An "Indirect Commensalism" between Marine Herbivores and the Importance of Competitive Hierarchies

Recent theory has suggested that in systems in which resource taxa compete, the abundance of a consumer specialized on one prey should be positively affected by the presence of a specialized consumer of the other prey. We have shown that the type of competition between prey (i.e., hierarchical vs. symmetrical) strongly affects the nature of the interaction between consumers. In the low intertidal zone on San Juan Island, Washington, two species of acmaeid limpets overlap substantially in habitat and food use with the large chiton Katharina tunicata. The limpets in this region consume microalgae, especially diatoms, while the chiton is a generalist, eating both microalgae and macroalgae. The experimental removal of Katharina from two large areas resulted (over 3 yr) in a dramatic rise in macroalgal cover and the disappearance of limpets. Artificially increased densities of Katharina at another site led to greater limpet abundances and increased reproductive output of both limpets and chitons. The probable mechanism for these changes is the ability of macroalgae to outcompete microalgae and monopolize the substratum, removing both the food and the habitat of the limpets. The specialist limpets thus depend on the generalist chiton to remove macroalgae and allow diatom growth. However, the hierarchical nature of the prey-prey competition and the ability of Katharina to consume the dominant prey prevents this dependence from being reciprocal. Such "indirect commensalisms" may be more common in nature than are "indirect mutualisms," which require specialized consumers feeding on prey that are of equal competitive vigor.