Chemical defenses against herbivores and fungi limit establishment of fungal farms on salt marsh angiosperms

Within coastal salt marshes of eastern North America, the snail Littoraria irrorata facilitates fungal growth on live plant tissues to gain access to a palatable and nutritious fungal food source. This snail-fungal mutualism increases exposure of the foundation species Spartina alterniflora to infection, whereas fungal farming on other local marsh plants is rarely observed. We sought to identify traits from five salt marsh angiosperm species, such as chemical defenses against snails or fungi, which restrict L. irrorata habitat choice, feeding patterns, and ability to establish fungal farms. In the field and in mesocosm experiments, L. irrorata densities were significantly higher on S. alterniflora than on other available plants, indicating that S. alterniflora is a favored habitat for L. irrorata. Highly avoided plants were rich in chemical defenses that rendered these plants unpalatable to L. irrorata in feeding trials, whereas S. alterniflora extracts deterred L. irrorata feeding only slightly. Removal of plant structure did not alter L. irrorata preferences indicating a negligible role of tissue toughness as a defense. All plants in our study produced compounds that inhibited growth of fungi typically farmed by L. irrorata, although S. alterniflora antifungal compounds were weaker than those of other plant species, consistent with the observation of fungi only on wounded S. alterniflora tissues. We propose that the weak chemical defenses produced by S. alterniflora make it a preferred plant for fungal farming, whereas less abundant species that invest in potent chemical defenses against grazers and fungi are not as frequently colonized, consumed, or subjected to fungal farming by L. irrorata. The inability of S. alterniflora to adequately deter herbivores and pathogens may lead to increasing losses in plant biomass and reduce the ecosystem services provided by this foundational species.