Dublin1995, personal observations. Redrawn fromSinclair and Krebs 2002).


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mortality that persisted for some 70 years(1890-1963), these eastern grasslandschanged in structure, becoming taller (1 m).Similar tall grasslands currently on the west-ern Serengeti plains show that most dicotspecies become overshadowed and dropout. The impact of wildebeest grazing isdemonstrated from the measurement ofgrass consumption on the short grass plainscompared to the long grass plains (Fig. 3)(McNaughton 1984, McNaughton andSabuni 1988, Augustine and McNaughton1998). Furthermore, our studies reveal thatthe long grass structure provides the habitatfor a wide range of grassland bird speciesincluding grass warblers (Cisticola spp.)and larks (Alaudidae). Long-term grazingresults in a short-grass structure. This inturn provides the habitat for a different birdcommunity, including species such as thered-capped lark (Calandrella cinerea),capped wheatear (Oenanthe pileata), anddesert cisticola (Cisticola aridulus). Grass-hopper species also change with grass struc-ture. Thus, wildebeest grazing creates aniche for several different groups of spe-

cies in the grassland community. Similarchanges in the dicot herbs occurred withgrazing in the flooded pampa grasslands ofArgentina (Sala 1988).

In tundra biomes caribou or reindeer(Rangifer tarandus) reduce lichen coverand promote crustose lichens and bryophytes(den Herder et al. 2003). Along the Arcticshoreline of Canada, geese rather thanmammal herbivores are the major determi-nants of structure (Jefferies et al. 1994).However, the low impact of mammals is arecent event. I address the Pleistoceneimpacts below.

SwampsGrazing by wildebeest, and their effect

on grass structure, illustrates the processknown as ‘facilitation’ whereby one spe-cies provides niches for other species. El-ephants can facilitate the coexistence ofother ungulates in swamp grasslands bybreaking down, trampling, and feeding onvery tall (3-5 m high) woody grasses. Theyoung regenerating shoots of these grassescombined with other species that can growin the openings provide the niche for Afri-can buffalo, topi (Damaliscus korrigum),and waterbuck (Kobus defassa), a se-quence that was classically named the ‘graz-ing succession’ (Vesey-Fitzgerald 1960).

The Kafue flood plains in Zambia areannually flooded to depths varying from afew cm to several meters. Kafue lechwe(Kobus leche), a semi-aquatic antelope,occur at high density and impose consider-able grazing pressure. The vegetation ex-hibits clear zonation determined by the de-gree of grazing, which in turn is determinedby the degree of flooding and depth ofwater. In shallow zones, grazing is yearround and grasses such as Panicum repenshave evolved a leaf structure that remainsunder water and protected from grazing. Indeep water, out of reach of grazers for partof the year, grasses like Vossia cuspidate

Fig. 3. Serengeti migrant herbivores maintainthe short grasslands by consuming most ofthe growth (triangles), measured from smallexclosure plots. In contrast, herbivores haveless impact on the long grass plains andsavannas as seen from the lower consumptionrates (circles). The taller the grass the less isconsumed (data from McNaughton and Sabuni1988).


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have evolved a canopy that grows abovethe water surface (Ellenbrock and Werger1988). It is likely that these different growthforms will support different animal commu-nities.

DesertsIn Australia, burrowing bettongs

(Bettongia lesueur), a small macropodmarsupial the size of rabbits, now extinct onthe mainland, were thought to structure thevegetation over large areas of Acaciashrubland (mulga) (Noble 1999, Noble et al.2001). They formed large undergroundwarrens from which they commuted sev-eral kilometres to feed on shrubs. Undercertain fire frequencies they were appar-ently able to prevent shrub regeneration andmaintain an open herbaceous structure. Theremoval of bettongs through invasion ofexotic red fox predators (Short et al. 2000)changed the landscape to dense stands ofAcacia shrubs. Incidentally, the pastoralvalue of these landscapes was probablymuch higher in the presence of bettongsthan at present with the unutilized stands ofshrubs.

The Chihuahuan deserts of Mexico arepresently characterized by dense stands ofcactus such as Opuntia. Currently, cattleopen up these stands but bison (Bison bi-son), elk, and peccaries did so previously.Openings increase diversity of herbs thatare redistributed by mammals (Janzen 1986).

MAMMALS AND ECOSYSTEMPROCESSES

Mammals influence the rates of nutri-ent cycling in addition to altering physicalstructure. In boreal forests moose de-crease nitrogen mineralization of the soil bydecreasing the return of high quality litter:their browsing on deciduous trees reducestheir leaf fall while promoting low qualitywhite spruce inputs (Pastor et al. 1988,1993; Pastor and Danell 2003). In contrast,

soil nitrogen cycling in Yellowstone andother prairie areas of the U.S.A. is in-creased by large mammal grazers (Hobbs1996, Frank and Evans 1997).

The woodland-savanna biomes of Af-rica are dichotomous in terms of nutrients.Soils formed from old granitic rocks aresandy, heavily leached, and low in nutrients(dystrophic), particularly in calcium andphosphorus. These areas tend to be in themiombo woodlands of southern Africa. Incontrast, soils formed from volcanic originssuch as basalt are high in nutrients and arefine, clay types (eutrophic). These aremore frequently found in East African Aca-cia savanna (Bell 1982, Frost 1985b, Naimanand Rogers 1997). However, superim-posed on this pattern is an effect of largeungulates: high soil nutrients lead to highungulate densities, rapid grazing/browsingofftake, and high fecal deposition. Nutri-ents in the feces are then returned rapidly tothe soil to be used by forage plants. Inessence, ungulates fertilize their own food,and thereby, create a positive feedbackincreasing their own density. These effectsare observed in the medium rainfall range of500-1000 mm per year (Botkin et al. 1981).In arid areas there is high soil nutrient butinsufficient rain to promote recycling,whereas in very wet (forest) areas there istoo much leaching and insufficient herblayer to support high densities of ungulates.

At a smaller scale within the Serengetisystem, McNaughton et al. (1997) havefound that concentrations of non-migratoryungulates occur at localities naturally highin sodium. These are similar to the ‘sodic’sites found in Kruger National Park, SouthAfrica, and at Yellowstone and prairie sitesin North America (Tracy and McNaughton1995). On the Serengeti sites the concen-tration of ungulates produces higher levelsof soil nutrients and hence higher nitrogenmineralization rates. Such sites have beendubbed ‘hotspots’.


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On the subarctic heathlands of Finlandreindeer reduce lichen biomass, which al-lows a higher mineralization by soil mi-crobes. Lichens are so efficient at remov-ing nitrogen from rainwater that they re-duce the amount reaching the soil (denHerder et al. 2003).

MAMMALS AND PLANT SPECIESCOMPOSITION

Black-tailed prairie dogs (Cynomysludovicianus) and pocket gophers(Geomys bursarius), rodents that live inlarge colonies on the prairies of NorthAmerica, provide one of the classic exam-ples of mammals that structure the land-scape, alter the species composition of thevegetation, and so facilitate other herbiv-ores (Huntly and Inouye 1988, Whicker andDetling 1988a,b). Miller et al. (1994) sug-gest that they act as ‘keystone species’through their disproportionately large influ-ence on vegetation composition. Studies atWind Cave National Park show that prairiedogs graze grasses to a low level (a few cm)around their colonies. Constant grazingchanges grass species composition to lowgrowing forms and many dicot species sur-vive due to reduced competition from grass.American plains bison preferentially grazethese short grasses and pronghorn antelope(Antilocapra americana) feed on thedicots. Originally prairie dogs affected atleast 20 % of the prairies (Coppock et al.1983, Whicker and Detling 1988a,b). Ex-clusion of prairie dogs and bison returns thevegetation to long grass prairie (Cid et al.1991).

Elk (Cervus elephus) maintain grasspatches in the understory of old growthconifer forests of Olympic and YellowstoneNational Parks, U.S.A. Exclusion of elkresults in grass species being replaced bymosses, ferns, and shrubs (Schreiner et al.1996, Augustine and McNaughton 1998).

Rabbits on the short grass chalk

grasslands of Sussex, England (the SouthDowns), determine both their structure andplant composition. These effects weredetected when marked vegetation changestook place after rabbits were removedthrough the epizootic myxomatosis in 1953(Ross 1982). Short grasses and many dicotswere replaced with tall tussock grasses,and there were subsequent changes in antsand lizards dependent on these plant forms.

On tundra and subarctic heathland, se-lective grazing by reindeer keeps the com-munity in an early succession stage. Theyreduce the preferred and competitively domi-nant Cladina lichens, which allows otherlichens, bryophytes, and dwarf shrubs toexist, but it also reduces regeneration ofconifer seedlings (den Herder et al. 2003).

CONSTRAINTS ON THE ROLE OFMAMMALS AS ECOSYSTEM

PROCESSORSFundamentally mammals restructure

landscapes when they are food limited.Herbivore populations that are regulated bypredators have only selective effects onvegetation, often in local (small-scale)predator-safe areas. What are the condi-tions, therefore, that determine when mam-mal herbivores are food limited? In essencethere are 4 main conditions that affect thecause of regulation:

Body SizeVery large herbivores are simply too

large for predators. Clearly elephants, rhi-nos, and hippos fall into this category de-spite a few newborn animals being killedoccasionally. In addition, even animals thesize of African buffalo and giraffe are largeenough that predators have difficulty killingthem. The consequence is that predationaccounts for only 25 % of annual mortalityin buffalo (Sinclair 1977, 1979). It appearsthat wood bison (B. bison athabascae)also falls in this category, since a population


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in the Mackenzie Bison Sanctuary ofCanada continues to expand despite wolfpredation of juveniles (Larter et al. 2000).

MigrationPredators cannot follow, on a year-

round basis, animals that migrate. Thisgeneral rule is evident in all mammal migra-tion systems including those by caribou(Rangifer tarandus) in northern Canada,white-eared kob (Kobus kob), in Sudan,gazelles in Botswana, and wildebeest andgazelles in Serengeti (Sinclair 1983, Fryxelland Sinclair 1988). These species, there-fore, escape from predator regulation. Inaddition, migration is an adaptation to ac-cess ephemeral, high-quality food resourcesnot available to non-migrants. These twofeatures of migration systems allowpopulations to become an order of magni-tude greater in number compared to resi-dents. Thus, migrant wildebeest in Serengetioccur at 50 animals/km2 compared to asympatric resident population at 5 animals/km2. Such large populations have majorstructuring effects on the ecosystem.

Diversity of Herbivore and CarnivoreGuilds

In some systems there is a high diver-sity of large mammal herbivores and carni-vores. Nearly all are associated with tropi-cal savanna and grassland. Whether apopulation of herbivores is limited by preda-tors, and so has little structuring effect onvegetation, is determined by its place in thehierarchy of herbivores.

In African savanna there are as manyas 10 co-existing canid or felid carnivoresfeeding on ungulates, lagomorphs, and ro-dents. They vary in size from the 200 kg lion(Panthera leo) to the 5 kg wild cat (Felissylvestris). The larger the carnivore, thegreater is its range of prey sizes (Fig. 4).Thus, the diet of lions ranges from buffalo(450 kg) to dik dik (Madoqua kirkii) (10

Fig. 4. The range of mammal prey sizes forSerengeti carnivores. The larger the carnivorethe greater the prey range. Thus, small ungu-lates can have as many as 9 different predatorspecies whereas larger prey have only one ornone (Avenant and Nel 1997, personal obser-vations).

kg), a small antelope, whereas that of caracal(Felis caracal) ranges from duiker (15 kg)to 100 g rodents (Avenant and Nel 1997).The consequence of this is that in theSerengeti system, for example, smaller un-gulates have as many as 7 predator species,intermediate sized antelope such as topi(Damaliscus korrigum) (120 kg) have 4predators, and very large ones like eland(Taurotragus oryx) have only one. Thus,smaller ungulates must experience morepredation and be predator regulated if theyare not migrants, and so have less effect onvegetation. Direct measures of mortalityby predators are consistent with this predic-tion. We have found that in small antelopesuch as oribi (Ourebia ourebi) (10 kg),nearly all mortality of adults is accountedfor by predators; in zebra (Equus burchelli)(250 kg) this is about 73 %, while in buffaloit is 23 % (Sinclair 1977).

Therefore, in a multi-species mammalcommunity, large herbivores will structurethe landscape whereas smaller ones can-not. The effect of large herbivores on


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vegetation structure is enhanced becausethey also feed in a broader range of habitatsthan do smaller species. Thus, elephantscan range from tropical forests to desertswhereas the smallest ungulates are con-fined to single habitats.

The Direction of RegulationIn many biomes of the temperate and

arctic regions there is only one major preda-tor and one or a few species of mammalianprey. Landscape structure and compositionin these areas are determined by whetherthere is top-down or bottom-up regulation.In some cases the direction of regulation isobligatory, in others, both top-down andbottom-up regulation can occur with thesystem switching from one state to anotherdepending on disturbances from outside thesystem. Obviously, bottom-up regulationoccurs when predators are absent. In thiscase browsing mammals must have an im-pact on the rate of regeneration of juvenilewoody plants simply from feeding. How-ever, such effects would not necessarilyprevent the formation of the eventual ma-ture climax. The issue is whether mammalscan hold the vegetation in a different state.In some cases they do. In Europe, wherepredators have been removed, browsing byred deer (C. elaphus), wild boar (Susscrofa), and chamois (Rupicapra spp.)changed forested areas into grasslands andheld them there (Miller et al. 1982); thesebrowsers maintain a different state.

Examples of obligatory top-down regu-lation are less prevalent. Wolves appar-ently regulate moose in parts of Canada(Messier 1994). When wolves were absenton Isle Royale, moose had major effects onvegetation structure. Even when wolvesarrived on the island their numbers ap-peared to track moose numbers and did notregulate that population (Peterson andVucetich 2001).

In other systems, either top-down or

bottom-up regulation can occur with conse-quent differences in the landscape struc-ture. For example, I have mentioned abovethe effect of elk in transforming aspenstands to open parklands in Banff NationalPark, Canada. This occurred when wolveswere removed in the 1930s. In 1985 wolvesreappeared and since then they have bothreduced elk numbers and confined them toa subset of the habitats. In elk-free areas,young trees are regenerating and more denseaspen stands should appear in the nextdecades (White 2001). The recent increaseof wolf numbers in Yellowstone should alsochange the aspen structure there. Thus,which of the two landscapes occur (wood-land or parkland) is determined by the pres-ence or absence of both mammalian herbiv-ores and carnivores. (Note, either state isa normal or ‘natural’ configuration of indig-enous species, neither should be regardedas aberrant in terms of conservation andmanagement).

MEGAHERBIVORES ANDPALEOHISTORY

Present-day elephants, rhinos, and othermegaherbivores clearly play a major role inshaping the landscapes in which they live.We must remember that megaherbivoreswere far more abundant in the Pliocene andPleistocene, even 20,000 years ago theywere common, and they died out a mere10,000 years ago on all continents exceptAfrica (Owen-Smith 1988). Before this,even larger ancient mammals such asBrontotheres (30 M b.p.), Indricotheres andChalicotheres (20 M b.p.), and Litopterns(10 M b.p.) must have imposed importantevolutionary pressures on the vegetation.

Mammoths, mastodons, and woolly rhi-nos roamed the tundra of the Holarctic. Ontundra only 13 % of annual production iscurrently consumed (C. J. Krebs, personalcommunication), the remainder in thePleistocene most likely eaten by the mam-


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moths. Mastodons fed on trees and shrubsin both the boreal and tropical rain forests ofthe New World while giant ground slothsand glyptodonts fed in Mexican deserts(Janzen 1986). Thus, the impacts of mam-mals in these biomes would have been moresimilar to those we currently see in Africanlandscapes. As in Africa, the biomes ofEurasia and the Americas would haveevolved adaptations to tolerate or mitigatethe impacts of megaherbivores, adaptationsthat are probably still present. Janzen andMartin (1982) have suggested that many ofthe seedpods in Costa Rican forests aredesigned for ingestion and dispersal bymastodons, and Janzen (1986) proposes thefleshy fruits of Opuntia cactus are de-signed for extinct large mammals. The lackof such dispersal agents today suggestsNew World forests now have a differentstructure and species dispersion pattern fromthe one when large mammals were com-mon. Similarly, the present-day boreal for-ests of North America and Asia, character-ized by homogeneous stands with few treespecies, were once a mosaic of matureconifers and regenerating deciduous patches,and with a more diverse fauna associatedwith the mosaic. Thus, the lack of largemammal impacts today could be an artifactof human induced extinctions in the recentpast.

CONCLUSIONThe main theme of this paper is that the

role of mammals in ecosystems is to modifyvegetation structure, alter pathways of nu-trients, and thereby change species compo-sition. The large-scale structuring effectsmake large mammals ‘ecological landscap-ers’ that influence both ecosystem functionand biodiversity. Moose in boreal forestsprovide a classic example of such effects.

Landscaping effects occur when mam-mals are regulated by food, a bottom-uptrophic process, rather than by predators.

This condition occurs, or is constrained, by4 factors: when (1) body size is large enoughto avoid predators; (2) populations adoptlarge scale migration behaviour becausepredators are unable to follow them; (3) inmulti-species communities with a range ofpredator and prey sizes (savanna, grass-land)¸ only the largest species can avoidpredation because they simultaneously sub-sidize predators that regulate smaller preyspecies; and (4) in single predator-preysystems (tundra, desert, boreal, and tem-perate forests) ecological conditions deter-mine whether or not predators regulateprey.

The landscaping role of mammals inmaintaining species diversity is evident notjust in vegetation, but also in birds, othermammals, and invertebrates. This rolemakes them prime candidates as ‘umbrellaspecies’ for conservation. Protection oflarge mammal species and their habitatsalso conserves a large part of the remainingcommunity. Such mammals become the’indicator species’ for the health of theecosystem. Thus, if the wildebeest popula-tion were to go into a prolonged decline, forexample, the Serengeti ecosystem woulddisappear.

ACKNOWLEDGEMENTSI thank John Pastor for insightful com-

ments and Anne Sinclair for much help inthe preparation of this paper. Funding wasprovided by the Canadian Natural Sciences& Engineering Research Council. TheNorwegian Department of Nature Man-agement supported my travel to Norway,and the CSIRO Sustainable EcosystemsDivision, Australia, provided facilities dur-ing the writing.

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