Microbiomes of Thalassia testudinum throughout the Atlantic Ocean, Caribbean Sea, and Gulf of Mexico are influenced by site and region while maintaining a core microbiome.

Plant microbiomes are known to serve several important functions for their host, and it is therefore important to understand their composition as well as the factors that may influence these microbial communities. The microbiome of Thalassia testudinum has only recently been explored, and studies to-date have primarily focused on characterizing the microbiome of plants in a single region. Here, we present the first characterization of the composition of the microbial communities of T. testudinum across a wide geographical range spanning three distinct regions with varying physicochemical conditions. We collected samples of leaves, roots, sediment, and water from six sites throughout the Atlantic Ocean, Caribbean Sea, and the Gulf of Mexico. We then analyzed these samples using 16S rRNA amplicon sequencing. We found that site and region can influence the microbial communities of T. testudinum, while maintaining a plant-associated core microbiome. A comprehensive comparison of available microbial community data from T. testudinum studies determined a core microbiome composed of 14 ASVs that consisted mostly of the family Rhodobacteraceae. The most abundant genera in the microbial communities included organisms with possible plant-beneficial functions, like plant-growth promoting taxa, disease suppressing taxa, and nitrogen fixers.

Herbivore effects increase with latitude across the extent of a foundational seagrass.

Climate change is altering the functioning of foundational ecosystems. While the direct effects of warming are expected to influence individual species, the indirect effects of warming on species interactions remain poorly understood. In marine systems, as tropical herbivores undergo poleward range expansion, they may change food web structure and alter the functioning of key habitats. While this process ('tropicalization') has been documented within declining kelp forests, we have a limited understanding of how this process might unfold across other systems. Here we use a network of sites spanning 23° of latitude to explore the effects of increased herbivory (simulated via leaf clipping) on the structure of a foundational marine plant (turtlegrass). By working across its geographic range, we also show how gradients in light, temperature and nutrients modified plant responses. We found that turtlegrass near its northern boundary was increasingly affected (reduced productivity) by herbivory and that this response was driven by latitudinal gradients in light (low insolation at high latitudes). By contrast, low-latitude meadows tolerated herbivory due to high insolation which enhanced plant carbohydrates. We show that as herbivores undergo range expansion, turtlegrass meadows at their northern limit display reduced resilience and may be under threat of ecological collapse.

Biodiversity influences the effects of oil disturbance on coastal ecosystems.

Biodiversity can enhance the response of ecosystems to disturbance. However, whether diversity can reduce the ecological effect of human-induced novel and extreme disturbances is unclear. In April 2010, the Deepwater Horizon (DwH) platform exploded, allowing an uncontrolled release of crude oil into the northern Gulf of Mexico. Initial surveys following the spill found that ecological impacts on coastal ecosystems varied greatly across habitat-type and trophic group; however, to date, few studies have tested the influence of local biodiversity on these responses. We used a meta-analytic approach to synthesize the results of 5 mesocosm studies that included 10 independent oil experiments and 5 independent oil + dispersant experiments. We tested whether biodiversity increased the resistance and/or resilience of coastal ecosystems to oil disturbance and whether a biodiversity effect depended on the type of diversity present (taxonomic or genetic) and/or the response type measured (population, community, or ecosystem level). We found that diversity can influence the effects of oiling, but the direction and magnitude of this diversity effect varied. Diversity reduced the negative impact of oiling for within-trophic-level responses and tended to be stronger for taxonomic than genetic diversity. Further, diversity effects were largely driven by the presence of highly resistant or quick to recover taxa and genotypes, consistent with the insurance hypothesis. However, we found no effect of diversity on the response to the combination of oil and dispersant exposure. We conclude that areas of low biodiversity may be particularly vulnerable to future oil disturbances and provide insight into the benefit of incorporating multiple measures of diversity in restoration projects and management decisions.

Tropicalization of the barrier islands of the northern Gulf of Mexico: A comparison of herbivory and decomposition rates between smooth cordgrass (Spartina alterniflora) and black mangrove (Avicennia germinans).

The expansion of black mangrove Avicennia germinans into historically smooth cordgrass Spartina alterniflora-dominated marshes with warming temperatures heralds the migration of the marsh-mangrove ecotone northward in the northern Gulf of Mexico. With this shift, A. germinans is expected to outcompete S. alterniflora where it is able to establish, offering another prevalent food source to first order consumers. In this study, we find A. germinans leaves to be preferable to chewing herbivores, but simultaneously, chewing herbivores cause more damage to S. alterniflora leaves. Despite higher nitrogen content, A. germinans leaves decomposed slower than S. alterniflora leaves, perhaps due to other leaf constituents or a different microbial community. Other studies have found the opposite in decomposition rates of the two species' leaf tissue. This study provides insights into basic trophic process, herbivory and decomposition, at the initial stages of black mangrove colonization into S. alterniflora salt marsh.

Ecological interactions between Gulf of Mexico snappers (Teleostei: Lutjanidae) and invasive red lionfish (Pterois volitans).

Indo-Pacific red lionfish (Pterois volitans) have invaded the western Atlantic, and most recently the northern Gulf of Mexico (nGOM), at a rapid pace. Given their generalist habitat affinities and diet, and strong ecological overlap with members of the commercially valuable snapper-grouper complex, increased density and abundance of lionfish could result in significant competitive interactions with nGOM commercially important species. We experimentally investigated the intensity of behavioral interactions between lionfish and indigenous, abundant and economically important juvenile nGOM red snapper (Lutjanus campechanus), and other increasingly abundant juvenile tropical snapper species (gray snapper-L. griseus and lane snapper-L. synagris) in large outdoor mesocosms to examine snapper vulnerabilities to lionfish competition. When paired with lionfish, red snapper swimming activity (i.e., time swimming and roving around experimental tank or at structure habitat during experiments) was significantly lower than in intraspecific control trials, but gray and lane snapper swimming activities in the presence of lionfish did not significantly differ from their intraspecific controls. Additionally in paired trials, red and lane snapper swimming activities were significantly lower than those of lionfish, while no significant difference in swimming activities was observed between lionfish and gray snapper. We found that red snapper prey consumption rates in the presence of lionfish were significantly lower than in their intraspecific 3-individual control trials, but when paired together no significant differences in prey consumption rates between red snapper and lionfish were observed. When paired with lane or gray snapper, lionfish were observed having comparatively higher prey consumption than snappers, or as observed in lionfish intraspecific 1-individual controls. However, lane and gray snapper consumption rates in the presence of lionfish did not significantly differ from those in intraspecific controls. These findings suggest that competition between juvenile snappers and invasive lionfish may be variable, with lionfish exhibiting differing degrees of competitive dominance and snappers exhibiting partial competitive vulnerability and resistance to lionfish. While the degree of intensity at which these interactions may occur in nGOM reefs may differ from those observed in our findings, this study enables greater understanding of the potential ecological effects of red lionfish on native reef fishes.

Lack of Impact of Posidonia oceanica Leaf Nutrient Enrichment on Sarpa salpa Herbivory: Additional Evidence for the Generalist Consumer Behavior of This Cornerstone Mediterranean Herbivore.

The fish Sarpa salpa (L.) is one of the main macroherbivores in the western Mediterranean. Through direct and indirect mechanisms, this herbivore can exert significant control on the structure and functional dynamics of seagrass beds and macroalgae. Past research has suggested nutritional quality of their diet influences S. salpa herbivory, with the fish feeding more intensively and exerting greater top down control on macrophytes with higher internal nutrient contents. However recent findings have questioned this notion and shown that herbivores do not preferentially feed on macrophytes with higher nutrient contents, but rather feed on a wide variety of them with no apparent selectivity. To contribute to this debate, we conducted a field fertilization experiment where we enriched leaves of the seagrass Posidonia oceanica, a staple diet for S. salpa, and examined the response by the herbivore. These responses included quantification of leaf consumption in fertilized and non-fertilized/control plots within the bed, and food choice assays where fertilized and non-fertilized/control leaves were simultaneously offered to the herbivore. Despite the duration of leaf exposure to herbivores (30 days) and abundant schools of S. salpa observed around the plots, leaf consumption was generally low in the plots examined. Consumption was not higher on fertilized than on non-fertilized leaves. Food choice experiments did not show strong evidence for selectivity of enriched leaves. These results add to a recent body of work reporting a broad generalist feeding behavior by S. salpa with no clear selectivity for seagrass with higher nutrient content. In concert, this and other studies suggest S. salpa is often generalist consumers not only dictated by diet nutrient content but by complex interactions between other traits of nutritional quality, habitat heterogeneity within their ample foraging area, and responses to predation risk.

Effects of Shoreline Dynamics on Saltmarsh Vegetation.

We evaluated the impact of shoreline dynamics on fringing vegetation density at mid- and low-marsh elevations at a high-energy site in the northern Gulf of Mexico. Particularly, we selected eight unprotected shoreline stretches (75 m each) at a historically eroding site and measured their inter-annual lateral movement rate using the DSAS method for three consecutive years. We observed high inter-annual variability of shoreline movement within the selected stretches. Specifically, shorelines retrograded (eroded) in year 1 and year 3, whereas, in year 2, shorelines advanced seaward. Despite shoreline advancement in year 2, an overall net erosion was recorded during the survey period. Additionally, vegetation density generally declined at both elevations during the survey period; however, probably due to their immediate proximity with lateral erosion agents (e.g., waves, currents), marsh grasses at low-elevation exhibited abrupt reduction in density, more so than grasses at mid elevation. Finally, contrary to our hypothesis, despite shoreline advancement, vegetation density did not increase correspondingly in year 2 probably due to a lag in response from biota. More studies in other coastal systems may advance our knowledge of marsh edge systems; however, we consider our results could be beneficial to resource managers in preparing protection plans for coastal wetlands against chronic stressors such as lateral erosion.

Accelerating Tropicalization and the Transformation of Temperate Seagrass Meadows.

Climate-driven changes are altering production and functioning of biotic assemblages in terrestrial and aquatic environments. In temperate coastal waters, rising sea temperatures, warm water anomalies and poleward shifts in the distribution of tropical herbivores have had a detrimental effect on algal forests. We develop generalized scenarios of this form of tropicalization and its potential effects on the structure and functioning of globally significant and threatened seagrass ecosystems, through poleward shifts in tropical seagrasses and herbivores. Initially, we expect tropical herbivorous fishes to establish in temperate seagrass meadows, followed later by megafauna. Tropical seagrasses are likely to establish later, delayed by more limited dispersal abilities. Ultimately, food webs are likely to shift from primarily seagrass-detritus to more direct-consumption-based systems, thereby affecting a range of important ecosystem services that seagrasses provide, including their nursery habitat role for fishery species, carbon sequestration, and the provision of organic matter to other ecosystems in temperate regions.

Ecological value of submerged breakwaters for habitat enhancement on a residential scale.

Estuarine shorelines have been degraded since humans arrived in the coastal zone. In recent history, a major cause of habitat degradation has been the armoring of shorelines with vertical walls to protect property from erosive wave energy; however, a lack of practical alternatives that maintain or enhance ecological function has limited the options of waterfront residents and coastal zone managers. We experimentally investigated the habitat value of two configurations of submerged breakwaters constructed along an eroding shoreline in northwest Mobile Bay, AL (USA). Breakwaters comprised of bagged oyster shell or Reef Ball™ concrete domes were built by a community-based restoration effort. Post-deployment monitoring found that: bagged oyster breakwaters supported much higher densities of live ribbed mussels than Reef Ball breakwaters; both breakwater configurations supported increased species richness of juvenile and smaller fishes compared to controls; and that larger fishes did not appear to be affected by breakwater presence. Our study demonstrates that ecologically degraded shorelines can be augmented with small-scale breakwaters at reasonable cost and that these complex structures can serve as habitat for filter-feeding bivalves, mobile invertebrates, and young fishes. Understanding the degree to which these structures mitigate erosive wave energy and protect uplands will require a longer time frame than our 2-year-long study.

The tropicalization of temperate marine ecosystems: climate-mediated changes in herbivory and community phase shifts.

Climate-driven changes in biotic interactions can profoundly alter ecological communities, particularly when they impact foundation species. In marine systems, changes in herbivory and the consequent loss of dominant habitat forming species can result in dramatic community phase shifts, such as from coral to macroalgal dominance when tropical fish herbivory decreases, and from algal forests to 'barrens' when temperate urchin grazing increases. Here, we propose a novel phase-shift away from macroalgal dominance caused by tropical herbivores extending their range into temperate regions. We argue that this phase shift is facilitated by poleward-flowing boundary currents that are creating ocean warming hotspots around the globe, enabling the range expansion of tropical species and increasing their grazing rates in temperate areas. Overgrazing of temperate macroalgae by tropical herbivorous fishes has already occurred in Japan and the Mediterranean. Emerging evidence suggests similar phenomena are occurring in other temperate regions, with increasing occurrence of tropical fishes on temperate reefs.

Interannual recruitment dynamics for resident and transient marsh species: evidence for a lack of impact by the Macondo oil spill.

The emulsification of oil at the Deepwater Horizon (DWH) well head relegated a large proportion of resultant hydrocarbon plumes to the deep sea, facilitated the incorporation of oil droplets into microbial and planktonic food web, and limited the severity of direct, wetland oiling to coastal Louisiana. Nevertheless, many transient fish and invertebrate species rely on offshore surface waters for egg and larval transport before settling in coastal habitats, thereby potentially impacting the recruitment of transient species to coastal nursery habitats quite distant from the well site. We compared the utilization of salt-marsh habitats by transient and resident nekton before and after the DWH accident using data obtained from an oyster reef restoration project in coastal Alabama. Our sampling activities began in the summer preceding the DWH spill and continued almost two years following the accident. Overall, we did not find significant differences in the recruitment of marsh-associated resident and transient nekton in coastal Alabama following the DWH accident. Our results, therefore, provide little evidence for severe acute or persistent oil-induced impacts on organisms that complete their life cycle within the estuary and those that spent portions of their life history in potentially contaminated offshore surface waters prior to their recruitment to nearshore habitats. Our negative findings are consistent with other assessments of nekton in coastal vegetated habitats and bolster the notion that, despite the presence of localized hydrocarbon enrichments in coastal habitats outside of Louisiana the most severe oil impacts were relegated to coastal Louisiana and the deep sea. Analyzing all the information learned from this accident will undoubtedly provide a synthesis of what has or has not been affected in the Northern Gulf of Mexico, which when put in context with oil spill studies elsewhere should improve our ability to avert and manage the negative consequences of such accidents.

Oyster reefs as natural breakwaters mitigate shoreline loss and facilitate fisheries.

Shorelines at the interface of marine, estuarine and terrestrial biomes are among the most degraded and threatened habitats in the coastal zone because of their sensitivity to sea level rise, storms and increased human utilization. Previous efforts to protect shorelines have largely involved constructing bulkheads and seawalls which can detrimentally affect nearshore habitats. Recently, efforts have shifted towards "living shoreline" approaches that include biogenic breakwater reefs. Our study experimentally tested the efficacy of breakwater reefs constructed of oyster shell for protecting eroding coastal shorelines and their effect on nearshore fish and shellfish communities. Along two different stretches of eroding shoreline, we created replicated pairs of subtidal breakwater reefs and established unaltered reference areas as controls. At both sites we measured shoreline and bathymetric change and quantified oyster recruitment, fish and mobile macro-invertebrate abundances. Breakwater reef treatments mitigated shoreline retreat by more than 40% at one site, but overall vegetation retreat and erosion rates were high across all treatments and at both sites. Oyster settlement and subsequent survival were observed at both sites, with mean adult densities reaching more than eighty oysters m(-2) at one site. We found the corridor between intertidal marsh and oyster reef breakwaters supported higher abundances and different communities of fishes than control plots without oyster reef habitat. Among the fishes and mobile invertebrates that appeared to be strongly enhanced were several economically-important species. Blue crabs (Callinectes sapidus) were the most clearly enhanced (+297%) by the presence of breakwater reefs, while red drum (Sciaenops ocellatus) (+108%), spotted seatrout (Cynoscion nebulosus) (+88%) and flounder (Paralichthys sp.) (+79%) also benefited. Although the vertical relief of the breakwater reefs was reduced over the course of our study and this compromised the shoreline protection capacity, the observed habitat value demonstrates ecological justification for future, more robust shoreline protection projects.

Response of coastal fishes to the Gulf of Mexico oil disaster.

The ecosystem-level impacts of the Deepwater Horizon disaster have been largely unpredictable due to the unique setting and magnitude of this spill. We used a five-year (2006-2010) data set within the oil-affected region to explore acute consequences for early-stage survival of fish species inhabiting seagrass nursery habitat. Although many of these species spawned during spring-summer, and produced larvae vulnerable to oil-polluted water, overall and species-by-species catch rates were high in 2010 after the spill (1,989±220 fishes km-towed(-1) [µ ± 1SE]) relative to the previous four years (1,080±43 fishes km-towed(-1)). Also, several exploited species were characterized by notably higher juvenile catch rates during 2010 following large-scale fisheries closures in the northern Gulf, although overall statistical results for the effects of fishery closures on assemblage-wide CPUE data were ambiguous. We conclude that immediate, catastrophic losses of 2010 cohorts were largely avoided, and that no shifts in species composition occurred following the spill. The potential long-term impacts facing fishes as a result of chronic exposure and delayed, indirect effects now require attention.

Decoupled effects (positive to negative) of nutrient enrichment on ecosystem services.

Eutrophication is a widespread phenomenon that disrupts natural ecosystems around the globe. Despite the general recognition that ecosystems provide many services and benefits to humans, little effort has been made to address how increasing anthropogenic eutrophication affects those services. We conducted a field experiment to determine the effect of nutrient enrichment on five ecological services provided by a model coastal system, a shallow seagrass community near Mobile Bay, Alabama (USA): (1) the provision of shelter for fauna; (2) the quality of food provided to first-order consumers; (3) quantity of food provision to first-order consumers and O2/CO2 exchange; (4) producer carbon and nitrogen storage, and (5) water clarity. The results showed a severe negative impact on seagrass density and biomass, which greatly reduced the structural complexity of the community and provision of shelter to fauna. Water clarity and the standing stock of producer carbon were reduced in the fertilized area in comparison with the control area. In contrast, nutrient addition did not affect in any consistent way the total quantity of food available for first-order consumers, the net exchange of O2/CO2, or the standing stock of producer nitrogen in the community. The nutritional quality of the food available for first-order consumers increased with fertilization. These results show that the impacts of nutrient enrichment on the services provided by natural systems may be disparate, ranging from negative to positive. These findings suggest that management policies for anthropogenic eutrophication will depend on the specific ecosystem service targeted. In the case of shallow seagrass beds, the loss of biogenic habitat and drastic impacts on commercially important fauna may be sufficiently alarming to warrant rigorous control of coastal eutrophication.

Differential habitat use and antipredator response of juvenile roach (Rutilus rutilus) to olfactory and visual cues from multiple predators.

The indirect, behavioral effects of predation and predator-predator interactions can significantly alter the trophic ecology of many communities. In numerous instances, the strength of these effects may be determined by the ability of prey to identify predation risk through predator-specific cues and respond accordingly to avoid capture. We exposed juvenile roach (Rutilus rutilus), a common forage fish in many brackish and freshwater environments, to vision and/or olfactory cues from two predators with different hunting methods: northern pike (Esox lucius, an ambush predator) and European perch (Perca fluviatilis, a roving predator). Our results demonstrated that responses of roach to perceived risk (as evidenced by their selection of structured or open-water habitats) were highly dependent on cue type and predator identity. For instance, roach responded to olfactory cues of pike by entering open-water habitat, but entered structured habitat when presented with a vision cue of this predator. Opposite responses were elicited from roach for both olfactory and visual cues of perch. Interestingly, roach defaulted to selection of structured habitat when presented with vision + olfaction cues of either predator. Moreover, when presented individual cues of both predators together, roach responded by choosing open-water habitat. Upon being presented with vision + olfaction cues of both predators, however, roach strongly favored structured habitat. Differences in habitat selection of roach were likely in response to the alternative foraging strategies of the two predators, and suggest that prey species may not always use structured habitats as protection. This appears particularly true when a threat is perceived, but cannot immediately be located. These results provide insight to the complex and variable nature by which prey respond to various cues and predators, and offer a mechanistic guide for how behaviorally mediated and predator-predator interactions act as structuring processes in aquatic systems.

Accelerating loss of seagrasses across the globe threatens coastal ecosystems.

Coastal ecosystems and the services they provide are adversely affected by a wide variety of human activities. In particular, seagrass meadows are negatively affected by impacts accruing from the billion or more people who live within 50 km of them. Seagrass meadows provide important ecosystem services, including an estimated $1.9 trillion per year in the form of nutrient cycling; an order of magnitude enhancement of coral reef fish productivity; a habitat for thousands of fish, bird, and invertebrate species; and a major food source for endangered dugong, manatee, and green turtle. Although individual impacts from coastal development, degraded water quality, and climate change have been documented, there has been no quantitative global assessment of seagrass loss until now. Our comprehensive global assessment of 215 studies found that seagrasses have been disappearing at a rate of 110 km(2) yr(-1) since 1980 and that 29% of the known areal extent has disappeared since seagrass areas were initially recorded in 1879. Furthermore, rates of decline have accelerated from a median of 0.9% yr(-1) before 1940 to 7% yr(-1) since 1990. Seagrass loss rates are comparable to those reported for mangroves, coral reefs, and tropical rainforests and place seagrass meadows among the most threatened ecosystems on earth.

Exploited species impacts on trophic linkages along reef-seagrass interfaces in the Florida Keys.

The removal of fish biomass by extensive commercial and recreational fishing has been hypothesized to drastically alter the strength of trophic linkages among adjacent habitats. We evaluated the effects of removing predatory fishes on trophic transfers between coral reefs and adjacent seagrass meadows by comparing fish community structure, grazing intensity, and invertebrate predation potential in predator-rich no-take sites and nearby predator-poor fished sites in the Florida Keys (USA). Exploited fishes were more abundant at the no-take sites than at the fished sites. Most of the exploited fishes were either omnivores or invertivores. More piscivores were recorded at no-take sites, but most (approximately 95%) were moderately fished and unexploited species (barracuda and bar jacks, respectively). Impacts of these consumers on lower trophic levels were modest. Herbivorous and smaller prey fish (< 10 cm total length) densities and seagrass grazing diminished with distance from reefs and were not negatively impacted by the elevated densities of exploited fishes at no-take sites. Predation by reef fishes on most tethered invertebrates was high, but exploited species impacts varied with prey type. The results of the study show that, even though abundances of reef-associated fishes have been reduced at fished sites, there is little evidence that this has produced cascading trophic effects or interrupted cross-habitat energy exchanges between coral reefs and seagrasses.

Experimental evidence that herbivory increases shoot density and productivity in a subtropical turtlegrass (Thalassia testudinum ) meadow.

The sea urchin, Lytechinus variegatus, has been estimated to consume between 50 and 90% of annual net aboveground production in selected turtlegrass (Thalassia testudinum) meadows in the eastern Gulf of Mexico. Nevertheless, turtlegrass persists where sea urchin grazing is intense. We hypothesized that turtlegrass productivity is stimulated by grazing, as has been reported from terrestrial grassland systems, and that this best explains the persistence of heavily grazed turtlegrass in St. Joseph Bay, Fla. This hypothesis was tested by manipulating sea urchin densities (0, 10, and 20 individuals/m2) in 1-m2 enclosures. These densities encompass the range of average densities at the study site and those reported in the literature. Changes in turtlegrass abundance (e.g., short shoot density and biomass), production by short shoots, and leaf width were monitored in these enclosures during the summer. Repeated-measures ANOVA showed that production by short shoots, leaf density/shoot, and leaf width decreased over time in all treatments. Leaf density/shoot and leaf width were not significantly impacted by grazing, nor did grazing significantly reduce seagrass biomass, but it did lead to significantly higher densities of short shoots than found in control cages. Our results indicate that turtlegrass compensates for the effects of sea urchin herbivory by increasing the recruitment of short shoots during the growing season. We estimate that this increased shoot density led to a 40% increase in net aboveground primary production (g dry weight/m2) in grazing treatments, which helps to explain the lack of significant reductions of sea grass biomass during the growing season.