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Top-down control of epifauna by fishes enhances seagrass production

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Predators can influence the structure and function of ecosystems by altering the composition or behavior of herbivore communities. Overexploitation of predators, therefore, may lead to habitat loss by altering important top-down interactions that facilitate habitat-forming species. In seagrass beds, top-down control of algal growth by mesograzers appears to facilitate seagrass production. The indirect consequences of higher-order trophic interactions, however, remain unclear. Although predators may limit the beneficial effects of algal mesograzers, it is also possible that they limit the abundance of invertebrates that consume and foul seagrasses. We used experimental enclosure and exclosure cages to explore the direct and indirect effects of microcarnivorous fishes on epifaunal invertebrates, epiphytic loads, and seagrass growth in a natural eelgrass (Zostera marina) bed in San Diego Bay, California, USA. Contrary to expectations, when fishes were excluded, invertebrate abundance increased by 300-1000%, fouling on eelgrass leaves increased by 600%, and eelgrass production declined by 50%. Despite high densities of predators in enclosures, subsequent effects did not differ from ambient conditions. When predators were excluded, however, abundances of epifauna (including tube-building crustaceans and an eelgrass-grazing limpet) increased dramatically, resulting in reduced seagrass production. Our results are supported by several studies of eelgrass communities in the northeastern Pacific, characterized by coastal upwelling, inverse estuaries, and a voracious seagrass-consuming limpet. These strong, positive, indirect effects of microcarnivores on seagrass production contrast with the beneficial mesograzer paradigm, highlighting the need for hypotheses to be tested across a variety of ecosystems with varying biophysical characteristics.
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... Beyond the ecological relationships described in sea otter-seagrass trophic cascade, we also examined our data for other biotic and abiotic relationships known to influence seagrass communities in other regions. These included the role of mesopredatory fishes which can exert top-down pressure on epifauna (Jephson et al. 2008, Moksnes et al. 2008, Baden et al. 2010, Lewis and Anderson 2012, benthic macroalgae and diatoms (Heck et al. 2000, Valentine andDuffy 2006), sediment grain size (De Boer 2007) and light availability (Lee et al. 2007). (Harper andMorris 2004, NOAA 2019). ...
... Our hypotheses were based on trophic cascade theory, documented trophic cascades in the northeast Atlantic and Elkhorn Slough, CA, and sea otter foraging ecology in southeast Alaska and focused on direct relationships between variables. Specifically we hypothesized that sea otters would have a negative relationship with crab biomass (Hoyt 2015), crab and fish biomass would have a negative relationship with epifauna load (Moksnes et al. 2008, Baden et al. 2010, Lewis and Anderson 2012, Hughes et al. 2013, epifauna load would have a negative relationship with macroalgae cover, diatom cover and epiphyte load, and epiphyte load would have a negative relationship with seagrass biomass (Hughes et al. 2004, Heck and Valentine 2007, Jephson et al. 2008, Duffy et al. 2015. We also hypothesized that the bottom-up forces of light and water nitrate concentration would have a positive relationship with both seagrass biomass and epiphyte load . ...
... Together, the potential that epifauna are not a reliable food source for crabs and fishes and the likelihood that these species life history operate on different spatial scales may indicate that our assumption that crabs and fishes consume seagrass epifauna was flawed. Field and laboratory studies have tightly linked these mesopredators and seagrass epifauna (Jephson et al. 2008, Moksnes et al. 2008, Baden et al. 2010, Lewis and Anderson 2012, Hughes et al. 2013, however our results suggest that this may not be the case in southeast Alaska; yet another example of local abiotic and biotic conditions potentially influencing the importance of top-down forces (Duffy et al. 2015). It is also possible that our metric of epifauna biomass is not a good indication of grazing pressure. ...
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The presence and strength of trophic cascades can be a function of the local abiotic environment and relative abundance of key species. The reintroduction and expansion of sea otters Enhydra lutris, a known keystone species in kelp ecosystems, in southeast Alaska provides a rare natural experiment to test the generality of a apex-predator-seagrass trophic cascades across a broad spatial scale. We conducted an in-depth sea-grass community survey at 21 sites spanning ~100 km with variable sea otter presence to test for patterns of alternating abundance and direct relationships between species indicative of trophic cascades. Our analysis revealed some of the trophic relationships predicted by the apex predator-seagrass trophic cascades theory, including a strong negative relationship between sea otters and crabs and many of the expected relationships between nitrate, seagrass, epiphytes and epifauna. Other expected relationships within a trophic cascade, however, were not supported-including no relationship between crabs and epifauna, a critical link in the trophic cascade. Given the lack of evidence for all hypothesized direct relationships, we conclude that a sea otter mediated trophic cascade may not be present in southeast Alaska and could be due to local scale factors including the spatial heterogeneity, low resource availability and non-linear food chains in southeast Alaska seagrass communities. However, correlation analyses suggest further interactions among biological and environmental variables in southeast Alaska seagrass communities, including a positive correlation between sea otters and seagrass biomass. These results suggest that the effects of recovering apex-predator populations may not be generalizable across regions and spatial scales, highlighting a need for local assessment on the ecology and management of these populations.
... In particular, the diversity and community structure of mobile and sessile epifauna within Neptune grass (Posidonia spp., dominant in the Mediterranean Sea), eelgrass (Zostera spp., globally widespread) and turtlegrass (Thalassia spp., chiefly distributed in Indo-Pacific and West Atlantic) meadows are relatively well documented (Virnstein et al. 1984, Knowles & Bell 1998, Sánchez-Jerez et al. 1999, Wong & Dowd 2015, Demers et al. 2016, McDonald et al. 2016, Tano et al. 2016, Boyé et al. 2017. Numerous published studies focus on plant-animal interactions and energy flows within seagrass meadows (Jernakoff & Nielsen 1998, Lepoint et al. 1999, Lewis & Anderson 2012, Hammerschlag-Peyer et al. 2013. Overall, seagrass systems are much less studied in the tropics (although see Ansari et al. 1991, Klumpp et al. 1992, Prieto et al. 2003, Unsworth et al. 2007, Leopardas & Nakaoka 2014, Tano et al. 2016, Cavalcante et al. 2019) than temperate latitudes (Hootsmans & Vermaat 1985, Edgar & Shaw 1995, Heck et al. 1995, Nakamura & Sano 2005, Polte et al. 2005a,b, Spivak et al. 2009, Gullström et al. 2012, Wong & Dowd 2015, Lefcheck & Duffy 2015, Lefcheck et al. 2016, Boyé et al. 2017, Wong 2018 or subtropical zones (Edgar 1990c, Connolly 1995, Lemmens et al. 1996, Jernakoff & Nielsen 1998, Alfaro 2006, Micheli et al. 2008 Number of studies conducted on epifaunal communities within particular marine habitats. ...
... Values are based on a search conducted in ISI Web of Science database in July 2020 using the terms "epifauna" and "epifaunal". Lewis & Anderson 2012, Hammerschlag-Peyer et al. 2013, McDonald et al. 2016, Douglass et al. 2018, Ledbetter & Hovel 2020. Limited tropical evidence does, however, suggest that latitudinal influences are likely less significant than differences between epifaunal communities at the level of microhabitat structure (Fraser et al. 2020a). ...
... Due to complex food webs made up of animals, plants and microbes, multilevel biotic interactions can exert important control on carbon cycling. For example, predators play a critical role in suppressing herbivore abundance, consequently facilitating the growth of primary producers through trophic cascades (Atwood et al., 2015;Finke & Denno, 2005;Lewis & Anderson, 2012;Silliman & Bertness, 2002). Furthermore, combined effects of grazing and fungal infection can substantially reduce salt marsh production (Daleo & Iribarne, 2009;Silliman & Newell, 2003). ...
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Research into biotic interactions has been a core theme of ecology for over a century. However, despite the obvious role that biota play in the global carbon cycle, the effects of biotic interactions on carbon pools and fluxes are poorly understood. Here we develop a conceptual framework that illustrates the importance of biotic interactions in regulating carbon cycling based on a literature review and a quantitative synthesis by means of meta‐analysis. Our study focuses on blue carbon ecosystems—vegetated coastal ecosystems that function as the most effective long‐term CO2 sinks of the biosphere. We demonstrate that a multitude of mutualistic, competitive and consumer–resource interactions between plants, animals and microbiota exert strong effects on carbon cycling across various spatial scales ranging from the rhizosphere to the landscape scale. Climate change‐sensitive abiotic factors modulate the strength of biotic‐interaction effects on carbon fluxes, suggesting that the importance of biota‐mediated carbon cycling will change under future climatic conditions. Strong effects of biotic interactions on carbon cycling imply that biosphere‐climate feedbacks may not be sufficiently represented in current Earth system models. Inclusion of new functional groups in these models, and new approaches to simplify species interactions, may thus improve the predictions of biotic effects on the global climate.
... The deep areas of these bays often provide an extension to coastal habitats and can create seasonal variation in fish assemblages (Froeschke and Allen, 2006). Seagrass beds not only provide a variety of critical ecosystems services such as stabilizing sediment and promoting biodiversity (Fonseca and Cahalan, 1992), but they also provide food to epifaunal invertebrates and fishes, along with physical refuge (Lewis and Anderson, 2012). From our initial trapping study, gnathiids rarely inhabited embayments, which could be attributable to multiple factors. ...
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The distribution and abundance of organisms is typically shaped by multiple biotic and abiotic processes. Micropredators are parasite-like organisms that are smaller than their hosts and/or prey and feed on multiple hosts during a given life stage. Unlike typical parasites, however, they spend much or most of their time free-living, associating only temporarily with hosts. In the ocean, micropredators can impact multiple fish species, and in particular can have significant lethal and sub-lethal effects on newly settled fish. Although gnathiid isopods are abundant and primary micropredators in coral reef ecosystems, their impacts are relatively unexplored within sub-tidal temperate rocky reefs. We investigated the distribution of juvenile gnathiid isopods along sub-tidal temperate rocky reefs and tested trap methodology. We also quantified both the sub-lethal and lethal impacts of feeding-stage juvenile gnathiid isopods on juvenile, post settlement reef fish, Heterostichus rostratus (giant kelpfish). We were most interested in determining the relationship between gnathiid infestation level and fish swimming performance, in particular swimming metrics relevant to predator avoidance maneuvers. We found that Gnathia tridens was present in rocky reefs rather than embayments along the Southern California coastline and that within rocky reefs, gnathiids occurred in the highest densities in lighted traps. Surprisingly, we observed almost no influence of fish size or gnathiid sub-lethal infestation level on ambient or burst swimming performance metrics. However, burst duration was reduced by gnathiid infestation, which is important in predator avoidance. There were significant differences in survivorship among small fish compared to large fish as a result of gnathiid infestation. Larger fish survived higher numbers of gnathiids than smaller fish, indicating that parasite-induced mortality is greater for smaller fish. Investigations of the effects of micropredators on subsequent predator-mediated mortality, including the susceptibility of fishes and their individual responses to micropredators, can further contribute to our understanding of processes affecting recruitment in resident reef fish populations. Further research, especially within temperate sub-tidal ecosystems, is needed to understand and highlight the overlooked importance of micropredation in shaping fish populations within a reefscape.
... That is, though the seagrass itself is considered the habitat and nursery for a great many species, and obviously food for apex species such as sea turtles and manatees, it is the epiphytes which provide a large part of the base of the food chain for micro-and meso-grazers. These grazers include but are not limited to amphipods, copepods, polychaete worms, molluscs, shrimp and herbivorous fishes [24][25][26][27][28][29][30]. These smaller grazers are then the next part of the food web including many larger fish species [2,6,7,20]. ...
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This paper presents pigment-based chemotaxonomy as a rapid method for the analysis of seagrass epiphyte communities and how that data may be applied to the assessment of the full seagrass ecosystem. Pigments-based chemotaxonomy uses diagnostic pigments to determine the biomass, using chlorophyll-a as a proxy, of microalgal taxa within phytoplankton or epiphyte communities. Seagrass samples were taken from Florida Bay, USA and around the southern tip of Eleuthera Island in the Bahamas. Data is presented which reveals. A. The need for care during sampling in order to avoid losing epiphytes due to sloughing, B. Consideration of the exact site of sampling with a given area, C. Variations in epiphyte production and community makeup with respect to time of year, D. Epiphyte loading variations along the length of a seagrass blade, E. Potential effects of light (top-down) and grazing (bottom-up) on epiphyte communities, F. The importance of diatoms on the seagrasses and macro-algae of Florida Bay, G. The use of epiphytometers to monitor epiphyte production versus time, and H. The strong variation in epiphyte communities around the southern tip of Eleuthera Island. All of these results and discussion are presented in order to reveal the application of pigment-based chemotaxonomy and epiphytometers (aka fake seagrass) in the assessment of seagrass epiphyte communities Keywords: Epiphytometers; Biodiversity; Atmospheric; Seagrass; Epiphyte; Cyanobacteria
... The increase of the former two species is substantially higher than those found in Baden et al. (2012). Topdown effects have recently shown to play important roles in seagrass ecosystems (Valentine and Duffy, 2006;Lewis and Anderson, 2012;Burkholder et al., 2013;Östman et al., 2016) including the Z. marina meadows on the Swedish west coast between mid-1980s to mid-2000s . During these two decades, there is no actual data revealing when the dramatic flip occurred in faunal composition and the cascade consequences resulting in 60% loss of Z. marina (Baden et al., 2003;Nyqvist et al., 2009). ...
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The interaction between bottom-up and top-down processes in coastal ecosystems has Marinebeen scarcely studied so far. Temporal changes in trophic interactions of Zostera marina along the Swedish west coast are relatively well studied, with the exception of epifaunal communities. Epifauna was used as a model study to explore resource (bottom-up) or predator (top-down) regulated in a vegetated ecosystem. We conducted a 21-year comparative study (1997 and 2018) using epifauna of 19 Zostera marina meadows along the Swedish Skagerrak coast. Large changes were observed in the composition of small (0.2–1 mm) and large (> 1 mm) epifauna. In the small-sized epifauna, the nematode Southernia zosterae and harpacticoids showed an increase of 90% and a decrease of 50% of their abundances, respectively. In the large-sized epifauna, the polychaete Platynereis dumerilii and chironomid larvae were absent in 1997 but thrived in 2018 (> 2000 ind. m−2). Mesoherbivores (Idoteids and gammarids) were locally very abundant in 1997 but disappeared in 2018. An 83% decline of mytilids settling in Zostera marina leaves was observed. Our results showed that epifauna is predominantly top-down regulated. An integrative framework of the study area is outlined to shed light on the causes and consequences of the environmental shifts reported in Zostera meadows from the northern Skagerrak area throughout the last three decades.
... and Rissoa spp.) or fouling (e.g. some tube-building amphipods) the perennial macrophytes (Fredriksen et al. 2004;Lewis and Anderson 2012) or by direct mesopredator consumption of ephemeral algae (Heck et al. 2000, but not found in stomachs here). Therefore, functional diversity and trophic interactions may have great influence on the strength and direction of trophic cascades (Duffy et al. 2015;Östman et al. 2016). ...
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Ecological impacts of top-down trophic cascades in combination with bottom-up nutrient enrichment are increasingly being reported. Such effects may be triggered by decline in the abundance and size of piscivore fish leading to a release of smaller-sized mesopredatory fish that are capable of reducing mesograzers and their buffering herbivorous effects, thus intensifying eutrophication symptoms. Hitherto, such mesopredator release has not been studied in controlled manner in macroalgal-dominated rocky shore communities. This study utilised twelve littoral mesocosms in southeastern Norway to investigate the impact of increased nutrient levels and increased abundance of the mesopredatory goldsinny wrasse (Ctenolabrus rup-estris) over 6 months, from spring (April) to autumn (October). The study mainly revealed typical eutrophication responses in both July and in October with nutrient enrichment leading to more ephemeral algae and less perennial Fucacean and red macroalgae. Significant responses to the addition of mesopredatory fish alone or with nutrients in combination were clearly fewer in July and almost non-existent in October. Mesopredatory fish reduced the number of some mesograzers, but not others, and some herbivores even benefitted. Few joint effects occurred between fish and nutrients and the anticipated negative consequences for perennial macrophytes were largely absent; the possible reasons for these observations are discussed in depth. Curiously, the presence of mesopredatory fish seems to favour some canopy-forming macrophytes. This last finding warrants further investigation as the labrid fishery in coastal waters of southern Norway and western Sweden is increasing and a too heavy reduction of mesopredators may have its own unforeseen ecosystem implications.
... Top-down (consumer) effects appear particularly strong in benthic marine habitats, thus simple changes in trophic structure can result in complex indirect impacts on habitat-forming species and the communities and processes that depend upon them (Shurin et al. 2006, Heck & Valentine 2007, Lewis & Anderson 2012. The ecological effects of consumers, however, can vary greatly among ecosystems. ...
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