Drivers of variation in seagrass-associated amphipods across biogeographical areas.

Amphipods are one of the dominant epifaunal groups in seagrass meadows. However, our understanding of the biogeographical patterns in the distribution of these small crustaceans is limited. In this study, we investigated such patterns and the potential drivers in twelve Cymodocea nodosa meadows within four distinctive biogeographical areas across 2000 Km and 13° of latitude in two ocean basins (Mediterranean Sea and Atlantic Ocean). We found that species abundances in the assemblage of seagrass-associated amphipods differed among areas following a pattern largely explained by seagrass leaf area and epiphyte biomass, while the variation pattern in species presence/absence was determined by seagrass density and epiphyte biomass. Seagrass leaf area was also the most important determinant of greater amphipod total density and species richness, while amphipod density also increased with algal cover. Overall, our results evidenced that biogeographical patterns of variation in amphipod assemblages are mainly influenced by components of the habitat structure, which covary with environmental conditions, finding that structurally more complex meadows harboring higher abundance and richness of amphipods associated.

Driving factors of biogeographical variation in seagrass herbivory.

Despite the crucial role of herbivory in shaping community assembly, our understanding on biogeographical patterns of herbivory on seagrasses is limited compared to that on terrestrial plants. In particular, the drivers of such patterns remain largely unexplored. Here, we used a comparative-experimental approach in Cymodocea nodosa meadows, across all possible climate types within the seagrass distribution, 2000 km and 13° of latitude in two ocean basins, to investigate biogeographical variation in seagrass herbivory intensity and their drivers during July 2014. Particularly, the density and richness of herbivores and their food resources, seagrass size, carbon and nitrogen content, as well as latitude, sea surface temperature, salinity, chlorophyll, and sediment grain size, were tested as potential drivers. We found that shallow meadows can be subjected to intense herbivory, with variation in herbivory largely explained by fish density, seagrass size, and annual sea temperature range. The herbivorous fish density was the most important determinant of such variation, with the dominant seagrass consumer, the fish Sarpa salpa, absent at meadows from regions with low herbivory. In temperate regions where herbivorous fish are present, annual temperature ranges drive an intense summer herbivory, which is likely mediated not only by increased herbivore metabolic demands at higher temperatures, but also by higher fish densities. Invertebrate grazing (mainly by sea urchins, isopods, amphipods, and/or gastropods) was the dominant leaf herbivory in some temperate meadows, with grazing variation mainly influenced by seagrass shoot size. At the subtropical region (under reduced annual temperature range), lower shoot densities and seagrass nitrogen contents contributed to explain the almost null herbivory. We evidenced the combined influence of drivers acting at geographic (region) and local (meadow) scales, the understanding of which is critical for a clear prediction of variation in seagrass herbivory intensity across biogeographical regions.

Resistance of seagrass habitats to ocean acidification via altered interactions in a tri-trophic chain.

Despite the wide knowledge about prevalent effects of ocean acidification on single species, the consequences on species interactions that may promote or prevent habitat shifts are still poorly understood. Using natural CO2 vents, we investigated changes in a key tri-trophic chain embedded within all its natural complexity in seagrass systems. We found that seagrass habitats remain stable at vents despite the changes in their tri-trophic components. Under high pCO2, the feeding of a key herbivore (sea urchin) on a less palatable seagrass and its associated epiphytes decreased, whereas the feeding on higher-palatable green algae increased. We also observed a doubled density of a predatory wrasse under acidified conditions. Bottom-up CO2 effects interact with top-down control by predators to maintain the abundance of sea urchin populations under ambient and acidified conditions. The weakened urchin herbivory on a seagrass that was subjected to an intense fish herbivory at vents compensates the overall herbivory pressure on the habitat-forming seagrass. Overall plasticity of the studied system components may contribute to prevent habitat loss and to stabilize the system under acidified conditions. Thus, preserving the network of species interactions in seagrass ecosystems may help to minimize the impacts of ocean acidification in near-future oceans.

Using seagrasses to identify local and large-scale trends of metals in the Mediterranean Sea.

To manage trace metal pollution it is critical to determine how much temporal trends can be attributed to local or large-scale sources. We tracked changes in metal content in the seagrass Posidonia oceanica, along the NW Mediterranean from 2003 to 2010. While Cu, Cd and Ni showed a large inter-site variation, likely due to local factors, Fe, Mn and Pb showed little local variation and synchronous interannual variability across sites, most likely due to large-scale sources. Zn showed equal importance of local and large-scale sources of variation. Temporal trends of Ni, Zn, Cd, Cu remained almost stable. In contrast, Fe, Mn and Pb slightly increased in the last decade. These trends suggest that metals like Cu, Cd, Ni can be effectively managed at local scale. Whereas, elements like Fe, Mn and Pb have an important large-scale component that needs to be managed across the frontiers of national jurisdictions.

Altered epiphyte community and sea urchin diet in Posidonia oceanica meadows in the vicinity of volcanic CO2 vents.

Ocean acidification (OA) predicted for 2100 is expected to shift seagrass epiphyte communities towards the dominance of more tolerant non-calcifying taxa. However, little is known about the indirect effects of such changes on food provision to key seagrass consumers. We found that epiphyte communities of the seagrass Posidonia oceanica in two naturally acidified sites (i.e. north and south sides of a volcanic CO2 vent) and in a control site away from the vent at the Ischia Island (NW Mediterranean Sea) significantly differed in composition and abundance. Such differences involved a higher abundance of non-calcareous crustose brown algae and a decline of calcifying polychaetes in both acidified sites. A lower epiphytic abundance of crustose coralline algae occurred only in the south side of the vents, thus suggesting that OA may alter epiphyte assemblages in different ways due to interaction with local factors such as differential fish herbivory or hydrodynamics. The OA effects on food items (seagrass, epiphytes, and algae) indirectly propagated into food provision to the sea urchin Paracentrotus lividus, as reflected by a reduced P. oceanica exploitation (i.e. less seagrass and calcareous epiphytes in the diet) in favour of non-calcareous green algae in both vent sites. In contrast, we detected no difference close and outside the vents neither in the composition of sea urchin diet nor in the total abundance of calcareous versus non-calcareous taxa. More research, under realistic scenarios of predicted pH reduction (i.e. ≤ 0.32 units of pH by 2100), is still necessary to better understand cascading effects of this altered urchin exploitation of food resources under acidified conditions on ecosystem diversity and function.

The Role of Seagrass Traits in Mediating Zostera noltei Vulnerability to Mesograzers.

Understanding how intra-specific differences in plant traits mediate vulnerability to herbivores of relevant habitat-forming plants is vital to attain a better knowledge on the drivers of the structure and functioning of ecosystems. Such studies, however, are rare in seagrass-mesograzer systems despite the increasingly recognized relevance of mesograzers as seagrass consumers. We investigated the role and potential trade-offs of multiple leaf traits in mediating the vulnerability of the seagrass Zostera noltei to different mesograzer species, the amphipod Gammarus insensibilis and the isopod Idotea chelipes. We worked with plants from two different meadows for which contrasting chemical and structural traits were expected based on previous information. We found that plants with high vulnerability to mesograzers (i.e. those preferred and subjected to higher rates of leaf area loss) had not only higher nitrogen content and lower C:N, fibre, and phenolics, but also tender and thinner leaves. No trade-offs between chemical and structural traits of the seagrass were detected, as they were positively correlated. When leaf physical structure was removed using agar-reconstituted food, amphipod preference towards high-susceptibility plants disappeared; thus indicating that structural rather than chemical traits mediated the feeding preference. Removal of plant structure reduced the size of isopod preference to less than half, indicating a stronger contribution of structural traits (> 50%) but combined with chemical/nutritional traits in mediating the preference. We then hypothesized that the high environmental nutrient levels recorded in the meadow exhibiting high susceptibility modulate the differences observed between meadows in seagrass traits. To test this hypothesis, we exposed low-vulnerability shoots to eutrophic nutrient levels in a 6-week enrichment experiment. Nutrient enrichment increased Z. noltei nitrogen content and lowered C:N, fibre, and phenolics, but had no effect on structural traits. Overall, our findings help to better understand the trait-mediated seagrass susceptibility to mesograzers and reinforce the increasingly recognized role of structural defences against herbivory.

Specificity in Mesograzer-Induced Defences in Seagrasses.

Grazing-induced plant defences that reduce palatability to herbivores are widespread in terrestrial plants and seaweeds, but they have not yet been reported in seagrasses. We investigated the ability of two seagrass species to induce defences in response to direct grazing by three associated mesograzers. Specifically, we conducted feeding-assayed induction experiments to examine how mesograzer-specific grazing impact affects seagrass induction of defences within the context of the optimal defence theory. We found that the amphipod Gammarus insensibilis and the isopod Idotea chelipes exerted a low-intensity grazing on older blades of the seagrass Cymodocea nodosa, which reflects a weak grazing impact that may explain the lack of inducible defences. The isopod Synischia hectica exerted the strongest grazing impact on C. nodosa via high-intensity feeding on young blades with a higher fitness value. This isopod grazing induced defences in C. nodosa as indicated by a consistently lower consumption of blades previously grazed for 5, 12 and 16 days. The lower consumption was maintained when offered tissues with no plant structure (agar-reconstituted food), but showing a reduced size of the previous grazing effect. This indicates that structural traits act in combination with chemical traits to reduce seagrass palatability to the isopod. Increase in total phenolics but not in C:N ratio and total nitrogen of grazed C. nodosa suggests chemical defences rather than a modified nutritional quality as primarily induced chemical traits. We detected no induction of defences in Zostera noltei, which showed the ability to replace moderate losses of young biomass to mesograzers via compensatory growth. Our study provides the first experimental evidence of induction of defences against meso-herbivory that reduce further consumption in seagrasses. It also emphasizes the relevance of grazer identity in determining the level of grazing impact triggering resistance and compensatory responses of different seagrass species.

Responses of seagrass to anthropogenic and natural disturbances do not equally translate to its consumers.

Coastal communities are under threat from many and often co-occurring local (e.g., pollution, eutrophication) and global stressors (e.g., climate change), yet understanding the interactive and cumulative impacts of multiple stressors in ecosystem function is far from being accomplished. Ecological redundancy may be key for ecosystem resilience, but there are still many gaps in our understanding of interspecific differences within a functional group, particularly regarding response diversity, that is, whether members of a functional group respond equally or differently to anthropogenic stressors. Herbivores are critical in determining plant community structure and the transfer of energy up the food web. Human disturbances may alter the ecological role of herbivory by modifying the defense strategies of plants and thus the feeding patterns and performance of herbivores. We conducted a suite of experiments to examine the independent and interactive effects of anthropogenic (nutrient and CO2 additions) and natural (simulated herbivory) disturbances on a seagrass and its interaction with two common generalist consumers to understand how multiple disturbances can impact both a foundation species and a key ecological function (herbivory) and to assess the potential existence of response diversity to anthropogenic and natural changes in these systems. While all three disturbances modified seagrass defense traits, there were contrasting responses of herbivores to such plant changes. Both CO2 and nutrient additions influenced herbivore feeding behavior, yet while sea urchins preferred nutrient-enriched seagrass tissue (regardless of other experimental treatments), isopods were deterred by these same plant tissues. In contrast, carbon enrichment deterred sea urchins and attracted isopods, while simulated herbivory only influenced isopod feeding choice. These contrasting responses of herbivores to disturbance-induced changes in seagrass help to better understand the ecological functioning of seagrass ecosystems in the face of human disturbances and may have important implications regarding the resilience and conservation of these threatened ecosystems.

Biotic indices for assessing the status of coastal waters: a review of strengths and weaknesses.

Biotic indices have become key assessment tools in most recent national and trans-national policies aimed at improving the quality of coastal waters and the integrity of their associated ecosystems. In this study we analyzed 90 published biotic indices, classified them into four types, and analyzed the strengths and weaknesses of each type in relation to the requirements of these policies. We identified three main type-specific weaknesses. First, the problems of applicability, due to practical and conceptual difficulties, which affect most indices related to ecosystem function. Second, the failure of many indices based on structural attributes of the community (e.g. taxonomic composition) to link deterioration with causative stressors, or to provide an early-detection capacity. Third, the poor relevance to the ecological integrity of indices based on attributes at the sub-individual level (e.g. multi-biomarkers). Additionally, most indices still fail on two further aspects: the broad-scale applicability and the definition of reference conditions. Nowadays, the most promising approach seems to be the aggregation of indices with complementary strengths, and obtained from different biological communities.

A multivariate index based on the seagrass Posidonia oceanica (POMI) to assess ecological status of coastal waters under the water framework directive (WFD).

We propose here a multivariate index based on structural and functional attributes of the Posidonia oceanica ecosystem (Posidonia oceanica multivariate index: POMI) to assess the ecological status of coastal waters following WFD requirements. POMI is based on the combination, through principal component analysis, of physiological, morphological, structural and community level seagrass descriptors (or metrics), univocally related to environmental quality. Scores on the first axis are normalised to a 0-1 scale (EQR) using reference and worst sites. The index was tested by sampling 22 seagrass beds in the Catalan coast (ca. 500 km, NW Mediterranean). The results show a clustering of variables on both sides of the first axis of the PCA, indicating a common relation of all metrics with ecological status. Moreover, the values (EQR) obtained reflect human pressure levels. The proposed index allows a practical and relatively simple assessment of the ecological status of coastal waters, and contains a considerable amount of ecological information, which can be useful for managing purposes.