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  • A review of common parameters and descriptors used in studies of the impacts of heavy metal pollution on marine macroalgae: identification of knowledge gaps and future needs
    Publication . Costa, Giulia Burle; Koerich, Gabrielle; Ramos, Bruna de; Ramlov, Fernanda; Martínez-Crego, Begoña; Costa, Monya; Jesus, Dora; Santos, Rui; Horta Jr., Paulo A.
    This study presents a systematic review to assess the main similarities and gaps in efforts to evaluate the impacts of heavy metals on benthic marine seaweeds. A total of 91 studies were compiled, the main parameters (abiotic, biological, ecotoxicological, and heavy metals) and descriptors of which were evaluated by quantitative and qualitative analyses. Our results indicate the importance of diversifying searches by including different languages (i.e. English, Portuguese and Spanish). Most of the studies were field characterizations, with few abiotic parameters and/or seasonality evaluations being employed. In contrast, the assessment of ecotoxicological parameters was highly frequent, which seems incoherent considering the absence of data to support the use of these results in biomonitoring applications. The genera Sargassum, Ulva and Enteromorpha were widely studied worldwide, apart from a small fraction of studies assessing higher levels of biological organization. Moreover, the use of different parameters and descriptors by the evaluated studies precludes making conclusive or reliable comparisons. These findings highlight the importance of greater efforts to construct a concise baseline of knowledge using similar parameters so that global evaluations of the impacts of heavy metals on photosynthetic organisms can be undertaken.
  • Influence of seagrass meadows on nursery and fish provisioning ecosystem services delivered by Ria Formosa, a coastal lagoon in Portugal
    Publication . Erzini, Karim; Parreira, Filipe; Sadat, Zineb; Castro, Margarida; Bentes, Luis; Coelho, Rui; Gonçalves, Jorge Manuel Santos; Lino, Pedro G.; Martínez-Crego, Begoña; Monteiro, Pedro; Oliveira, Frederico; Ribeiro, Joaquim; de los Santos, Carmen B.; Santos, Rui
    This study is the first to evaluate the fish provisioning services of a whole transitional landscape (Ria Formosa lagoon, Portugal), in parallel with the enhancement of growth, survival and production of single cohorts of the most important commercial fish species by vegetated and unvegetated sub-tidal habitats. Based on monthly beach seine samples, total density and biomass of 96 species of fishes were 1.89 and 3.03 times greater in vegetated habitats than unvegetated habitats, respectively. Vegetated habitat enhanced survival in six of eight commercial species for which survival could be estimated in both habitats. The total production of all 12 commercially important species within vegetated habitat was approximately double that of unvegetated habitat, with production enhancement in 7 of 12 species ranging from 1.8 to 169-fold for the vegetated habitats. Within the lagoon, vegetated sub-tidal habitat covers an area 5-fold smaller than unvegetated habitat, yet it accounts for 27.1 % of fish production. Estimated total lifetime economic values of the single cohorts of the 12 commercial species were between 30 million and 59 million EUR. An exceptionally strong year class of the European seabass (Dicentrarchus labrax), a species with higher density and biomass in unvegetated habitat, accounts for the higher overall values per hectare for unvegetated habitat (Low natural mortality (M): EUR 32,844 ha-1; High M: EUR 16,751 ha-1) than for vegetated habitat (Low M: EUR 22,028 ha-1; High M: EUR 10,700 ha-1). These results highlight the enormous importance of temperate coastal lagoons as a nursery and source of recruits for coastal fisheries. Our evaluation of fish provisioning services based on data for individual cohorts of fish for a whole transitional landscape is a stronger and more valid approach for estimating future biomass and value than previous studies based on mean densities and biomasses of fish that did not distinguish between cohorts.
  • CO2 and nutrient-driven changes across multiple levels of organization in zostera noltii ecosystems
    Publication . Martínez-Crego, Begoña; Olivé, Irene; Santos, Rui
    Increasing evidence emphasizes that the effects of human impacts on ecosystems must be investigated using designs that incorporate the responses across levels of biological organization as well as the effects of multiple stressors. Here we implemented a mesocosm experiment to investigate how the individual and interactive effects of CO2 enrichment and eutrophication scale-up from changes in primary producers at the individual (biochemistry) or population level (production, reproduction, and/ or abundance) to higher levels of community (macroalgae abundance, herbivory, and global metabolism), and ecosystem organization (detritus release and carbon sink capacity). The responses of Zostera noltii seagrass meadows growing in low-and high-nutrient field conditions were compared. In both meadows, the expected CO2 benefits on Z. noltii leaf production were suppressed by epiphyte overgrowth, with no direct CO2 effect on plant biochemistry or population-level traits. Multi-level meadow response to nutrients was faster and stronger than to CO2. Nutrient enrichment promoted the nutritional quality of Z. noltii (high N, low C : N and phenolics), the growth of epiphytic pennate diatoms and purple bacteria, and shoot mortality. In the low-nutrient meadow, individual effects of CO2 and nutrients separately resulted in reduced carbon storage in the sediment, probably due to enhanced microbial degradation of more labile organic matter. These changes, however, had no effect on herbivory or on community metabolism. Interestingly, individual effects of CO2 or nutrient addition on epiphytes, shoot mortality, and carbon storage were attenuated when nutrients and CO2 acted simultaneously. This suggests CO2-induced benefits on eutrophic meadows. In the high-nutrient meadow, a striking shoot decline caused by amphipod overgrazing masked the response to CO2 and nutrient additions. Our results reveal that under future scenarios of CO2, the responses of seagrass ecosystems will be complex and context-dependent, being mediated by epiphyte overgrowth rather than by direct effects on plant biochemistry. Overall, we found that the responses of seagrass meadows to individual and interactive effects of CO2 and nutrient enrichment varied depending on interactions among species and connections between organization levels.
  • Biodiversity consequences of Caulerpa prolifera takeover of a coastal lagoon
    Publication . Parreira, Filipe; Martínez-Crego, Begoña; Lourenço Afonso, Carlos Manuel; Machado, Margarida; Oliveira, Frederico; Gonçalves, Jorge Manuel Santos; Santos, Rui
    The genus Caulerpa has attracted much attention because many of its species were introduced into non-native regions and became notoriously invasive. This is the case of Caulerpa prolifera that has been rapidly expanding in Ria Formosa lagoon, taking over the deeper unvegetated soft bottoms and competing with seagrass meadows in the shallower areas. Here we address how C. prolifera invasion may affect the support of biodiversity, and specifically, the provision of habitat and nursery for commercial species by the native habitats of this coastal lagoon. Even though no significant differences in total species richness, diversity and evenness were found between C. prolifera and the native unvegetated habitat, the dissimilarity between these two habitats was highest, mostly driven by the extreme reduction of the gastropod Bittium reticulatum and of the tanaid Apseudopsis formosus. This may implicate changes in the trophic interactions of the ecosystem, for example decreasing the tanaid food source for seahorses, which are presently endangered in the lagoon. On the other hand, the fauna species richness, diversity and evenness were significantly higher in the native seagrass habitat than in C. prolifera. Juveniles of valuable flat and sparid fish were only observed in unvegetated sediments and seagrass meadows, respectively. The aggressive spread of C. prolifera in Ria Formosa may alter the structure of native faunal communities, with likely negative implications on fisheries. Nevertheless, the global biodiversity of the lagoon will not be likely drastically affected unless the seaweed takes over the seagrass meadows.
  • Resistance of seagrass habitats to ocean acidification via altered interactions in a tri-trophic chain
    Publication . Martínez-Crego, Begoña; Vizzini, Salvatrice; Califano, Gianmaria; Massa-Gallucci, Alexia; Andolina, Cristina; Gambi, Maria Cristina; Santos, Rui
    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
    Publication . Roca, Guillem; Romero, Javier; Farina, Simone; Martínez-Crego, Begoña; Alcoverro, Teresa
    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.
  • Drivers of variation in seagrass-associated amphipods across biogeographical areas
    Publication . Navarro-Mayoral, Sandra; Tuya, Fernando; Prado, Patricia; Marco-Méndez, Candela; Fernandez-Gonzalez, Victoria; Fernández-Torquemada, Yolanda; Espino, Fernando; Antonio de la Ossa, Jose; Vilella, David Mateu; Machado, Margarida; Martínez-Crego, Begoña
    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 biogeo-graphical areas across 2000 Km and 13 degrees 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 envi-ronmental conditions, finding that structurally more complex meadows harboring higher abundance and rich-ness of amphipods associated.
  • Effects of nutrient enrichment on seagrass population dynamics: evidence and synthesis from the biomass-density relationships
    Publication . Cabaco, Susana; Apostolaki, Eugenia T.; Garcia-Marin, Patricia; Gruber, Renee; Hernandez, Ignacio; Martinez-Crego, Begona; Mascaro, Oriol; Perez, Marta; Prathep, Anchana; Robinson, Cliff; Romero, Javier; Schmidt, Allison L.; Short, Fred T.; van Tussenbroek, Brigitta I.; Santos, Rui
    The available data from experimental and descriptive studies on seagrass biomass and density responses to nutrient enrichment were analysed to assess the intraspecific mechanisms operating within seagrass populations and whether biomass-density relationships can provide relevant metrics for monitoring seagrasses. The response of shoot biomass and density to nutrient enrichment was dependent on the type of study; the short-term positive response of biomass and density in experimental studies reveals context-specific nutrient limitation of seagrasses. The long-term negative response of descriptive studies probably results from ecosystem-scale events related to nutrient enrichment such as increased turbidity, algal blooms, epiphyte loads and anoxia. Most seagrass species analysed lie in the nonthinning part of the theoretical biomass-density curves. A simultaneous increase in biomass and decrease in density, evidence of self-thinning, were only observed in 4 of 28 studies. The analysis of both the static and the dynamic biomass-density relationships revealed that the slopes increase under nutrient enrichment. Surprisingly, the species-specific slopes (log B-log D) were higher than one, revealing that the B/D ratio, that is, the average shoot biomass, increases with density in all seagrass species analysed. Nutrient enrichment further enhanced this effect as biomass-density slopes increased to even higher values. The main drivers behind the increasing biomass-density slopes under nutrient enrichment were the increase in shoot biomass at densities above a species-specific threshold and/or its decrease below that threshold. Synthesis. Contrasting short- and long-term responses of both biomass and density of seagrasses to nutrient enrichment suggest that the former, positive ones result from nutrient limitation, whereas the later, negative ones are mediated by whole ecosystem responses. In general, shoot biomass of seagrasses increases with density, and nutrient enrichment enhances this effect. Experimental testing of facilitation processes related to clonal integration in seagrasses needs to be done to reveal whether they determine the low incidence of self-thinning and the intriguing biomass-density relationships of seagrass species. The increasing slopes and decreasing intercepts of the species-specific dynamic biomass-density relationships of seagrasses and the decreasing coefficients of variation of both biomass and density constitute relevant, easy-to-collect metrics that may be used in environmental monitoring.