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Seagrass meadows support key ecosystem services, via provision of food directly for herbivores, and indirectly to their predators. The importance of herbivores in seagrass meadows has been well-documented, but the links between food webs and ecosystem services in seagrass meadows have not previously been made explicit. Herbivores interact with ecosystem services — including carbon sequestration, cultural values, and coastal protection.

Interactions can be positive or negative and depend on a range of factors including the herbivore identity and the grazing type and intensity. There can be unintended consequences from management actions based on a poor understanding of trade-offs that occur with complex seagrass-herbivore interactions. Tropical seagrass meadows support a diversity of grazers spanning the meso-, macro-, and megaherbivore scales. We present a conceptual model to describe how multiple ecosystem services are influenced by herbivore pressure in tropical seagrass meadows. Our model suggests that a balanced ecosystem, incorporating both seagrass and herbivore diversity, is likely to sustain the broadest range of ecosystem services.

Our framework suggests the pathway to achieve desired ecosystem services outcomes requires knowledge on four key areas: 1 how size classes of herbivores interact to structure seagrass; 2 desired community and management values; 3 seagrass responses to top—down and bottom—up controls; 4 the pathway from intermediate to final ecosystem services and human benefits.

We suggest research should be directed to these areas. Herbivory is a major structuring influence in tropical seagrass systems and needs to be considered for effective management of these critical habitats and their services. Herbivores can dramatically influence primary production through top—down regulation in global ecosystems, including seagrass meadows.

Seagrasses are well-adapted to cope with grazing pressure Heck and Valentine, ; however, plant—herbivore interactions can modify characteristics such as biomass, productivity, and species diversity. There are 31 tropical seagrass species, approximately half of the global total, grazed by a broad suite of herbivores Carruthers et al. This diversity leads to complex interactions among plants and herbivores.

In the tropics, how these interactions shape seagrass meadow properties is not fully understood York et al. Such grazer-mediated changes in meadow structure can also influence the ecosystem services provided by seagrass, an area that has received little research focus Bakker et al. The Millennium Ecosystem Assessment outlined four categories of ecosystem services: provisioning, regulating, cultural, and supporting Millennium Ecosystem Assessment, These categories have been refined to better reflect how humans use ecosystems and to distinguish between intermediate ecosystem services, final ecosystem services, and benefits Mace et al.

This new classification prevents double-counting of services in management or economic valuations Boyd and Banzhaf, ; Fisher et al. Benefits are the ways human well-being is enhanced through ecosystem services Mace et al. Seagrass meadows provide numerous intermediate and final ecosystem services Nordlund et al. For example, nutrient cycling in seagrass meadows is an intermediate service, which produces the final ecosystem service of improved water quality, with the benefit of improved human health. Herbivory has the potential to modify these seagrass ecosystem services by reducing biomass, changing productivity, or altering species assemblages within meadows.

The multiple ecosystem services provided by seagrass meadows respond to environmental pressure and interact in complex ways, presenting challenges for managers. Science-based management requires knowledge of the trade-offs that arise from antagonistic interactions between ecosystem services. Trade-offs occur when one service is enhanced at a cost to another, and are a common outcome of management decisions, often unrecognized Raudsepp-Hearne et al.

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Summary of the expected change in herbivore abundance, key seagrass meadow properties and selected ecosystem services as habitats shift from seagrass-dominated to megaherbivore-dominated. At low levels of herbivory, disturbance is minimal and seagrass biomass dominates the system.

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In this system, the diversity of both seagrass and herbivore assemblages are generally at their highest. Bars illustrate likely direction of change and do not signify predicted linear relationships. In this article, we review the current literature and identify the plant—herbivore interactions that structure tropical seagrass meadows. We synthesize this information to develop a conceptual model of how seagrass and herbivory interact to deliver ecosystem services.

We suggest a management framework to ensure a holistic approach to achieve desired community and management outcomes for seagrasses, herbivores and the ecosystem services they deliver. Herbivores in tropical seagrass meadows are diverse, with a range of feeding strategies, each influencing meadows differently.

We classify them into three groups based on size: mesograzers, macroherbivores, and megaherbivores. Mesograzers e. Macroherbivores e. In contrast, megaherbivores, green turtles and dugongs, crop leaves.

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  7. Dugongs also excavate whole seagrass plants turtles only excavate in extreme cases Marsh et al. Each herbivore group contributes to structuring seagrass meadows in different ways, influencing biomass, productivity, leaf nutritional quality, species assemblage structure, and meadow extent. The impact of herbivory on seagrass biomass changes with herbivore size and density.

    Megaherbivores and macroherbivores can consume significant amounts of seagrass, resulting in biomass declines, particularly when they are present in large numbers Masini et al. In multi-species tropical meadows, biomass declines may only be observed in some seagrass species Armitage and Fourqurean, Grazing by fish can result in bare strips, or halos, around reefs Randall, , and can outstrip production in tropical meadows Unsworth et al.

    Biomass losses from increased megaherbivore and macroherbivore grazing, or high numbers of herbivores, are often accompanied by reductions in shoot density Preen, ; Lal et al. Other structural properties including canopy height, leaf width and area, might decrease due to megaherbivore and macroherbivore grazing Moran and Bjorndal, ; Kuiper-Linley et al. In contrast, herbivory by mesograzers can have positive effects on seagrass biomass.

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    These animals feed on leaf epiphytes, which benefits seagrasses by reducing shading Orth and Van Montfrans, ; Reynolds et al. Experiments show that mesograzers substantially reduce seagrass epiphytes in temperate and subtropical systems Cook et al. Herbivory directly affects seagrass productivity, with impacts caused by grazing intensity and the size class of herbivores.

    Increased productivity has been recorded in response to grazing by megaherbivores Aragones and Marsh, ; Christianen et al. Megaherbivore grazing can also cause the redistribution of productivity within tropical seagrasses, leading to higher leaf growth relative to rhizome growth Aragones and Marsh, Grazing activity can also affect the seagrass species assemblage.

    Megaherbivore grazing disturbance creates an environment that favors colonizing seagrass species sensu Kilminster et al. The opposite pattern has also been observed where urchins prefer colonizing species, and their grazing maintains the climax community Vonk et al. Seagrass diversity increases as meadows recover from disturbance because a mix of climax and colonizer species are present Rasheed, Recovery from grazing can take less than a month to years, depending on the grazing intensity and the life history traits of the seagrass species Aragones and Marsh, ; Kilminster et al.

    High herbivore diversity can enhance secondary production in temperate seagrass meadows Duffy et al. Herbivores can also have large-scale positive impacts on seagrass meadows: by dispersing seagrass propagules and seeds up to s of kilometers, they provide a mechanism for meadow recovery Tol et al. Herbivores reduce the accumulation of organic matter and nutrients by consuming seagrass, reducing the risk of factors such as hypoxia and diseases that cause seagrass die-off Jackson et al. Megaherbivore grazing also increases microbial nutrient cycling in seagrass sediments Perry and Dennison, Tropical seagrass responses to grazing pressure are dependent upon the size and densities of herbivores present.

    There is variability both between seagrass species and due to differences between study locations. Studies within the same location have also produced differing results Myers and Heck, ; Mutchler and Hoffman, Seascape configuration and the proximity of other habitats can have an impact on seagrass meadow fauna and meadows in proximity to other habitats can have increased herbivory Valentine et al.

    Grazing by one herbivore group can change seagrass meadows as habitats, in ways that affect other herbivores. Heavy grazing by megaherbivores can diminish the available habitat for mesograzers, and the suitability of habitat for macroherbivores. The consumption of epiphytes by mesograzers may be positive for herbivores that consume seagrass directly, due to increased seagrass growth. Larger herbivores may inadvertently consume mesograzers while feeding on the seagrass they live among Marsh et al.


    Interactions also occur within grazer groups. Grazing can cause changes to seagrass habitat complexity, which can affect where fish choose to feed, with higher fish herbivory in more complex sites Unsworth et al. Chemical changes in seagrass tissue composition caused by herbivory can be beneficial to herbivores. Nitrogen content can increase in response to herbivory, making the seagrass more nutritionally rich Aragones et al. However, these changes can be negative, with reductions in starch and increases in fiber Aragones et al. Grazing intensity and type e.

    If the intensity of herbivory is moderate, productivity may increase, resulting in more nutrient uptake by the seagrass Christianen et al. Grazing that leads to loss of biomass and reductions in shoot height may alter intermediate services provided by seagrasses.

    Megaherbivores may impact expansion of invasive seagrass in the Caribbean

    In this case, ecosystem services would cease to be delivered, and stored biomass or sediment carbon could be released back into the environment Fourqurean et al. Meadow loss on a large scale also results in mortality and changes in fecundity in seagrass-dependent herbivore populations Meager and Limpus, ; Fuentes et al.

    How plant—herbivore interactions change ecosystem services depends on location, season, habitat type, seagrass species and the herbivore community composition. Some services are more valuable in certain locations; e. Bottom—up anthropogenic stressors and environmental conditions e. Sometimes the impact of herbivores on seagrass ecosystem service delivery is unexpected; for example even when meadows are heavily grazed, the below-ground biomass can still provide an important coastal protection service Christianen et al.

    The interactions in a seagrass-herbivore system for managers and researchers to consider, to maintain a balanced system. Different herbivores interact with each other to modify seagrass properties and ecosystem services which depend on herbivore numbers, herbivore numbers are determined by top—down controls. These measures which control human activities will influence seagrass properties, herbivores and ecosystem services and will in turn be influenced by the relative importance of the various community values and important ecosystem services.

    Seagrass extent is determined by productivity, species and biomass as well as bottom—up controls, this influences both the ecosystem services provided and the number of herbivores feeding. Ecosystem services are influenced by seagrass extent, herbivores and management measures and require human inputs for benefits to be realized. By altering the species composition in seagrass meadows and creating disturbance, herbivores can change biodiversity in seagrass communities. Terrestrial ecosystems with more plant species provide higher levels of ecosystem services Gamfeldt et al.

    Increases in diversity are associated with increased provision of ecosystem services and greater multi-functionality of systems, attributed to greater interspecific niche complementarity Cardinale et al. The dominant plant species in ecological communities can be the predominant drivers of ecosystem functioning mass ratio: cf. The identity of dominant seagrass species, and their interactions with herbivore groups, may also play a role alongside, or instead of, high functional diversity to influence seagrass ecosystem service delivery.

    There are links between intermediate and final seagrass ecosystem services, some of which are well-established, such as changes in seagrass primary production and mesograzer removal of epiphytes mitigating nutrient pollution Christianen et al. Yet for others, the relationship is unclear. Ecosystem services and human well-being are linked, but the relationship is neither consistent nor linear, so it is difficult to predict how well-being outcomes respond to pressure Baker et al. Herbivores themselves are also important for the ecosystem services delivered by a seagrass meadow.

    The ecosystem service benefits of tourism, hunting, fishing, and cultural values depend explicitly on the presence of herbivores Butler et al. Cultural ecosystem services provided by seagrass meadows are important, but they are understudied, difficult to quantify and are rarely incorporated into management Garcia Rodrigues et al. Dugongs and green turtles have been referred to as cultural keystone species for communities in the tropics Butler et al. Plants under colder and darker environmental conditions accumulated more total fatty acids TFA and also exhibited larger concentration of polyunsaturated fatty acids PUFA relative to saturated fatty acids SFA.

    Additionally, the comparison of FA composition of Z. Furthermore, we studied both morphological and biochemical responses of Halophila stipulacea populations from Gulf of Aqava Red Sea across an irradiance gradient. Also, we performed two warming experiments; one with Irish Z. Moreover, experimental and in-situ analysis of FA suggested that future warming may negatively affect the lipid nutritional value of Z. In combination, these results highlight the capacity of seagrasses to adjust their lipid composition to achieve optimal membrane fluidity under variable environmental conditions.

    Seagrass Ecosystem Services and Their Variability across Genera and Geographical Regions

    Finally, we mapped large areas of previously undocumented seagrass meadows in the Irish coast by developing a new mapping approach, integrating species distribution models SDM , satellite-derived images and field surveys. This project is particularly relevant due to i the previous scarcity of knowledge available on seagrass ecology and spatial information in Ireland, ii the undisturbed status of the eelgrass meadows described, and iii the potential application of these baseline data in assessing impacts of anthropogenic disturbances or future climate change effects on these valuables ecosystems.

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