PROVIDENCE, R.I. -- A startling mutual-aid society is linking fungus and snails in marine ecosystems, according to a study led by a Brown University biologist. The study presents the first evidence that a species of marine snail engages in a previously undemonstrated form of food acquisition and ecological control by initiating and encouraging the growth of fungi, its preferred food, on live marsh grass. Infestation by fungi greatly slows the growth of the grass.
In surveys conducted along 2,000 kilometers of salt marshes on the southern U.S. shoreline, the researchers observed that the snail, Littoraria irrorata, actively grazes a live salt-marsh cordgrass. As the snail crawls along the grass surface, it scrapes grass tissue with its band of saw-like teeth and creates longitudinal cuts in leaf surfaces, making a much larger meal possible. While it travels, the snail also deposits feces laden with fungal spores and nutrients into the sensitive inner-tissue of the leaf, effectively stimulating and fertilizing fungal crops.
The result of snail grazing on marsh grass surface is an infestation of fungi, a major diet component for the snail, and the slowing of marsh grass growth.
"In its manner of manipulating fungi, the snail is conducting a low-level form of food production," said lead scientist Brian Silliman, an ecology and evolutionary biology doctoral candidate at Brown University. "This is fungal farming in a completely new group (phylum) of organisms and the first demonstration in the marine environment."
This method of agriculture – called "fungiculture" – was thought to occur only in three distinct insect lineages, including certain ants, termites and beetles. The development of fungus-growing behavior has enabled these insects to rise to major ecological importance in land communities where they can strongly affect ecosystem process and community structure through their farming activities.
The new study, which appears in the current Proceedings of the National Academies of Sciences, establishes the mechanism by which the snail, among the most abundant grazers found in southern salt marshes, is able to affect its ecosystem. Silliman authored the study with Steven Newell of the University of Georgia Marine Institute.
Southern salt marshes have been among the most productive grasslands in the world. In addition, they serve important ecological functions, including tempering coastal flooding, filtering mainland run-off, and acting as nurseries for commercially important fish and other species.
Earlier research by Silliman and others observed that the snail, long thought to eat only dead or dying plant materials, also grazed live salt-marsh cordgrass. A 2002 collaboration with another Brown researcher indicated that the snail participates in a top-down "trophic cascade" in which the control of grazers (snails) by predators (crabs) is a major determinant of plant growth in the marine environment.
The earlier findings suggested that the over-harvesting of snail predators may be an important factor contributing to the massive die-off of salt marshes across the southeastern United States in recent years. According to Silliman, several other theories have been advanced to help explain marsh die-off, including drought and the dispersion of a fungal pathogen.
By suggesting a synergy between fungus and snail that leads to increased growth for both and diminished growth for the host marsh grass, the new study may add to discussion of the role of fungi in this environmental change.
In the laboratory, the researchers observed that snails fed fungus and marsh grass were more robust than snails fed marsh grass leaves alone. In addition, field experiments determined that the fungus was more abundant in the snail-maintained wounds than on the leaf surfaces. Fungal removal experiments indicated that fungal invasion of the leaves was a greater determinant of grass deterioration than was snail grazing.
The snail is the first gastropod, or mollusk, shown to exhibit fungal-farming behavior, Silliman said. However, the researchers note that given the biological simplicity of this low-level fungal production, fungal farming may be more geographically and phylogenetically widespread than presently envisioned, especially in systems where fungal spores are abundant, grazers can manipulate fungus growing media and fungus is a major diet of consumers.
The National Science Foundation, Environmental Protection Agency (Science To Achieve Results fellowship), and the National Oceanic and Atmospheric Association Narragansett Bay Fellowship funded the study.
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