In terrestrial systems, grazers can have large and diverse effects on plant communities. Studies across multiple habitats have demonstrated grazers’ ability to influence primary production (Vickery, 1972; Hik and Jefferies, 1990; Bruno et al., 2008; He and Silliman, 2016), leaf abscission rates (Mingo and Oesterheld, 2009), nutrient content in leaves (Zieman et al., 1984), flowering rates (Maschinski and Whitham, 1989; Brys et al., 2011), colonial propagation (Maschinski and Whitham, 1989), as well as plant diversity and succession (Huntly, 1991; Olff and Ritchie, 1998). Mechanisms of control can be direct, through the consumption of plant tissue, and/or through a myriad of indirect pathways. A powerful indirect pathway of grazer control on plant growth is facilitation of microbial infection in live plant tissues via grazer wounding (Taylor and Bardner, 1968; Smith and Odum, 1981; Turner, 1989; Furbish and Albano, 1994; Silliman and Newell, 2003; Daleo et al., 2009). For example, plant grazers, such as insects, can carry and facilitate invasion by microbial pathogens in agricultural crops, trees, and other plants (Linit, 1988; Pimentel, 1991; Eigenbrode et al., 2018). This grazer-pathogen-plant interaction often leads to suppressed plant growth and can make plants more susceptible to environmental stressors such as drought (Silliman, 2005; He et al., 2013).

In marine systems, grazers can similarly control many aspects of plant community structure and ecosystem function. Marine grazers have been shown to alter plant growth, reproduction, diversity, and plant-regulated nutrient cycling across virtually every marine ecosystem (Poore et al., 2012). Many of these studies recognize that grazer control of plant growth can occur through direct consumption of live plant tissue. For example, parrot fish consume macroalgae thus reducing competition between plants and algae (Valentine and Duffy, 2006; Mumby, 2009), crabs consume mangrove propagules leading to forest zonation patterns (Smith, 1987; Sousa and Mitchell, 1999), and snails and chitons rasp intertidal algae (Hawkins and Hartnoll, 1983). Additionally, in seagrass systems, it has been shown that urchins grazing seagrasses can lead to local extinction of seagrass beds (Camp et al., 1973; Valentine and Heck, 1991; Heck and Valentine, 1995), and dugongs and sea turtles grazing seagrasses can reduce seagrass shoot density and above and belowground biomass (Heinsohn and Birch, 1972; Ogden et al., 1983; Lanyon et al., 1989; Heck and Valentine, 2006; Larkum et al., 2006). Furthermore, other studies have shown that grazers can also control plant growth via indirect interactions, such as mesograzer facilitation of seagrass growth by ingesting epiphytic algae that would otherwise smother seagrasses (Orth et al., 1984).

However, only a few studies in marine systems have shown that grazer facilitation of disease in plants is an important mechanism of top-down control. In one example, research in salt marshes has shown that grazer facilitation of microbial infection in live plant tissue has negative consequences for plants (Silliman and Newell, 2003). Specifically, in southeastern U.S. salt marshes, the marsh periwinkle (Littoraria irrorata) has been shown to facilitate fungal infection in live smooth cordgrass (Spartina alterniflora). A series of experiments revealed L. irrorata, previously thought to be a detritivore specialist, grazes live S. alterniflora and generates open wounds that leaves the plant susceptible to fungal infection (Silliman and Zieman, 2001; Silliman and Newell, 2003). L. irrorata returns to grazed plants to consume fungi growing in wounds, exhibiting low-level fungal farming behavior. The result of this grazer-fungus interaction is decreased S. alterniflora growth and, at high snail densities, plant death. Fungal removal studies have demonstrated that microbial infection, not the direct consumption of live plant tissue, is the primary mechanism by which snails control plant growth (Silliman and Newell, 2003). This top-down fungal mechanism also occurs in Argentinian marshes, but with crabs as the primary facilitator (Daleo et al., 2009). Given these findings, and the abundance of grazers in marine systems, it is possible grazer control through microbial infection in marine plants is more common than currently thought.

In seagrass systems, small invertebrate grazers (e.g., amphipods, isopods, and gastropods, collectively called mesograzers) that eat plants and algae are of widespread importance (Brearley and Walker, 1995; Nakaoka et al., 2002; Fredriksen et al., 2004; Valentine and Duffy, 2006; Lewis and Boyer, 2014). However, most research testing for their top-down effects has focused on those grazer species that consume epiphytes growing on seagrass, rather than those that consume live seagrass directly. These studies have shown that epiphyte grazers often improve seagrass productivity by controlling the growth of competitively dominant algae, especially in eutrophic environments (Heck et al., 2000; Hughes et al., 2004; Reynolds et al., 2014; Campbell et al., 2018). In general, research on direct grazing (i.e., consumption of live plant tissue) of seagrass has typically highlighted the ability of vertebrates, such as fish, birds, sea turtles, and dugongs, to exert top-down control over seagrass (Valentine and Duffy, 2006; Kollars et al., 2017). Additionally, while there has been extensive research on certain invertebrate grazers, notably sea urchins, less work has explored the influence of small invertebrate grazers, such as snails, that feed directly on live seagrass and their cascading impacts on seagrass (Valentine and Heck, 1991; Alcoverro and Mariani, 2004; Eklöf et al., 2008). For example, a microcosm study found that snail grazing on live seagrass significantly reduced foliar biomass and chlorophyll (Zimmerman et al., 2001; Fredriksen et al., 2004; Holzer et al., 2011; Fong et al., 2018), while another study found that isopods could strongly suppress seagrass growth in a mesocosm (Nienhuis and Groenendijk, 1986; Duffy et al., 2001). In both cases, these grazers consumed live seagrass by making vertical scars, similar to those made by L. irrorata in marshes (B.R. Silliman personal observations and Silliman and Newell, 2003). This work, combined with observed scars on turtlegrass (Thalassia testudinum) in the Caribbean (B.R. Silliman personal observation) suggests that direct grazing of live seagrass by mesoinvertebrates could be common but understudied in tropical seagrasses. Furthermore, few studies have examined if this grazing by invertebrates can facilitate fungal growth on seagrasses, as has been shown in other coastal plant systems (Silliman and Zieman, 2001; Silliman and Newell, 2003).

Given the importance of seagrass as a foundation species in the Caribbean and evidence that invertebrate grazers can have cryptic but strong top-down control in other marine systems, we investigated if commonly abundant snails graze live turtlegrass (Thalassia testudinum) at multiple, dispersed Caribbean sites and if so, whether resulting scars promote fungal infection in live seagrass blades. We conducted field surveys to identify and quantify common snails in Belize’s seagrass beds and tested which of these snails would graze live seagrass. For those that did, we examined if their distribution in the field was positively correlated with abundance of grazing scars on live seagrass blades. To investigate the prevalence of snail grazing in other locations in the Caribbean, we conducted surveys in three other tropical seagrass beds (Florida, Bahamas, and USVI). Finally, we experimentally tested the effect scaring has on fungal presence on green seagrass blades.

Our results demonstrate that scarring by snails on live turtlegrass (Thalassia testudinum) is common at the five sites we surveyed that span four regions in the Caribbean (Belize, Florida, San Salvador, and USVI). Observational and experimental evidence show that two commonly occurring snail species (Tegula fasciata – smooth tegula and Smaragdia viridis – emerald nerite) generate scars on turtlegrass blades and that scarring on turtlegrass increases with increasing density of Tegula fasciata. Through scarring experiments, we demonstrated that simulated grazing wounds that damage live turtlegrass blades can facilitate fungal infection with the potential to amplify direct grazing effects. Future studies should investigate context-dependency and generality of this grazer-plant-fungal interaction in seagrasses and whether it can affect direct grazing effects on seagrass growth.

By highlighting the prevalence of snail grazing on live turtlegrass, our results contribute to a growing body of evidence demonstrating that consumption of seagrass by invertebrates is ubiquitous (Lewis and Hollingworth, 1982; Brearley and Walker, 1995; Heck and Valentine, 1995; Nakaoka et al., 2002; Fredriksen et al., 2004; Eklöf et al., 2008; Holzer et al., 2011; Unabia, 2011). Small invertebrates such as snails, chitons, and amphipods have been studied extensively in seagrass systems, however, those studies emphasize how these animal feed on the epiphytic algae that grow on seagrasses or on detritus, rather than directly on the seagrass itself (Orth et al., 1984). Results from our mesocosm feeding trial and surveys support this general trend, given that only a subset of the prevalent snail species were found to directly graze on turtlegrass. However, our results also expand this idea to show that some commonly abundant snails do graze live turtlegrass. Moreover, we found that the most common turtlegrass-grazing snail, smooth tegula, showed a positive, density-dependent relationship and that there was a high prevalence of grazing on turtlegrass at the five sites we surveyed (South Water Caye, Belize: 56.8–57% scarred, St Croix, USVI: 87% scarred, San Salvador, Bahamas: 97% scarred, Tampa Bay, Florida, United States: 90% scarred). This suggests that smooth tegula could be a key link in the direct grazing food-web in seagrass systems. Furthermore, since smooth tegula (and other grazing snails) are common prey items of predators in seagrass beds such as puffers, octopus, grunts, and hogfish (Fawcett, 1984), it is possible that theses predators/consumers control densities of fungal facilitating snails, similar to those in salt marshes (Silliman and Bertness, 2002). Further studies are needed to examine the effect of predator density on snail abundance. Smooth tegula also showed a strong preference for grazing unepiphytized leaves, which suggests that epiphytes could protect turtlegrass blades from direct grazing. Consequently, this also suggests that snails that graze epiphytes could potentially facilitate direct grazing on turtlegrass blades by removing epiphytes from the blade surface. Lastly, grazing snails (i.e., smooth tegula and green nerite) also seemed to be most active and abundant at night, which suggests many wounds are produced nocturnally and could explain why this phenomenon has been overlooked (i.e., most seagrass research takes place during the day). This also suggests that nocturnal predators, such as grunts and octopus, may have the ability to control grazing snail populations in seagrass systems, similar to what has been shown for snails on coral reefs (Shaver et al., 2020).

Our results question the notion in turtlegrass ecology that direct grazing by invertebrates is uncommon (Orth et al., 1984). Our survey results revealed that more than half of all turtlegrass blades (∼56–97%) surveyed in four different regions of the Caribbean were directly grazed by snails. However, our results also highlight the importance of species composition of snails in seagrass, with only two of the five common snail species consuming live seagrass tissue, of which only smooth tegula was particularly abundant during field surveys. This highlights how one species may have disproportionate scarring effects and could thereby have a larger and unique impact on seagrass systems through direct grazing. For example, Duffy et al. (2001) demonstrated amphipod grazer composition had a strong influence on Zostera marina biomass accumulation through grazing on epiphytes. Similarly, we found that direct grazing pressure by snails on seagrass is likely dependent on species composition, providing further evidence that biodiversity of the mesograzer functional group is an important factor in seagrass productivity.

Plant scarring has been shown to facilitate fungal infection in other marine systems. For example, snail scarring on Spartina alterniflora can cause fungal infections that lead to die-off of marsh plants (Silliman, 2005). Our simulated herbivory experiment suggests that herbivore damage to live seagrass blades may facilitate fungal growth in live turtlegrass tissue, similar to what has been shown in marsh systems. We hypothesize that snail grazer-generated scars damage the tissue of turtlegrass, thus creating an entry point for infection and resources for fungal growth within grazer wounds, possibly leading to a harmful infection. However, this hypothesis and the implication for ecosystem health has yet to be tested in seagrass systems, as the wounds produced during our herbivory experiments more closely mimics wounds produced by grazing fish than snails. If grazers do indeed facilitate fungal growth and fungal presence is shown to be detrimental to turtlegrass health, we predict that under physical stressors (i.e., water quality degradation and pollution), the impacts of grazer-facilitated microbial infection on seagrass health could be exacerbated, as has been shown in marshes (Silliman, 2005).

Despite evidence in terrestrial and other marine systems of the strong top-down control invertebrates can exhibit over plant communities, studies of herbivory in seagrass systems have primarily focused on direct consumption by megafauna (turtles, manatees, dugongs, and parrotfish) and indirect grazing effects of mesograzers. While some studies have investigated the role of direct grazing by small invertebrates, such as gastropods and sea urchins (Heinsohn and Birch, 1972; Ogden et al., 1983; Lanyon et al., 1989; Alcoverro and Mariani, 2004; Larkum et al., 2006; Eklöf et al., 2008; Mumby, 2009), relatively few studies have examined the negative impacts of invertebrate grazing on seagrass health (most of those studies have been with urchins). One explanation for the lack of studies investigating how small scars (from invertebrate grazers) on live seagrass tissue affects seagrass health, could be that these abundant scars may have been overlooked because apparent tolerance to such sublethal damage suggests they are not harmful to turtlegrass or their impact may be offset by epiphyte grazing snail species. Additionally, while the scars are commonplace, they may also be overlooked due to the marks of discoloration being difficult to distinguish relative to cropped blades while conducting field surveys (e.g., swimming above seagrass beds) and are only easily seen when looking carefully at collected seagrass blades. Alternatively, invertebrate grazers may have only recently become more important in seagrass beds as a result of overfishing of their predators such as blue crabs and smaller fish (Eriksson et al., 2009). While invertebrate grazers (i.e., mesograzers) have historically been presented as key species that generate positive impacts on seagrass growth through the consumption of epiphytes (Orth and Van Montfrans, 1984), emerging research is demonstrating their ability to have negative cascading impacts on community structure through the consumption of seagrass tissue, especially as their predator populations decline (Alcoverro and Mariani, 2004; Heck and Valentine, 2006).

Our study found pervasive evidence that snails commonly graze on living turtlegrass blades. However, only a few snail species are likely responsible for this grazing pattern that is density-dependent and may result in fungal infection in seagrasses. Further studies are needed to test whether gastropod grazing facilitates fungal infection and the resulting impact on seagrass health, and studies should also test the generality and relative importance of direct and indirect effects of gastropod grazing on tissue senescence, blade turnover, growth, and overall health. Studies should also examine how shifting food webs, disturbance regimes, and environmental stressors may alter the strength of gastropod-seagrass interactions.

The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found below: The datasets analyzed for this study can be found on Dataverse in the Experimental and survey data for “Invertebrate grazing on live turtlegrass (Thalassia testudinum): a common but overlooked interaction that can facilitate fungal infection.” repository (https://dataverse.harvard.edu/dataset.xhtml?persistentId=doi:10.7910/DVN/7HWCDF).

ADB and BRS wrote the original manuscript and interpreted the results. BRS designed all experiments and field surveys. AHA, CC, and BRS collected the data. NSW analyzed the data and produced the manuscript figures. VG processed fungal samples. All authors revised the manuscript and gave final approval for publication.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.