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.top-down control ͉ salt marshes ͉ fungi-animal interactions

Farming of a defensive fungal mutualist by an attelabid weevil

“…The marine snails Littoraria irrorata farm intertidal fungi on marsh grass (Silliman and Newell, 2003), the fungus-growing lizard beetle Doubledaya bucculenta make a fungal garden inside bamboo (Toki et al, 2012), and the attelabid weevils inoculate symbiotic fungus on leaf-rolls (Sakurai, 1985). In these systems, the elaborate structural and behavioral adaptations of the insects have been involved for fungal cultivation.…”

“…In protofungiculture stystems, the farming strategies are relatively simpler. The Littoraria snails promote fungal growth on live Spartina plants through grazing activities and direct application of fecal pellets but do not utilize intricate pest management or inoculating techniques (Silliman and Newell, 2003). The attelabid weevils put great effort into planting the fungal garden (by forming leaf-rolls and inoculating them with spores) but do nothing more to maintain the gardens.…”

“…The capacity to grow fungus has not been restricted to insect lineages; also snails have been discovered to be nutritionally dependent on external fungal symbionts (Silliman and Newell, 2003).…”

“…Outside the class Insecta, marine snails farming intertidal fungi provide an example in the marine environment. Littoria snails (Littoraria irrorata) 'protofarm' fungi by creating plant wounds that become infected with fungal mycelia that are part of the snails' diet, but the snails do not actively inoculate plant wounds or otherwise garden the fungi (Silliman and Newell, 2003). The fungus-growing lizard beetle Doubledaya bucculenta transmits symbiotic yeast into bamboo internode cavities and disperses the yeast in the cavities to make gardens (Toki et al, 2013).…”

Habitat size, flora, and fauna: Interactions in a tidal saltwater marsh

“…Littoraria grazes on Spartina, removing both grass tissue and fungal biomass from the leaves (Haines and Montague, 1979;Graça et al, 2000, Silliman andNewell, 2003). Littoraria can exert significant top-down control on Spartina production through grazing (Silliman and Zieman, 2001;Silliman and Bertness, 2002).…”