Ungulate herbivory: Indirect effects cascadeinto the treetopsAndrew J. Larson*† and Robert T. Paine‡

*College of Forest Resources, University of Washington, Box 352100, Seattle, WA 98195-2100; and ‡Departmentof Biology, University of Washington, Box 351800, Seattle, WA 98195-1800

Changes in population numbersof top (apex) predators areincreasingly acknowledged topromote major shifts in ecosys-

tem organization. The early evidencewas both experimental and observation-ally based: for instance, predatory star-fish can influence the ability of speciesto coexist on marine rocky shores (1);bass, by consuming grazing minnows,alter primary production in freshwaterstreams (2); and sea otters, by eating seaurchins, themselves major consumers ofmarine benthic algae, indirectly exert amajor influence on the biological per-formance of these primary producers(3). The initial impression was that suchpotent top-down effects were ‘‘all wet’’(4) and that terrestrial ecosystems mightbe fundamentally different from aquaticones; in this issue of PNAS, Pringle etal. (5) add to a growing body of evi-dence suggesting the contrary. Somereasons for this initial impression seemobvious: many terrestrial apex predatorshave been hunted to near or local ex-tinction; many of the more charismaticspecies now enjoy stringent legal protec-tion, which hampers or denies any ma-nipulation; and terrestrial ecosystemsthemselves are less experimentally trac-table than their aquatic counterparts, inpart because of extreme longevity of theplant community and because of thegreat spatial scale required to retain asemblance of natural reality. Nonethe-less, an important role for apex preda-tors is increasingly recognized as thesepredators persist in fragmented habitats(e.g., coyotes; ref. 6), are introduced toislands (e.g., fox–seabird–vegetationlinkages in the Aleutian Islands; ref. 7),are reintroduced to historic habitats(e.g., wolves into Yellowstone; ref. 8),when comparable habitats with andwithout a massive human presence areexamined (e.g., the mountain lion–amphibian connection in Zion NationalPark; ref. 9), and in the rare cases inwhich sufficient time series data existto develop tri-trophic models (10). Oneconclusion is that sites with a fullercomplement of apex predators oftensupport a greater number of species,may be more productive, and deliverhigher-quality ecosystem services (e.g.,water). The structural differences aresufficiently clear to have led to a pro-

posed ‘‘rewilding’’ of large tracts of land(11), that is, a repopulating by mega-fauna including apex predators.

Pringle et al. (5) examine an Africansavanna system in which three pairs ofmegaherbivore exclusions and their con-trols (sites with normal grazer access)were established on productive volcanicclays and compared with a second setwithin 12 km on less productive sandyloams. The ungulate herbivore exclu-sion, that is, all grazing mammals �15kg, included a nine-species guild of suchfavorites as elephants and zebras butalso domestic cattle and was enforced bya 2.4-m high electrified fence obviouslyentirely permeable by insects, snakes,lizards, birds, and smaller mammals.

The exclosure treatment reduced ungu-late density to zero over the manipula-tion’s duration: this is analogous to anexperimental system in which ‘‘preda-tion’’ on these large ungulates was 100%efficient.

Pringle et al. (5) found greater pro-ductivity at all six ungrazed sites relativeto controls. Plants, i.e., trees and moreconventional forage, might be expectedto grow better when not consumed bya phalanx of large-bodied consumers,but grazing is also known to stimulategrowth (12). The research ‘‘gold’’ comesfrom the well documented but certainlyincomplete cascade of related indirecteffects. Associated with the increase intree density and profile complexity wasa 61% increase in lizard density. Theirmajor prey, beetles (22% of diet),marched to the same drummer: greaterproduction yields more beetles. Onesubtlety is the dual mechanisms bywhich ungulate exclusion increased lizarddensities: density of beetles, a major liz-

ard prey item, increased, as did arborealhabitat available for lizards to colonize.Multiple mechanisms linking ungulateherbivory to lizard density certainly sup-port the idea that ungulates initiaterampant indirect effects.

Perhaps the most significant findingof Pringle et al. (5) is that the strengthof the indirect influences was negativelycorrelated with site productivity; that is,at less-productive sites, exclusion ofmegaherbivores generated a greater ef-fect. The environmental message seemsclear: ecosystems with a low intrinsicprimary production capacity, generated,for instance, by low annual rainfall orrelatively reduced soil nutrients, will beboth more susceptible to and less capa-ble of responding to anthropogenicmodifications than more productivesites. However, the relationship betweeneffect strength and productivity carrieswith it other implications. Namely, Prin-gle et al. show how the nature of inter-specific interactions in putatively similarcommunities changes in response toforcing by a ‘‘global’’ variable, in thiscase productivity. By documenting vary-ing strengths of indirect effects of herbi-vores along a productivity gradient,Pringle et al. introduce a new twist toquestions about community organizationin terrestrial habitats (albeit one thathas been explored in intertidal commu-nities; ref. 13): how do species interac-tions within a given community varyalong an environmental gradient? Thisadded detail foreshadows a type ofinvestigation, and a conceptual frame-work, that may help transition commu-nity ecology from a ‘‘science of place’’to a science that subsumes place. Stud-ies that look for general trends acrosswidely dispersed sites (14) approachthis challenge from one direction; themethod used in the present case (5),characterizing variation in species inter-actions within a community in responseto environmental heterogeneity, ap-

Author contributions: A.J.L. and R.T.P. wrote the paper.

The authors declare no conflict of interest.

See companion article on page 193.

†To whom correspondence should be addressed. E-mail:a975764@u.washington.edu.

© 2006 by The National Academy of Sciences of the USA

Ecosystems witha low intrinsic primary

production capacity willbe more susceptible

to anthropogenicmodifications.

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proaches the problem from a different,yet informative, perspective.

Pringle et al. (5) barely discuss thespecies composition of what must bea complex and interactive community.Ants are mentioned and help defendthe dominant Acacia trees, much as inJanzen’s early neotropical studies (15).But what role do arachnid predatorsplay? In an old-field ecosystem (16),spider-specific identity and abundancedetermined how herbivorous grasshop-pers, plant nutrient level, and thereforeprimary production interacted: spidersin abundance reduced herbivore activ-ity and thus facilitated plant perfor-mance. Could the ‘‘herbaceous species’’studied by Pringle et al. (5) have bene-fited from such inf luences? The answerdepends on effect magnitude. Similarrelationships should be sought in twoother trophic groups. Insectivorousbirds could have been major playersin the indirectly enhanced food web.Their exclusion has been shown experi-mentally to diminish plant production(17). In a neotropical forest, bird pres-ence reduced insect damage to canopyfoliage, although not in the less-pro-ductive understory (18). Finally thereis the issue of snakes, apparently withnumbers increased in the absence ofungulates (5). Did these eat smallmammals and birds? By temperate-zone standards, the question is nottrivial because small rodents can deter-mine the survival of tree seeds andseedlings (19). The above questions arenot criticisms: no ecological field studyyet, and possibly ever, can be trophi-cally complete. The question about in-direct effects is always not whetherthey occur but rather, what is theirmagnitude and, therefore, significance.

Lastly, we turn to the problem of ex-perimental intractability due to long-lived, slow-growing plants in terrestrialecosystems. Suppose comparisons ofexclosure and control sites had beenconducted after 20 years, 50 years, ormore. How different would the resultshave been? Fig. 1 illustrates an exampleof ecological change wrought by denying

Roosevelt elk access to a portion of theOlympic rainforest. In this instance,grass biomass plummeted, herbaceousunderstory plant diversity declined,woody shrubs aggressively filled the site,and seedling and sapling density of thetree western hemlock (Tsuga hetero-phylla) increased (20, 21). In both theOlympic rainforest and the African sa-vanna, it would be fascinating to knowthe long-term consequence of a main-tained herbivore-free treatment. Struc-tural development in the Olympicrainforest proceeds over several centu-ries (22), indicating, as we have alludedfor the African savanna, that the transi-tion to an herbivore-free equilibriumwill be protracted. Obviously, a temper-ate rainforest is conspicuously distinctfrom an African savanna. However, both

ecosystems share one feature in com-mon: exclusion of ungulate herbivoresincreases the density of long-lived, habi-tat-forming trees. In the African sa-vanna, this mediated an indirect effectof ungulates on arboreal lizards. Simi-larly, indirect effects of ungulate her-bivory on epiphytic plants, for which theOlympic rainforest is famous, as well asother canopy biota will likely propagatethrough the trees. How will the speciesassemblage and the strength of interspe-cific interactions change as populationsof trees fully respond (i.e., reach maxi-mum size and structural complexity) torelease from herbivory? Do the indirecteffects of ungulate herbivory follow anindependent ‘‘successional’’ trajectorythemselves? Only long-term manipula-tive ecological studies can provide defin-itive answers to these questions.

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Fig. 1. Vegetation response after 26 years of continuous exclusion of Roosevelt elk herbivory from a sitein the Olympic rainforest of western Washington. Within the protected area, the shrub salmonberry(Rubus spectabilis) has formed a near-monodominant stand. Densities of the tree western hemlockincreased with the exclusion of elk, suggesting that further changes to vegetation structure and compo-sition will occur with the continued absence of herbivory.

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