Fungal farming in a snail

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.

Fig. 1.

(A) Snail fecal pellets at high density (>40 pellets; average densities were found to be 22.75 pellets per 10 cm of radulation; see Results) concentrated on a snail-induced wound on a live Spartina leaf. Note the fungal concentration (dark area) along the radulation edges. A leaf with fecal pellets was collected at night and photographed the next morning. (B) Littoraria on a Spartina leaf grazing a radulation. The majority (>80%) of snail-induced wounds on cordgrass extend through the leaf, as is the case in this picture.

Fig. 4.

Interactive and separate effects of snail presence and fungicide on the total length of grazer-induced wounds per stem (A), fungal biomass [μg of ergosterol (erg.) per cm² of leaf blade] on green leaves (B), and Spartina aboveground biomass (C). Different letters denote significant pairwise differences at P < 0.05 in mean values as determined from Tukey's post hoc test. Error bars represent ± SE.

Fig. 2.

(A and B) Fungal abundance [μg of ergosterol (erg.) per cm² of leaf blade] in naturally occurring uninjured and radulated green Spartina leaves (A) and experimentally generated uninjured (snail removal treatments), snail-grazed (control snail treatments), and razor-cut (simulated snail grazing treatments) green leaves (B). (C) Juvenile snail growth rates on each experimentally generated green leaf type. Different letters denote significant pairwise differences at P < 0.05 in mean values as determined from Tukey's post hoc test. Error bars represent ± SE.

Fig. 3.

Response of fungal growth [μg of ergosterol (erg.) per cm² of leaf blade] to snail fecal pellet addition on simulated grazing scars on green Spartina leaves. Error bars represent ± SE. *, P < 0.05, paired t test.