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African mammals, foodwebs, and coexistenceDavid Tilmana,b,1 and Elizabeth T. BoreraaDepartment of Ecology, Evolution and Behavior, University of Minnesota, St. Paul,MN 55108; and bBren School of Environmental Sciences and Management, University ofCalifornia, Santa Barbara, CA 93106

In the 65 million years since a mass extinc-tion led to the demise of dinosaurs, evolutionhas generated amazingly diverse and complexfoodwebs on each continent (1). These food-webs contain hundreds to thousands of inter-acting species, each linked to other specieseither by feeding on them or by being fedon by them. However, it has been difficultto determine consumer diets across seasons,individuals, and space, and especially hard toquantify the strengths of these linkages in allbut the simplest foodwebs. These issues havelimited the ability of ecologists to understandhow foodwebs are structured, how so manyinteracting species can coexist, and how thepatterning and strengths of these linkages de-termine the stability of foodwebs (2). The useof next-generation sequencing is emerging asa key tool for quantifying, with fine resolu-tion, the diet composition of consumers (3).By using these high-throughput techniqueson fecal samples from large African herbivorespecies to quantify their diets, Kartzinel et al.(4) provide important insights into foodwebstructure and coexistence in one of the fewremaining terrestrial foodwebs that still hasits full complement of large mammals.In particular, Kartzinel et al. (4) extracted

DNA from the feces of seven large Africanherbivores—the African elephant, impala,two species of zebra, buffalo, Boran cattle,and dik-dik—within a 150 km2 portion ofKenyan savanna (Fig. 1). To determine dietsof each species, they obtained from 27 to 52fecal samples per species during a single sea-son. DNA metabarcoding allowed them toquantify the relative dietary abundances ofabout 100 different plant species or genera,thus demonstrating the efficacy of this ap-proach for coexisting mammals. They foundsurprisingly strong dietary differences amongthese herbivore species. This dietary nichedifferentiation can explain the stable coexis-tence of these competing species.An earlier study that used carbon isotopes

in feces was able to quantify abundances oftwo major groups of plants, grasses, andbrowse, and showed that many (but not all)herbivore species were separated along agradient defined by the ratio of these two

plant groups (5). Kartzinel et al. (4) have pro-vided the finest-resolution evidence to datedemonstrating that each large African herbi-vore species consumes a suite of plant speciesdifferent from the suite consumed by othercooccurring herbivore species.Why is this so important? The work of

Kartzinel et al. (4) suggests that the perfor-mance of a given herbivore species dependsnot on how much “forage” a grassland orsavanna may contain but on the actual abun-dances of those particular plant species onwhich that herbivore specializes. For exam-ple, the plains zebra and Grevy’s zebra bothmainly eat grass and thus would seem to bestrong competitors. However, Kartzinel et al.found that there were 14 grass species and aforb species upon which these two competi-tors were niche differentiated, with 10 ofthese plant species mainly eaten by Grevy’szebra and 5 mainly eaten by the plains zebra.Why does this dietary differentiation lead

to coexistence? Clearly, by eating differentplant species, each herbivore species reducesthe abundances of its own preferred foodplant species more than it reduces the abun-dances of the preferred food for the otherspecies. This dietary differentiation meets theclassic ecological criterion for the coexistenceof competing species: that each species in-hibits itself more than it inhibits the otherspecies. However, because of the multiplelinkages and potential feedback paths infoodwebs, cause and effect relations are rarelyso simple (6–9). These 15 plant species likelycompete with each other. When Grevy’s ze-bras are at high abundance, they will causetheir 10 favored plant species to be rarer. Thefive plant species preferentially consumedby the plains zebra might then increase inabundance because of reduced competition,which would benefit the plains zebra. A sim-ilar process could cause high densities ofplains zebras to benefit Grevy’s zebras. Theseindirect effects, mediated by competitive in-teractions among plants for their own limit-ing resources (water, nitrogen, phosphorus,light, etc.), would enhance the ability of twoseemingly close competitors to stably coex-ist. Indeed, the net effect of each of the zebra

species on the other might actually becomepositive and form an “indirect mutualism” ifthe competitive interactions among the 15plant species were strong (7).Achieving a more mechanistic and pre-

dictive understanding of foodwebs is one ofthe major challenges facing ecology. Afoodweb is a complex network influencedby the intensity of species interactions, whichthemselves quantitatively depend on thetradeoffs each species faces in dealing withtop-down forces (e.g., from its predators ordisease), bottom-up forces (from competition

Fig. 1. African mammals studied range in size fromelephants (Top), to Grevy’s zebra (Middle), to the dik-dik(Bottom). Images courtesy of Andrew Dobson (Depart-ment of Ecology and Evolutionary Biology, PrincetonUniversity).

Author contributions: D.T. and E.T.B. wrote the paper.

The authors declare no conflict of interest.

See companion article 10.1073/pnas.1503283112.

1To whom correspondence should be addressed. Email: tilman@umn.edu.

www.pnas.org/cgi/doi/10.1073/pnas.1509325112 PNAS Early Edition | 1 of 2

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for growth-limiting resources), and feedbackeffects that propagate through the network.Generalist consumers, such as large herbi-vores, can affect distant parts of a food web,yet a detailed understanding of the interact-ions between generalist consumers and theirfood species was generally out of reach untilthe development of next-generation sequenc-ing tools.Dietary differentiation, should it prove to

be of general importance in other mamma-lian foodwebs, could shed light not just onthe present-day ecology of these foodwebsbut also on the ecological constraints thatmay have structured the evolution of largemammalian herbivores and that perhapsdetermined which species were successfulmigrants between continents during the last20+ million years.Earth’s large terrestrial mammals evolved

on five continents but now mainly survive inAfrica. Africa’s high diversity resulted fromland bridges that periodically allowed mam-malian herbivores and predators that evolvedon one continent to move to another. A va-riety of mammals that evolved in NorthAmerica migrated to Asia and Africa, includ-ing camels, horses, and other grazing orbrowsing herbivore species and several scav-engers and predators. Other mammals of Af-rican or Asian origin similarly migrated intoNorth America. Despite apparent similaritiesamong species, the resident and invadingspecies coexisted (1, 10, 11). Such coexistenceis also common following migration by mol-lusks, plants, and other taxonomic lines tonew geographic regions (12–14).The work of Kartzinel et al. (4) raises the

interesting possibility that the species thatwere successful invaders had dietary prefer-ences different from the established specieson their new continent, and that such differ-ences allowed both their invasion and theircoexistence. After all, an invading speciesmust be able to survive and reproduceon the resources left unconsumed by the

species established in the shared habitat.There will generally be notable levels ofunconsumed resources if an invadingspecies has dietary preferences that aresignificantly different from those of theestablished species. Although we cannot goback in time, comparative studies of currentdiets of both herbivores and predators might

Kartzinel et al. provideimportant insights intofoodweb structure andcoexistence in one ofthe few remaining ter-restrial foodwebs thatstill has its full comple-ment of large mammals.shed considerable light on why some specieswere able to invade and coexist with, but notdisplace, the established species, and whyother species were not able to invade, andyet also were not displaced by species thatdid invade their habitat.The work of Kartzinel et al. (4) also raises

many questions. For instance, what con-straints and tradeoffs limit the breadth of di-ets and lead to specialization by herbivores?

Are dietary choices mainly the result of howplant species meet the nutritional needs of anherbivore? Or do diets reflect spatial patternsof cooccurrence of various plant species? Ormight the dietary choices of large herbivoresbe determined by the plant species that tendto cooccur in the sites that provide a givenspecies of herbivore with its greatest protec-tion from its predators?Each terrestrial foodweb is a 1,000+ piece

puzzle containing some subset of Earth’s>300,000 species of vascular plants, >25,000species of vertebrate herbivores, omnivores,and predators, and >1,000,000 species ofherbivorous, predatory, parasitoid, and pol-linating insects and arthropods (15). Allorganisms evolved in, and live in, suchfoodwebs, where, to survive, they must suc-cessfully compete for limiting resources anddefend themselves from predators, parasites,and diseases. The next-generation sequenc-ing approaches used by Kartzinel et al. (4)may finally allow us learn, at the level ofindividual species, how the constraints, trade-offs, and feedback effects species experiencein foodwebs interact to determine the di-versity, functioning, and stability of Earth’smost complex, and most threatened, terres-trial ecosystems.

1 Benton MJ (1996) Testing the roles of competition and expansionin tetrapod evolution. Proc Biol Sci 263(1370):641–646.2 Gross T, Rudolf L, Levin SA, Dieckmann U (2009) Generalizedmodels reveal stabilizing factors in food webs. Science325(5941):747–750.3 Pompanon F, et al. (2012) Who is eating what: Diet assessmentusing next generation sequencing. Mol Ecol 21(8):1931–1950.4 Kartzinel TR, et al. (2015) DNA metabarcoding illuminates dietaryniche partitioning by African large herbivores. Proc Natl Acad SciUSA, 10.1073/pnas.1503283112.5 Codron D, et al. (2007) Diets of savanna ungulates from stablecarbon isotope composition of feces. J Zool (Lond) 273(1):21–29.6 Holt RD (1977) Predation, apparent competition, and the structureof prey communities. Theor Popul Biol 12(2):197–29.7 Vandermeer JH (1980) Indirect mutualism: Variations on a themeby Stephen Levine. Am Nat 116(3):441–448.8 Holt RD, Lawton JH (1993) Apparent competition and enemy-freespace in insect host-parasitoid communities. Am Nat 142(4):623–645.

9 Polis GA, Anderson WB, Holt RD (1997) Toward an

integration of landscape and food web ecology: The dynamics

of spatially subsidized food webs. Annu Rev Ecol Syst

28:289–316.10 Flynn LJ, Tedford RH, Zhanxiang Q (1991) Enrichment and

stability in the Pliocene mammalian fauna of North China.

Paleobiology 17(3):246–265.11 Flannery T (2001) The Eternal Frontier: An Ecological History of

North America and Its Peoples (Text Publ, Melbourne).12 Vermeij GJ (1991) When biotas meet: Understanding biotic

interchange. Science 253(5024):1099–1104.13 Sax DF, Gaines SD (2003) Species diversity: From global decreases

to local increases. Trends Ecol Evol 18(11):561–566.14 Tilman D (2011) Diversification, biotic interchange, and the

universal trade-off hypothesis. Am Nat 178(3):355–371.15 Chapman AD (2009) Numbers of Living Species in Australia and

the World (Aust Biodiversity Inf Serv, Canberra, ACT, Australia),

2nd Ed.

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