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.
Historical exploitation of the Mediterranean Sea and the absence of rigorous baselines makes it difficult to evaluate the current health of the marine ecosystems and the efficacy of conservation actions at the ecosystem level. Here we establish the first current baseline and gradient of ecosystem structure of nearshore rocky reefs at the Mediterranean scale. We conducted underwater surveys in 14 marine protected areas and 18 open access sites across the Mediterranean, and across a 31-fold range of fish biomass (from 3.8 to 118 g m−2). Our data showed remarkable variation in the structure of rocky reef ecosystems. Multivariate analysis showed three alternative community states: (1) large fish biomass and reefs dominated by non-canopy algae, (2) lower fish biomass but abundant native algal canopies and suspension feeders, and (3) low fish biomass and extensive barrens, with areas covered by turf algae. Our results suggest that the healthiest shallow rocky reef ecosystems in the Mediterranean have both large fish and algal biomass. Protection level and primary production were the only variables significantly correlated to community biomass structure. Fish biomass was significantly larger in well-enforced no-take marine reserves, but there were no significant differences between multi-use marine protected areas (which allow some fishing) and open access areas at the regional scale. The gradients reported here represent a trajectory of degradation that can be used to assess the health of any similar habitat in the Mediterranean, and to evaluate the efficacy of marine protected areas.
Despite the importance of coastal ecosystems for the global carbon budgets, knowledge of their carbon storage capacity and the factors driving variability in storage capacity is still limited. Here we provide an estimate on the magnitude and variability of carbon stocks within a widely distributed marine foundation species throughout its distribution area in temperate Northern Hemisphere. We sampled 54 eelgrass (Zostera marina) meadows, spread across eight ocean margins and 36° of latitude, to determine abiotic and biotic factors influencing organic carbon (Corg) stocks in Zostera marina sediments. The Corg stocks (integrated over 25‐cm depth) showed a large variability and ranged from 318 to 26,523 g C/m2 with an average of 2,721 g C/m2. The projected Corg stocks obtained by extrapolating over the top 1 m of sediment ranged between 23.1 and 351.7 Mg C/ha, which is in line with estimates for other seagrasses and other blue carbon ecosystems. Most of the variation in Corg stocks was explained by five environmental variables (sediment mud content, dry density and degree of sorting, and salinity and water depth), while plant attributes such as biomass and shoot density were less important to Corg stocks. Carbon isotopic signatures indicated that at most sites <50% of the sediment carbon is derived from seagrass, which is lower than reported previously for seagrass meadows. The high spatial carbon storage variability urges caution in extrapolating carbon storage capacity between geographical areas as well as within and between seagrass species.
Terrestrial plants benefit from many well-understood mutualistic relationships with root- and leaf-associated microbiomes, but relatively little is known about these relationships for seagrass and other aquatic plants. We used 16S rRNA gene amplicon sequencing and metatranscriptomics to assess potential mutualisms between microorganisms and the seagrasses Zostera marina and Zostera japonica collected from mixed beds in Netarts Bay, OR, United States. The phylogenetic composition of leaf-, root-, and water column-associated bacterial communities were strikingly different, but these communities were not significantly different between plant species. Many taxa present on leaves were related to organisms capable of consuming the common plant metabolic waste product methanol, and of producing agarases, which can limit the growth of epiphytic algae. Taxa present on roots were related to organisms capable of oxidizing toxic sulfur compounds and of fixing nitrogen. Metatranscriptomic sequencing identified expression of genes involved in all of these microbial metabolic processes at levels greater than typical water column bacterioplankton, and also identified expression of genes involved in denitrification and in bacterial synthesis of the plant growth hormone indole-3-acetate. These results provide the first evidence using metatranscriptomics that seagrass microbiomes carry out a broad range of functions that may benefit their hosts, and imply that microbe–plant mutualisms support the health and growth of aquatic plants.
Summary 1.A striking example of climate-mediated range shifts in marine systems is the intrusion of tropical species into temperate areas world-wide, but we know very little about the ecological consequences of these range expansions. 2. In the Mediterranean Sea, the range expansion of tropical rabbitfishes that first entered the basin via the Suez Canal provides a good example of how tropical herbivorous fish can impact the structure of rocky bottoms in temperate seas. Two species of rabbitfishes have now become a dominant component of total fish biomass in the southernmost part of the eastern Mediterranean. Experimental evidence shows these species can profoundly transform benthic communities, turning algal forests into 'barrens', but the specific mechanisms that facilitate this shift have not been established. 3. We surveyed~1000 km of coastline in the eastern Mediterranean and identified two clearly distinct areas, a warmer group of regions with abundant tropical rabbitfish and a colder group of regions where these consumers were absent/ extremely rare. In regions with abundant rabbitfish, canopy algae were 65% less abundant, and there was a 60% reduction of overall benthic biomass (algae and invertebrates) and a 40% decrease in total species richness. 4. Video-recorded feeding experiments showed that the extensive barrens characteristic of regions with abundant rabbitfish were not due to greater rates of herbivory by these tropical consumers, but rather by functional differences among the herbivores. Temperate herbivorous fish displayed the greatest macroalgae consumption rates overall, but they fed exclusively on established adult macroalgae. In contrast, in regions with abundant rabbitfishes, these consumers fed complementarily on both established macroalgae and on the epilithic algal matrix, which typically contains macroalgal recruits. 5. Synthesis. Range-shifting tropical rabbitfish can severely reduce the biomass and biodiversity of temperate reefs at a scale of hundreds of kilometres. A shift from macroalgal dominance to barrens is mediated by the addition of functionally diverse herbivores that characterize tropical reefs. This work highlights the importance of assessing the functional traits of range-shifting species to determine potential mechanisms of impact on ecological communities.
The rates of seagrass defoliation exerted by the herbivorous fish Sarpa salpa and by the sea urchin Paracentrotus lividus were evaluated through both direct (tethering experiment) and indirect (bite marks) methods. Sampling was conducted once per season in 10 shallow meadows of Posidonia oceanica (L.) Delile from the continental NW Mediterranean coast covering a spatial scale of > 300 km. Results indicated that a large proportion (ca. 57%) of the annual leaf production is lost to herbivory, yet with considerable spatial variation. Patterns of seagrass defoliation showed high temporal variability, with a peak in summer with values that exceeded about 2.5 times those of leaf production and a minimum during the winter period. On average, defoliation exerted by S. salpa accounted for 40% of leaf production (ca. 70% of total annual losses to herbivory), while P. lividus was also responsible for a substantial 17% removal of leaf production. High discrepancies encountered when comparing direct and indirect measurements suggest that the latter are inappropriate to achieve accurate estimates of herbivory pressure. This study evidences that P. oceanica leaf losses to herbivores are not marginal, but a widespread process that occurs at much higher rates than previously estimated through indirect methods (ca. 2%), resetting the paradigm of the negligible importance of herbivory in temperate systems.
Despite increasing evidence that herbivory on seagrasses can be substantial in nearshore systems, there is only scarce experimental data on the direct quantification of seagrass removal by herbivores. To help fill this gap, and to evaluate the hypothesis that herbivory on the Mediterranean seagrass Posidonia oceanica (L.) Delile is generally low, we assessed the patterns of grazing pressure variability and its effects on seagrass in an undisturbed meadow in the NW Mediterranean. We quantified herbivore density and grazing pressure through both direct (tethering experiment) and indirect (through marks of herbivore attacks) measurements. Although grazing varied greatly both temporally and spatially, our results show that whereas consumption by the sea urchin Paracentrotus lividus is relatively minor, P. oceanica is intensely grazed by the fish Sarpa salpa in summer. During this period, fish are very abundant at a depth of 5 m, with consumption rates that temporarily exceed seagrass production, which is at its yearly minimum. This imbalance between consumption and production causes the appearance of mowed patches that can be seen from early summer to September; seagrass biomass is reduced by 50% in such patches. Through direct measurements of consumption, our study has revealed that P. oceanica consumption by herbivores can be substantial with respect to the total annual production and much higher than previously estimated through indirect measurements. Thus, it becomes apparent that estimation of consumption rates by indirect methods can grossly underestimate the importance of herbivory in seagrass ecosystems, which leads us to strongly advocate the use of direct methods whenever possible.
We measured settlement and recruitment of one of the main invertebrate herbivores in the Mediterranean, the sea urchin Paracentrotus lividus, in 2 neighbouring and contrasting habitats: a seagrass meadow and a vertical rock wall. We quantified and compared temporal and bathymetrical variability in settlement and compared settlement with recruitment over a 4 yr period. Two settlement peaks were observed each year, a main peak in spring-early summer and a second peak in autumn-early winter. Interannual variability in settlement was very high (ca. 1 order of magnitude). Settlement was generally higher on the rock wall than in the seagrass meadow. No appreciable successful recruitment was observed in the meadow during the 4 yr studied despite the arrival of settlers. The few juvenile urchins found in the meadow were encountered at the shallow part and were completely hidden between the rhizomes. However, no differential settlement on the rhizome stratum was observed. In contrast to the seagrass meadow, recruitment occurred every year on the rock wall. Despite the arrival of settlers in both habitats, the population in the seagrass meadow appears to be recruitment-limited and probably mainly sustained by immigration, while settlement and recruitment appear to determine, to a certain extent, adult population structure and dynamics on the rock wall.
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