HSS organized the food chain into three trophic levels. At the lowest trophic level they put producers (plants), with consumers (herbivores) at the next higher trophic level and predators at the top—as in Elton's food pyramid. Resources limit each trophic level. HSS noted interspecific competition among members of each level and concluded that because herbivores are seldom food limited, they appear to be most often predator limited and thus unlikely to compete for common resources. They offered the example of the vast carbon deposits that had accumulated globally as evidence that herbivores historically have been limited by predation, and they provided cases of the direct effect of predator removal on herbivore populations, such as the mule deer (Odocoileus hemionus) herd irruption on the Kaibab Plateau. This deer population, which lived on the northern rimof the Grand Canyon in Arizona, increased sharply almost immediately after extirpation of wolves (Canis lupus) and substantial removal of cougars (Puma concolor) in the 1920s, with estimates of deer numbers ranging from 4,000 in 1908 to 30,000 from 1923 through 1930. The powerful ramifications of HSS' hypothesis —that predators influence community dynamics at all trophic levels—inspired vital new hypotheses about community ecology.
Trophic cascades are based on HSS' three trophic levels (an odd number), in which a top predator consumes herbivores at the next lower level, and that in turn affects vegetation at the next level below. These cascades are essentially the indirect effects of predation. Direct effects occur via a predator killing prey, while indirect effects are mediated by a third species. An example would be the indirect effects of sea stars on vegetation in the rocky intertidal zone caused by changes in mussel density via predation. In some systems indirect effects of predation can also arise as a result of behavioral changes by prey in response to the threat of predation, which we will further explore in this chapter. In all cases, indirect and direct effects of predation interact to structure ecosystems.
Aldo Leopold was one of many who contributed to this more enlightened perspective, as was Elton. Although Elton and Leopold identified trophic cascades in primarily terrestrial systems, such as the Kaibab Plateau and northern Mexico, today the majority have been observed in aquatic systems. The sea otter (Enhydra lutris), sea urchin (Strongylocentrotus polyacanthus), and kelp (Laminaria spp. and Agarum cribrosum) cascade reported by marine ecologist James Estes in Alaska provides a classic example. When Vitus Bering explored the North Pacific in 1741 he found shorelines teeming with sea otters. By 1911 they were nearly extinct. Enough remained in sheltered rocky pockets along the coast that by the 1960s the otter population had recovered in places. Otters have a varied carnivorous diet and prey heavily on sea urchins. In areas without otters Estes found herbivorous sea urchins thickly carpeting the ocean floor—and no kelp. On reefs with otters he found a lush, green kelp forest and low numbers of sea urchins.
Top-Down versus Bottom-Up
Not everyone bought the green world hypothesis. William Murdoch's counterargument, termed the plant self-defense hypothesis by conservation biologist John Terborgh, suggests that food (bottom-up control) has the strongest influence, that the world may be green because not all plants are palatable to herbivores, and that predators are unnecessary for ecosystem regulation. Or, as evolutionary ecologist Stevan Arnold puts it, the world is green, but that doesn't mean it's edible.
Murdoch asserted that food shortage and plant defense strategies may be regulating herbivore numbers. He hypothesized that while plants are essential for the survival of the trophic levels above, the reverse is not true. He and other critics of the green world hypothesis, such as ecologists Donald Strong and Gary Polis, suggested that HSS' failure to address the full complexity of systems, which includes omnivory, weakened their hypothesis. Some have identified HSS' tri-level trophic model as a hypothetical construct because in the real world food webs are not so tidy and can have fewer or more than three levels. Still others, such as conservation biologist Michael Soulé, believe that top-down versus bottom-up, like all dualisms, is false, because the natural world is complex and bottom-up forces (nutrient flow) interact with top-down forces (the effects of predation). Other scientists, such as Rolf Peterson, concur; in the wolf–moose–balsam fir system he studies in Isle Royale National Park, it's never one or the other but a synergy of the two.