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    The integrated impacts of marine acidification, temperature and precipitation changes on bivalve coastal biodiversity and fisheries: how to adapt?


    Scientific assessment of ocean acidification impacts on bivalves. Propose adaptation measures for bivalves aquaculture.


    Climate change and predictions of changes in air temperature and precipitation regimes will affect aquatic ecosystems functioning. Moreover, increasing atmospheric CO2 concentrations will lead to the acidification of coastal waters in the Mediterranean area, as around the world, and the consequences to animals with calcium carbonate shells are expected. The predicted changes in environmental conditions (temperature, salinity, pH) may alter physiological rates of bivalves, modifying their impact (filtration, respiration, excretion rates) on the ecosystem. These impacts need to be evaluated in integrative way.  Bivalves play an important role on ecosystem structure functioning since they link primary productivity with upper trophic levels. Moreover, bivalve species to be studied in this project also constitute important economic resources for fisheries and aquaculture in Galicia, Algarve, Adriatic and Golf of Tunis coastal areas. With this project, our first aim is to analyse the cumulative effects of temperature, precipitation and pH, as predicted in climate changes scenarios, on the most relevant bivalve species for the study areas, both in terms of ecologic and economic importance. Based on this knowledge, our second aim is to propose adaptation measures to sustain bivalve biodiversity, fisheries and aquaculture production in the Mediterranean estuaries and coastal waters. For achieving these aims we structured the project considering a bottom-up approach: starting by selecting the most relevant species to be studied, defining testing and calibrating the methodologies to be used, developing laboratory experiments, testing these experiments with in situ mesocosms and finally, testing and proposing adaptation measures to sustain bivalve assemblages and related economic uses and contribute to CO2 sequestration. The proposed solutions will be discussed with water managers, conservation and environmental areas responsible and with fisheries and aquacultures companies.
    Main findings and future research
    The experiments done in the Ria Formosa (Portugal) and in the Northern Adriatic sea, next to the Lagoon of Venice (Italy) revealed contrasting responses of the bivalves to marine acidification. Results obtained in the Northern Adriatic sea highlighted effects of seawater acidification at biochemical, cellular and organism level in both species considered. Detrimental effects were observed in adults exposed for short time to reduced pH and temperature/salinity variations (as foreseen in climate change scenarios), as well as the long-term exposure of juvenile bivalves to reduced pH, which caused severe damage to the shells of both species tested and reduced growth in one of those species (C. gallina). Furthermore, increased mortality, reduced capability to survive to aerial exposure and reduced well-being were found in animals maintained at high temperature and salinity values close to the tolerance limits of the species. Among the studied species, C. gallina was already known as less tolerant and demonstrated to suffer more severely from environmental changes, sea water acidification in particular.
    Alterations in physiological responses, such as filtration, respiration and excretion, were also observed in the Northern Adriatic sea. Immune parameters were affected by the experimental conditions tested, which suggests that some bivalves may have a reduced capability of defense against pathogens under future conditions of elevated CO2 and reduced pH. Variations in biochemical responses variously involved in metabolic pathways and mechanisms of defense from oxidative stress were also found. Overall, results from the Northern Adriatic sea indicate increased stress conditions for both mussels and clams exposed to reduced pH and extreme temperature/salinity values, suggesting weakening of natural populations followed by possible reduction of their presence/abundance and increased risk of local extinction.
    In general, the experiments done in the Ria Formosa lagoon showed a less detrimental response of the studied bivalves to seawater acidification. Juveniles of both species studied were able to survive more than 80 days exposed to extreme reductions of seawater pH (0.7 units). No dissolution or damage to the shells was observed, although mussels in the acidified treatments showed reduced net calcification, indicating that the composition or structure of the shell was affected. Some physiological parameters of R. decussatus were significantly affected by the acidification conditions tested. Reduced clearance, ingestion and respiration rates and increased the ammonia excretion rate were observed in the acidified treatments, which, in the long terms, will likely contribute to a slower growth of the clams. The physiological responses of the studied bivalves to seawater acidification were, therefore, also more varied than previously thought. The responses of the common species (M. galloprovincialis) also differed between locations and according to the stage of life cycle. This suggest that, even for the same species or process, the responses may be variable at local scales, which emphasizes the danger of extrapolating results from a few model species or from one region to another.
    It seems clear that there are unidentified variables interacting or mediating the effects of seawater acidification by CO2, which causes the effects to be site-specific. The most remarkable characteristic of the carbonate chemistry of the water from Ría Formosa is the extremely high Total Alkalinity, probably associated to extremely alkaline runoff from continental waters, which prevented under-saturation of CaCO3, even in the most extreme acification treatments, minimizing the impact of the carbonate supply-side on calcification and the growth of the bivalves.
    Studying biological responses to ocean acidification in coastal, estuarine and transitional waters is particularly important because human interactions with marine organisms mainly occur within these areas. Nevertheless, the results obtained from sampling of natural intertidal mussel habitats of in the Galician Rías (Spain) clearly show that bivalves living in coastal and transitional waters are routinely exposed to greater variations in terms of seawater carbonate chemistry, relative to the open ocean. This has been suggested to reduce their sensitivity to future ocean acidification. Accordingly, we expect that local responses will be particularly relevant in coastal, estuarine and transitional waters.
    As is often the case in scientific research, the results of the ACIDBIV project clearly suggest more questions for future work than definitive answers for the proposed questions. One question that aroused particular interest was the possibility of interactions with the chemical composition of local seawater (carbonates, pollutants, etc) determining the biological effect of seawater acidification by CO2. Accordingly, two small experiments targeting these issues are being implemented in Padova (UNPD) and Algarve (CCMAR), using the same target-species.

    Added value for the Mediterranean scientific community

    The semi-enclosed geography of the Mediterranean Sea has many unique oceanographic and biogeographical features which could either serve to exacerbate or reduce future effects of increased concentrations of CO2 and ocean acidification (Fowler 2008). Anthropogenic stressors such as increasing river nutrient loads, atmospheric inputs, pollution, fishing and aquaculture activities combine with climate change-induced temperature increase and changes in seawater chemistry. Nevertheless, since the first biological consequences of marine acidification are expected to occur in high latitude seas, research on this topic is a recent trend in the Mediterranean sea and robust data are still scarce (CIESM 2008).
    Based on current knowledge, bivalves are expected to be among the first taxa to experience the adverse effects of ocean acidification. Considering the importance of bivalve aquaculture and commercial/artisanal fisheries in the Mediterranean basin, any adverse effect on the viability or productivity of living resources could have high socioeconomic significance. In this respect our results on both juveniles and adults of C. gallina in the Adriatic Sea pose serious concerns about maintenance of natural clam beds. Along the western Adriatic coasts, a dramatic decrease in population densities has already been observed due to heavy fishing effort, this decline in clam biomass being also enhanced by the occurrence of repeated mortality events, and recruitment failures.
    The ACIDBIV project made a small, but significant contribution to increase our understanding about synergistic effects of multiple climatic stressors (pH, temperature and salinity) on the survival, growth, calcification, ecophysiology and fitness of some of the most ecologically relevant and economically important bivalve species in the Mediterranean basin. It also allowed the development of a new line of research for the participating institutions and constituted a solid foundation for future research initiatives. Finally, in accordance with the objectives of the Circle-Med call, the project contributed to improve the integration of the research communities from the North and South rim of the Mediterranean, which is of crucial importance to successfully address the multiple challenges posed by climatic changes in this region.


    See also article in Regional Environmental Change supplement issue (Volume 14 - supplement 1 - Feb. 2014)


    Fernandez-Reiriz MJ, Range P, Alvarez-Salgado XA, Labarta U (submitted) Physiological energetics of juvenile clams (Ruditapes decussatus) in a high CO2 coastal ocean. MARINE ECOLOGY-PROGRESS SERIES.

    Range P, Chicharo MA, Ben-Hamadou R, Piló D, Matias D, Joaquim S, Oliveira AP, Chicharo L (2011) Calcification, growth and mortality of juvenile clams Ruditapes decussatus under increased pCO2 and reduced pH: variable responses to ocean
    acidification at local scales? J. Exp. Mar. Biol. Ecol. 396:177-184.

    Chinellato A., Munari M., Matozzo V., Bressan M., Marin M.G. (2010). First attempts in evaluating acidification effects on physiological responses in Mytilus galloprovincialis. 27th Congress of the new European Society of Comparative Biochemistry and Physiology, Alessandria (Italy) — Sept. 5–9, 2010, “Biological effects of climatic changes and pollution: from biomarkers to system biology”. Comparative Biochemistry and Physiology, Part A 157, S13. doi:10.1016/j.cbpa.2010.06.051

    Munari M., Chinellato A., Matozzo V., Bressan M., Marin M.G. (2010).Combined effects of temperature, salinity and pH on immune parameters in the clam Chamelea gallina. 27th Congress of the new European Society of Comparative Biochemistry and Physiology, Alessandria (Italy) — Sept. 5–9, 2010, “Biological effects of climatic changes and
    pollution: from biomarkers to system biology”. Comparative Biochemistry and Physiology, Part A 157, S14. doi:10.1016/j.cbpa.2010.06.052
    Munari M., Chinellato A., Matozzo V., Bressan M., Marin M.G. (2010). First attempts at evaluating combined effects of pH, temperature and salinity on haemocyte responses of the mussel Mytilus galloprovincialis. SETAC Europe, 20th Annual Meeting, 23-27 May 2010, Seville, Spain, Abstract book, WEPC1-2.

    Range P, Chicharo L, Chicharo MA, Ben-Hamadou R, Piló D, Matias D, Joaquim S, Oliveira AP (2010) Effects of ocean acidification on juvenile clams Ruditapes decussatus. In: Proceedings of the 39th CIESM Congress. International Commission for Scientific Exploration of the Mediterranean Sea, Venice, Italy, Italy, 10 - 14 May 2010, p. 789.


    Prof. Luis Chicharo: lchichar@ualg.pt

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