Evolutionary consequences of food chain length in kelp forest communities.

Kelp forests are strongly influenced by macroinvertebrate grazing on fleshy macroalgae. In the North Pacific Ocean, sea otter predation on macroinvertebrates substantially reduces the intensity of herbivory on macroalgae. Temperate Australasia, in contrast, has no known predator of comparable influence. These ecological and biogeographic patterns led us to predict that (i) the intensity of herbivory should be greater in temperate Australasia than in the North Pacific Ocean; thus (ii) Australasian seaweeds have been under stronger selection to evolve chemical defenses and (iii) Australasian herbivores have been more strongly selected to tolerate these compounds. We tested these predictions first by measuring rates of algal tissue loss to herbivory at several locations in Australasian and North Pacific kelp forests. There were significant differences in grazing rates among sea otter-dominated locations in the North Pacific (0-2% day-1), Australasia (5-7% day-1), and a North Pacific location lacking sea otters (80% day-1). The expectations that chronically high rates of herbivory in Australasia have selected for high concentrations of defensive secondary metabolites (phlorotannins) in brown algae and increased tolerance of these defenses in the herbivores also were supported. Phlorotannin concentrations in kelps and fucoids from Australasia were, on average, 5-6 times higher than those in a comparable suite of North Pacific algae, confirming earlier findings. Furthermore, feeding rates of Australasian herbivores were largely unaffected by phlorotannins, regardless of the compounds' regional source. North Pacific herbivores, in contrast, were consistently deterred by phlorotannins from both Australasia and the North Pacific. These findings suggest that top-level consumers, acting through food chains of various lengths, can strongly influence the ecology and evolution of plantherbivore interactions.

What was natural in the coastal oceans?

Humans transformed Western Atlantic coastal marine ecosystems before modern ecological investigations began. Paleoecological, archeological, and historical reconstructions demonstrate incredible losses of large vertebrates and oysters from the entire Atlantic coast. Untold millions of large fishes, sharks, sea turtles, and manatees were removed from the Caribbean in the 17th to 19th centuries. Recent collapses of reef corals and seagrasses are due ultimately to losses of these large consumers as much as to more recent changes in climate, eutrophication, or outbreaks of disease. Overfishing in the 19th century reduced vast beds of oysters in Chesapeake Bay and other estuaries to a few percent of pristine abundances and promoted eutrophication. Mechanized harvesting of bottom fishes like cod set off a series of trophic cascades that eliminated kelp forests and then brought them back again as fishers fished their way down food webs to small invertebrates. Lastly, but most pervasively, mechanized harvesting of the entire continental shelf decimated large, long-lived fishes and destroyed three-dimensional habitats built up by sessile corals, bryozoans, and sponges. The universal pattern of losses demonstrates that no coastal ecosystem is pristine and few wild fisheries are sustainable along the entire Western Atlantic coast. Reconstructions of ecosystems lost only a century or two ago demonstrate attainable goals of establishing large and effective marine reserves if society is willing to pay the costs. Historical reconstructions provide a new scientific framework for manipulative experiments at the ecosystem scale to explore the feasibility and benefits of protection of our living coastal resources.