Fungal Farming in a Snail

Fungal farming in a snail Brian R. Silliman*† and Steven Y. Newell‡ *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 Edited by Robert T. Paine, University of Washington, Seattle, WA, and approved October 21, 2003 (received for review August 14, 2003) Mutualisms between fungi and fungus-growing animals are model create and maintain longitudinal wounds on the leaf surface with systems for studying coevolution and complex interactions be- their radulae (typically, wounds eventually go all of the way tween species. Fungal growing behavior has enabled cultivating through the leaf; see Fig. 1) and feed on the senescent material animals to rise to major ecological importance, but evolution of surrounding those wounds [radulations (20)]. Microscopic ex- farming symbioses is thought to be restricted to three terrestrial amination of injured leaves indicates that ascomycete fungi insect lineages. Surveys along 2,000 km of North America’s Atlantic [probably primarily ascomycetes in the genera Phaeosphaeria coast documented that the marine snail Littoraria irrorata grazes and Mycosphaerella (22, 23)], the snails’ preferred food (16, 17), fungus-infected wounds on live marsh grass throughout its range. are more abundant in snail-maintained wounds than on green Field experiments demonstrate a facultative, farming mutualism leaf surfaces and fungi dominate the microbial communities that between Littoraria and intertidal fungi. Snails graze live grass invade radulated Spartina leaves [bacteria are typically Ͻ5%, by primarily not to feed but to prepare substrate for fungal growth mass, of the microbial community on decomposing, standing and consume invasive fungi. Fungal removal experiments show Spartina leaves (22, 23)]. Field observations also suggest that that snails and fungi act synergistically to suppress marsh grass snails concentrate deposition of nitrogen- and hyphae-rich fecal production. These results provide a case of fungus farming in the pellets (24, 25) on fungus-invaded wounds [Littoraria feces are marine environment and outside the class Insecta and reveal a typically dense with fungal hyphae, and snails digest only Ϸ50% previously undemonstrated ecological mechanism (i.e., facilitation of the mycelium they consume (25)]. Based on these preliminary of fungal invasion) by which grazers can exert top-down control of findings, we hypothesize that (i) Littoraria promote fungal marine plant production. growth on live Spartina plants through grazing activities and ECOLOGY direct application of fecal pellets and that this growth promotion top-down control ͉ salt marshes ͉ fungi–animal interactions has a positive effect on snail growth; and (ii) fungi benefit from snail wound-grazing by gaining access to nutritious and relatively elationships between fungus-farming animals and fungi are defenseless inner plant tissues and by receiving supplements Rmodels of how coevolution can drive positive interactions (potentially nutrients and͞or propagules) from snail feces. and establish some species as ecosystem engineers (1–5). These Removal experiments demonstrate that Littoraria’s unique intimate mutualisms can be obligate for both animal and fungal grazing behavior suppresses Spartina growth and that snail species and are distinguished by elaborate behavioral adapta- consumption accounts for Ͻ5% of biomass reductions (18, 19). tions of participant animals to a life of fungal cultivation (1–3). Given these findings and the observation that potentially growth- Around 40–60 million years ago, three distinct insect lineages, suppressing fungi are abundant on snail-induced wounds, we ants, termites, and beetles, independently evolved the charac- further hypothesize that (iii) the primary mechanism of snail teristic of cultivating fungi for nutrition (6). Fungus-growing control of plant growth is tissue death caused by the facilitation behavior evolved only once in ants (7) and termites (8), whereas of fungal invasion. it evolved at least seven times in beetles (9–11). There has been remarkable radiation within these insect lineages, and evolution Methods of fungus-growing behavior is thought to be a major force driving Patterns in Snail Grazing. To examine the geographical extent of each radiation (6, 7). Development of fungal cultivation has also Littoraria wound-grazing, we surveyed 16 marshes (haphazardly enabled these insects to rise to major ecological importance in chosen on a map) along 2,000 km of southeast shoreline in eight a variety of terrestrial communities (e.g., forests and grasslands), different states in September 2002 (Table 1). Ten 0.25-m2 where they can strongly regulate ecosystem processes and com- quadrats in each marsh were randomly placed in the short-form munity structure through their farming activities (4, 6, 12, 13). Spartina zone, and the total length of the radulations per stem Despite obvious success afforded by fungus-growing behavior, was measured (18). evolution of fungiculture is thought to have occurred only in Based on these observations from the southeast coast, we these three distinct, terrestrial insect lineages (6). surveyed and conducted experiments in marshes on Sapelo In detritus-based marine systems, fungi that grow on dead Island, Georgia, at the University of Georgia Marine Institute. plant material are a primary food source for invertebrate grazers Initially, we quantified our preliminary observations that fungi (14–17). Fungal supply to grazers is thought to be a bottom-up are abundant on radulations and that snails concentrate fecal process largely dependent on the availability of dead plant mass deposition on grazer-induced wounds. In May 2000, we sampled (14, 15). However, significant abrasion by grazers can facilitate 16 uninjured (i.e., completely green with no abrasions) and 16 both the invasion and growth of nutritious fungi (18). Marine radulated [i.e., completely green except for snail grazing scars detritivores (e.g., snails and crabs) capable of shredding and (Fig. 1)] Spartina leaves and analyzed them for fungal biomass by cutting live plant material might therefore have the potential to using ergosterol-proxy techniques (23). Each leaf was collected initiate and encourage the growth of fungi on living plant from a different Spartina stem, and stems were located at least substrates. 3 m apart. We sampled the first 16 leaves of each leaf type we In salt marshes along U.S. southeast coasts, the marsh snail encountered while walking a 200-m line transect through the Littoraria irrorata is one of the most abundant grazers and short-form Spartina zone. Leaf sections (5 cm in length) were cut commonly occurs at densities ranging from 40 to 500 individuals per m2 (19–21). Long thought to be strictly a detritivore, recent research has shown that Littoraria actively grazes live salt marsh This paper was submitted directly (Track II) to the PNAS ofﬁce. cordgrass, Spartina alterniflora (20). When grazing live plants, †To whom correspondence should be addressed. E-mail: brian࿝[email protected]. however, snails do not consume live tissue directly; instead, they © 2003 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.2535227100 PNAS ͉ December 23, 2003 ͉ vol. 100 ͉ no. 26 ͉ 15643–15648 Downloaded by guest on September 27, 2021 Table 1. Snail grazing intensity on green leaves of salt marsh were designed to elucidate potential causal processes underlying cordgrass in southeast salt marshes those patterns. Radulations, State cm per stem Effects of Snail Grazing Activities on Fungal Biomass. To test the hypothesis that snails facilitate fungal invasion through grazing Delaware 8.6 Ϯ 1.8 activities, we measured the effects of snail presence and simu- Maryland 10.3 Ϯ 1.4 lated snail grazing (i.e., razorblade cuts) on fungal growth in Virginia 16.7 Ϯ 2.3 green Spartina leaves in a 2-month caging experiment. In Feb- Ϯ North Carolina 12.8 1.6 ruary 2001, before snails began to graze live marsh grass (20, 21), Ϯ South Carolina 9.3 2.8 in the intermediate height-form Spartina zone, we established Ϯ Georgia 28.3 2.3 replicated (n ϭ 6) 1-m2 galvanized mesh cages (20) assigned to Ϯ Florida 13.6 3.5 the following treatments: control (Ϸ220 snails per m2), snail Ϯ Louisiana 9.8 2.7 removal, and snail removal plus simulated grazing. We simulated Data are means Ϯ SE and represent pooled data from two marshes in each snail grazing on uninjured green Spartina by using razorblades to state. make longitudinal cuts that went all of the way through the leaves. Every week, the average total length of radulations per stem in the control snail treatments was quantified. We then from each sample, all fecal pellets were removed, and, because replicated those radulation distributions (i.e., the same average of logistical constraints (i.e., the constraint of having to use short number of radulations) on all stems in simulated grazing treat- leaf sections with available lab equipment combined with the ments. After 2 months, we measured fungal biomass on respec- difficulty of detecting ergosterol concentrations in small sam- tive green leaf types (uninjured, radulated, and simulated scar) ples), four sections of each leaf type, uninjured or radulated, from each treatment (n ϭ 2 leaves per leaf type per replicate) by were pooled for analysis (n ϭ 4 per treatment). We also using the ergosterol methods described above (23). We randomly quantified fecal pellet density on 10-cm-long midleaf sections of pooled the two leaves from each of our six replicates into three 300 uninjured and 300 radulated green leaves sampled from groups of four leaves each for analysis because of logistical independent stems. We counted pellets on the 10-cm-long constraints (see above) of the ergosterol extraction technique. radulations themselves, not on green tissue surrounding the area For statistical analysis, then, n ϭ 3 per treatment. Snail densities (see Fig. 1B). On undamaged leaves, we counted fecal pellets on were monitored weekly (20). similarly sized and oriented areas.

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