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Disease and the Dynamics of Food Webs

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1PrimerDisease and the Dynamics of Food WebsWayne M. Getz1,2*1 Department of Environmental Science, Policy and Management, University of California Berkeley, Berkeley, California, United States of America, 2 Mammal ResearchInstitute, Department of Zoology and Entomology, University of Pretoria, Pretoria, South AfricaFifty years ago, ecologists Hairston, Smith, and Slobodkin [1]proposed the provocative idea that herbivores are limited bypredators rather than food. If true, the implications are that we livein a green (lots of uneaten plants) rather than a brown (the bareearth is visible due to overgrazing) world [2]—which is largely,though not universally true. This idea has come to be known as thetrophic cascade hypothesis (TCH), and is a seminal idea in thesubfield of ecology known as foodweb theory [3]. The TCHgenerated numerous studies on whether such tritrophic, and evenlonger aquatic [4], food chains are truly controlled from the topdown (the TCH) or from the bottom up through food-limitingherbivore populations [2,5], even if only at critical points in time.The importance of such studies to our understanding of theresponses of ecosystems to land use and climate change, as well asto the ecological implications of emerging disease, will becomeapparent in this primer.Like all dialectical arguments, the debate on whether foodchains are controlled from the ‘‘top down’’ or ‘‘bottom up’’ is onlyuseful for finding the relative influence of both types of control asthey may relate to other ecological, environmental, and particu-larly seasonal factors. The world, of course, is much morecomplicated in that identifiable food chains are hardly eversufficiently isolated from other ecological processes (Figure 1) [6]for models of such processes to make reliable long-termpredictions. Omnivores [7], for example, distort food chains byfeeding at several trophic levels, whereas microbes feed at alllevels: at the bottom as detritivores [8], without which all trophicchains would soon run out of essential resources, and at otherlevels as parasites and pathogens, often constituting a substantialfraction of ecosystem biomass [9].How To Model Trophic ChainsMathematical models are used to explore questions regardingwhat factors tip the balance in favor of top-down or bottom-upcontrol. The most versatile models from a trophic point of view arethose that take a consumer-resource perspective, irrespective of theparticular trophic level under consideration (Box 1): suchformulations have utility in modelling how plants extract photonsand nutrients from the environment, herbivores consume plants,carnivores consume herbivores, insects consume insects, fishconsume fish, and macroparasites (e.g., nematodes, cestodes)extract biomass from most vertebrates. By setting up equationsthat for each component of a foodweb account for the dominantlinks among all components, scientists can build models of trophicdynamics that address a plethora of interesting questions. Thisincludes the focal question addressed by Holdo et al. in this issue ofPLoS Biology [10]: in the competition between trees and grass forspace, what is the relative importance of top-down effects exertedby fire and elephants versus bottom-up effects of rainfall and risingCO2. Further, and more specifically (as illustrated in Holdo et al.’sFigure 4B), they assess the relative importance of the human-elephant-tree cascade (influenced by poaching) compared with therinderpest-wildebeest-fire-tree cascade that has resulted from thenear eradication of rinderpest—a highly contagious measles-likevirus the infects cattle and buffalo, giraffe, kudu, wildebeest, andother artiodactyls—through the vaccination of cattle in east Africain the early 1960s.Episodic Versus Steady ProcessesHoldo et al. [10] highlight two very different classes of processesthat potentially influence the ecological state or regime in which aparticular system resides [11]—for example, whether a particularecosystem functions predominantly as a grassland with isolatedtrees or as a woodland interspersed with patches of grass, with allthe attendant differences in guilds of birds, mammals, and insectsthat are supported, not to mention plants, fungi, and bacteria.Citation: Getz WM (2009) Disease an d the Dynamics of Food Webs. PLoS Biol 7(9):e1000209. doi:10.1371/journal.pbio.1000209Published September 29, 2009Copyright: ß 2009 Wayne M. Getz. This is an open-access article distributedunder the terms of the Creative Commons Attribution License, which permitsunrestricted use, distribution, and reproduction in any medium, provided theoriginal author and source are credited.Funding: This work was funded by a US National Science Foundation andNational Institutes of Health Ecology of Infectious Disease programme grantGM083863-01. The funders had no role in study design, data collection andanalysis, decision to publish, or preparation of the manuscript.* E-mail: [email protected] provide a concise introduction into an important aspect of biologyhighlighted by a current PLoS Biology research article.Figure 1. Disease mediation of a lion-zebra-grass tritrophicchain in the Etosha National Park ecosystem in Namibia. Theanthrax pathogen, Bacillus anthracis, accounts for a substantial numberof deaths of zebra and other herbivores (including springbok, elephant,wildebeest), thereby providing a largess of resources for the scavengercommunity dominated by jackals, hyenas, and several species of vulturesand corvids, not to mention lions themselves. (In the lower right picture isa zebra carcass a few hours after death from anthrax with vultures andjackals the first to arrive on the scene). Thus the microbe B. anthracis playsan important role in determining the ultimate structure of the Etoshaherbivore-carnivore-scavenger foodweb.doi:10.1371/journal.pbio.1000209.g001PLoS Biology | www.plosbiology.org 1 September 2009 | Volume 7 | Issue 9 | e1000209The first class of processes are episodic perturbations such asoutbreaks of fires and diseases that ‘‘burn’’ their way throughsystems, or environmental switches such as those driven by ENSO(El Nin˜o-Southern Oscillation); although we need to bear in mindthat what might be episodic and intense at one spatial scaleappears as more regular and less intense at a larger spatial scale.Irregular episodic events (best characterized in terms of probabilitydistributions describing the frequencies and intensities of occur-rences) can


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