EG35CH01-Strong ARI 13 September 2010 10:20 Human Involvement in Food Webs∗ Donald R. Strong1 and Kenneth T. Frank2 1Department of Evolution and Ecology, University of California, Davis, California 95616; email: [email protected] 2Bedford Institute of Oceanography, Ocean Sciences Division, Dartmouth, Nova Scotia B2Y 4A2, Canada; email: [email protected] Annu. Rev. Environ. Resour. 2010. 35:1–23 Key Words First published online as a Review in Advance on bottom-up, fisheries, intraguild predation, mesopredator, top-down, July 1, 2010 trophic cascade The Annual Review of Environment and Resources is online at environ.annualreviews.org Abstract This article’s doi: Human involvement in food webs has been profound, bringing about 10.1146/annurev-environ-031809-133103 enormous and disproportionate losses of large apex predators on land Copyright c 2010 by Annual Reviews. and in water. The losses have modified or even eliminated concatena- All rights reserved tions of indirect interactions propagating from predators to herbivores 1543-5938/10/1121-0001$20.00 to plants, inter alia. Food webs are a synthesis of bottom-up energy and ∗This article was co-authored by an employee of nutrient flow from plant producers to consumers and top-down regula- a British Commonwealth government as part of tion of producers by consumers. The trophic cascade is the simplest top- his official duties and is therefore subject to down interaction and accounts for a great deal of what is known about Crown Copyright. food webs. In three-link cascades, predators suppress herbivores, re- leasing plants. In longer cascades, predators can suppress smaller meso- by UNIVERSITY OF IDAHO LIBRARY on 03/21/11. For personal use only. predators, releasing their prey animals. Hunting, fishing, and whal- Annu. Rev. Environ. Resourc. 2010.35:1-23. Downloaded from www.annualreviews.org ing have brought parallel losses of large apex predators to food webs. Without apex predators, smaller mesopredators have often become su- perabundant, sometimes with unprecedented suppression of their prey, extinctions, and endangerment. Flourishing mesopredators also can re- verse the web regulation and suppress apex predators that have become rare owing to hunting and fishing. This can prevent fisheries recovery and lead to persistent alternative ecosystem states. Although food-web modules of large animals are increasingly well understood, the parts of webs consisting of small inconspicuous organisms, such as mutualists and parasites, and webs in obscure places, such as in the soil, are much of the challenge of future research. 1 EG35CH01-Strong ARI 13 September 2010 10:20 Contents Cod, Seabirds, Forage Fish, INTRODUCTION.............. 2 andPlankton............... 9 HUMANS ON THE SCENE . 3 Sharks, Rays, and Scallops . 10 THE STRUCTURE Upwelling Ecosystems . 10 OF FOOD WEBS . 4 Geese, Blue Crabs, and DirectInteractions............ 4 Alligators in Salt Marshes . 10 Aggregations of Functionally Big Predators, Big Herbivores, SimilarSpecies............. 5 and Vegetation . 11 IndirectInteractions........... 5 SIZEMATTERS................ 12 Bottom-Up Indirect DIVERSITY AND TROPHIC Interactions................ 5 STABILITY.................. 12 Top-Down Indirect OUT OF THE GUILDED Interactions................ 5 CAGE........................ 13 EVOLVING HUMAN Omnivory, Intraguild PERCEPTIONS ON Predation, and FOOD-WEB STRUCTURE . 6 Mesopredators............. 14 The American Alligator. 6 Mesopredator Release, LargeMarineEcosystems...... 6 Suppression, and Species Resolving the Influence Introductions . 14 of Top-Down Control. 8 Life-History Omnivory and TROPHIC CASCADES: Mesopredators in Large FROMWETTODRY....... 8 MarineEcosystems......... 14 Shallow Benthic Marine Alternative Ecosystem States . 15 Ecosystems................ 9 AVENUES TO RECOVERY? . 15 Continental Shelf and Inland VALUES, FOOD WEBS, AND SeaEcosystems............. 9 ECOSYSTEM SERVICES . 16 INTRODUCTION powerful food webs continue to be discovered in terrestrial systems (6–8), and the commonali- As the consummate omnivores, humans are ties among biomes indicate the scientific power by UNIVERSITY OF IDAHO LIBRARY on 03/21/11. For personal use only. predisposed to deep involvement in food webs. of food-web ecology and its application (9). Be- Humans prey upon animals at all trophic lev- Annu. Rev. Environ. Resourc. 2010.35:1-23. Downloaded from www.annualreviews.org yond this review are some emerging, exciting els, use almost half of the terrestrial earth to topics, for example, those of tiny organisms that raise livestock (1), consume a large fraction of play large roles in food webs in the soil (10) and the sea’s plants and animals (2), and appropriate among parasites and mutualists (11). We need more than a quarter of terrestrial net primary these food webs, but they do not need us (12), productivity for food (3). Although we set our and future work should think small as well as ideas in general food-web theory, our examples large. place somewhat greater emphasis on aquatic Food webs are the synthesis of bottom-up systems. This largely reflects our interests, the energy and nutrient flow from plant produc- huge ecosystem services from food webs of ers to consumers and top-down regulation of large marine systems (4), and the tendencies producers by consumers. The former has no in the literature (5). At the same time, diverse, 2Strong· Frank EG35CH01-Strong ARI 13 September 2010 10:20 feedback, and all negative feedback in food of labor, new weapons, and symbioses with dogs webs comes from the top down. The trophic penetrated deeper into prey food webs than ear- cascade is the simplest top-down interaction: lier people without these devices (14). Megafau- Trophic cascade: the (a) predators suppress herbivores and allow nal extinctions followed humans region by re- apex predator plants to thrive, and (b) apex predators suppress gion (15). Large animals went first. Bronze age suppresses its prey and smaller mesopredators, releasing herbivores to agriculturalists of China vanquished elephants, allows the prey of the suppress plants. Trophic cascades account for a rhinoceros, big cats, and others by hunting prey to increase great deal of what is known about the function- and forest clearing (16). Fire, deforestation, ad- Top-down ing of food webs on land and in the sea (13). vanced fishing methods (17), animal domesti- interactions: negative Humans persecute large species of animals cation, and early agriculture undoubtedly car- feedback upon producers from in the gamut of ecosystems, with huge food-web ried humans profoundly into food webs (18). In consumers, as in effects. At mid- and high latitudes, carnivore de- Roman Europe, protopastoralist hunters coex- carnivores diminishing crease can lead to irruption of large herbivores, isted with tarpan horses, aurochs, bison, and elk. populations of such as ungulates. The resulting heavy grazing The suppression of nondefended, slow grow- herbivores, which they can cascade into apparent competition among ing trees by these large herbivores, in food-web require for food plants that are differentially preferred, resistant, theory, cascaded through the vegetation by ap- Mesopredators: and tolerant of grazing.1 This string of indi- parent competition. The result was likely open animals that are smaller than apex rect interactions has shifted the constitution of parklands, thorny shrubs, and grasses with basal predators and are vegetation over large areas. Absent apex preda- meristems that resisted browsing (19). In recent suppressed by them; tors, such as wolves, big cats, or piscivorous fish, centuries, large terrestrial predators, such as the without apex the numbers of smaller mesopredators, such as American alligator (20), wolves, large cats, and predators, coyote, skunks, and planktivorous fish, become large bears (21), were virtually or actually ex- mesopredators threaten smaller abnormally abundant. The prey of these, such terminated from areas where humans or agri- animals as rare, endangered, and sensitive animals, are culture were dense. then depressed. In America, pre-Colombian early agricul- Many of the changes brought to food webs ture simplified the flora and subsidized garden by humans will never be reversed. Extinct key hunting (animals were attracted to and were species cannot be replaced, and people do not hunted in cultivated fields and gardens), and desire to live closely with large fierce ani- sophisticated fishing endeavors depleted fauna mals. Fisheries recovery by definition requires around population centers (22). Dense popula- reestablishment of the food web on which the tions of shore dwellers reduced valued species, target species depend. In some cases, remedia- such as the sea otter, and thrust human influ- tion is conceivable. In others, biological or so- ence multiple trophic levels into food webs (23). cial impediments augur for pessimism. Seafaring colonists and explorers from Europe by UNIVERSITY OF IDAHO LIBRARY on 03/21/11. For personal use only. caused the famous rapid, global extinctions of species, such as Steller sea cow and the great auk Annu. Rev. Environ. Resourc. 2010.35:1-23. Downloaded from www.annualreviews.org HUMANS ON THE SCENE (24). With fossil-fueled vessels, fishermen cap- Human influence in food webs accelerated with tured a more diverse fauna at far higher rates each technological advancement and increase in than the early wind-powered craft (25). The population. Warmly clad hunters with division magnitude of twentieth century harvest would have made