Fungal farming in a snail
- *Department of Ecology and Evolutionary Biology, Box G-W, Brown University, Providence, RI 02912; and ‡University of Georgia Marine Institute, University of Georgia, Sapelo Island, GA 31327
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Edited by Robert T. Paine, University of Washington, Seattle, WA, and approved October 21, 2003 (received for review August 14, 2003)
Abstract
Mutualisms between fungi and fungus-growing animals are model systems for studying coevolution and complex interactions between species. Fungal growing behavior has enabled cultivating animals to rise to major ecological importance, but evolution of farming symbioses is thought to be restricted to three terrestrial insect lineages. Surveys along 2,000 km of North America's Atlantic coast documented that the marine snail Littoraria irrorata grazes fungus-infected wounds on live marsh grass throughout its range. Field experiments demonstrate a facultative, farming mutualism between Littoraria and intertidal fungi. Snails graze live grass primarily not to feed but to prepare substrate for fungal growth and consume invasive fungi. Fungal removal experiments show that snails and fungi act synergistically to suppress marsh grass production. These results provide a case of fungus farming in the marine environment and outside the class Insecta and reveal a previously undemonstrated ecological mechanism (i.e., facilitation of fungal invasion) by which grazers can exert top-down control of marine plant production.
Footnotes
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↵ † To whom correspondence should be addressed. E-mail: brian_silliman{at}brown.edu.
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This paper was submitted directly (Track II) to the PNAS office.
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↵ § Strict criteria for “low,” “medium,” and “high” levels of fungal farming have not been established and have only recently been suggested (27). Although we argue that snail fungus-growing behavior represents low-level farming, this could be revised based on future results. Our findings are relatively silent as to whether growth-promotional effects of snails are adaptations or mere by-products. If they are by-products, then this snail–fungus interaction may be more accurately classified as protofarming behavior. In addition, because we have no evidence that either fungus or snails have undergone selection for participation in this interaction and both organisms survive independent of the relationship, we have classified this positive interaction as a facultative mutualism.
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↵ ¶ We did not determine whether snails purposefully deposited fecal pellets on grazer-induced wounds or, rather, that pellets were simply concentrated on wounds because of increased time spent by snails feeding in those areas. If the former is found to be true, then a stronger case for higher-level fungal cultivation [given its current definition (27)] can be made, because snail behavior would then seem to have evolved for “planting” or “manuring” by means of feces.
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↵ ∥ Mechanisms of growth enhancement are not exactly known, but nutrient transfer from fecal pellets is likely, given that snail pellets are high in nitrogen content and fungal growth on cordgrass is nitrogen-limited (17, 18, 22, 23). Pellets could additionally provide fungal propagule supplements, given that 50% of mycelium in snail feces typically remains undigested and intact (25).
- Copyright © 2003, The National Academy of Sciences
