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Impacts of Ocean Acidification on Marine Shelled Molluscs

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Impacts of Ocean Acidification on Marine Shelled Molluscs Mar Biol DOI 10.1007/s00227-013-2219-3 ORIGINAL PAPER Impacts of ocean acidification on marine shelled molluscs Fre´de´ric Gazeau • Laura M. Parker • Steeve Comeau • Jean-Pierre Gattuso • Wayne A. O’Connor • Sophie Martin • Hans-Otto Po¨rtner • Pauline M. Ross Received: 18 January 2013 / Accepted: 15 March 2013 Ó Springer-Verlag Berlin Heidelberg 2013 Abstract Over the next century, elevated quantities of ecosystem services including habitat structure for benthic atmospheric CO2 are expected to penetrate into the oceans, organisms, water purification and a food source for other causing a reduction in pH (-0.3/-0.4 pH unit in the organisms. The effects of ocean acidification on the growth surface ocean) and in the concentration of carbonate ions and shell production by juvenile and adult shelled molluscs (so-called ocean acidification). Of growing concern are the are variable among species and even within the same impacts that this will have on marine and estuarine species, precluding the drawing of a general picture. This organisms and ecosystems. Marine shelled molluscs, which is, however, not the case for pteropods, with all species colonized a large latitudinal gradient and can be found tested so far, being negatively impacted by ocean acidifi- from intertidal to deep-sea habitats, are economically cation. The blood of shelled molluscs may exhibit lower and ecologically important species providing essential pH with consequences for several physiological processes (e.g. respiration, excretion, etc.) and, in some cases, increased mortality in the long term. While fertilization Communicated by S. Dupont. may remain unaffected by elevated pCO2, embryonic and Fre´de´ric Gazeau and Laura M. Parker have contributed equally to this larval development will be highly sensitive with important work. reductions in size and decreased survival of larvae, increases in the number of abnormal larvae and an increase Electronic supplementary material The online version of this in the developmental time. There are big gaps in the current article (doi:10.1007/s00227-013-2219-3) contains supplementary material, which is available to authorized users. understanding of the biological consequences of an F. Gazeau Á J.-P. Gattuso W. A. O’Connor Laboratoire d’Oce´anographie de Villefranche, CNRS-INSU, Industry and Investment NSW, Port Stephens Fisheries Centre, BP 28, 06234 Villefranche-sur-Mer Cedex, France Taylors Beach, NSW 2316, Australia F. Gazeau (&) Á J.-P. Gattuso S. Martin Universite´ Pierre et Marie Curie-Paris 6, Observatoire Laboratoire Adaptation & Diversite´ du Milieu Marin, CNRS- Oce´anologique de Villefranche, 06230 Villefranche-sur-Mer INSU, Station Biologique de Roscoff, 29682 Roscoff, France Cedex, France e-mail: [email protected] S. Martin Laboratoire Adaptation & Diversite´ du Milieu Marin, Universite´ L. M. Parker (&) Á P. M. Ross Pierre et Marie Curie, Station Biologique de Roscoff, School of Natural Sciences, Ecology and Environment Research 29682 Roscoff, France Group, College of Health and Science, University of Western Sydney, Hawkesbury H4, Locked Bag 1797, Penrith South DC H.-O. Po¨rtner 1797, Sydney, NSW, Australia Alfred-Wegener-Institut fu¨r Polar-und Meeresforschung, e-mail: [email protected] O¨ kophysiologie und O¨ kotoxikologie, Postfach 120161, 27515 Bremerhaven, Germany S. Comeau Department of Biology, California State University, 18111 Nordhoff Street, Northridge, CA 91330-8303, USA 123 Mar Biol acidifying ocean on shelled molluscs. For instance, the source for other organisms in their ecosystem. In addition, natural variability of pH and the interactions of changes in shelled molluscs have a significant economic value as the the carbonate chemistry with changes in other environ- global shellfish aquaculture industry reached a global value mental stressors such as increased temperature and of US$ 13.1 billion in 2008 (FAO 2008). In recent decades, changing salinity, the effects of species interactions, as severe declines in shelled mollusc populations have been well as the capacity of the organisms to acclimate and/or reported. Surveys conducted annually along the coast of adapt to changing environmental conditions are poorly British Columbia have shown a decline of up to 80 % in described. some populations since 1978 (Hankewich and Lessard 2006). Moreover, in hatcheries located on the northwest coast of the USA, there has been a year-by-year decline in Introduction the survival of oyster larvae since 2005, which appears to be connected to the upwelling of acidified deep waters The Mollusca is a very large and highly diverse phylum of shifting coastward and associated near-shore ocean acidi- invertebrate animals. There are between 50,000 and fication (Barton et al. 2012). Indeed, Feely et al. (2008) 120,000 described living molluscan species (Chapman have noticed that even though seasonal upwelling of waters 2009) among which around 30,000 species are found in undersaturated with aragonite (one of the most soluble marine environments (23 % of all marine organisms; metastable forms of calcium carbonate) is a natural feature Gosling 2003). Among the six classes of this phylum on the northern California shelf, the uptake of anthropo- (Gastropoda, Bivalvia, Cephalopoda, Polyplacophora, genic CO2 has increased the affected area over recent Scaphopoda and Monoplacophora), gastropods (i.e. stom- decades. ach–foot) and bivalves are the largest classes ([80 % of Ocean acidification poses a threat for ecologically and described living marine molluscan species). Information on economically important shelled molluscs. Losses in species the effects of ocean acidification is, to the best of our numbers and population densities due to ocean acidificat- knowledge, only available for Gastropoda, Bivalvia and ion would further drive habitat restructuring, changes in Cephalopoda. Besides the important differences in terms of food webs, losses of marine resources for human society as life cycle and metabolism between bivalves/gastropods and well as job losses for those working in industries associated cephalopods, only in one order of cephalopods (nautilus), with shelled molluscs (Newell 2004). In the present review, have organisms developed an external shell. For these we will discuss the ecological and biogeochemical roles reasons, this review paper will only focus on marine played by shelled molluscs and the use of these species by bivalves and gastropods (hereafter referred to as marine humans through aquaculture activities. We will then shelled molluscs). Marine shelled molluscs have a complex describe the present knowledge on the formation of the life cycle, which often includes a pelagic embryonic and shell and review the current literature on the effects of larval stage followed by a benthic (sometimes sessile) ocean acidification on adults, juveniles and early-life-his- juvenile and adult stage. Furthermore, shelled molluscs are tory stages of shelled molluscs. Finally, we will highlight found in a wide variety of ecological niches in marine, the current gaps in our understanding and the need for freshwater and terrestrial habitats. For instance, gastropods future research. can be found from the poles to the tropics as they adapt to a wide range of environmental conditions on Earth, having colonized aquatic and terrestrial habitats. Although some of A short primer on marine shelled molluscs the most familiar gastropods are terrestrial (snails and slugs), more than two-thirds of all extant species live in a Ecological and biogeochemical importance of marine marine environment. Although gastropods are mostly shelled molluscs associated with life in intertidal rocky-shore habitats, they can be found in deep basins and have been found in Shelled marine molluscs are recognized as key species at extreme environments close to hydrothermal vents (e.g. the ecosystem level, as they have the potential to impact Suzuki et al. 2006). In contrast to gastropods, bivalves only both community structure and ecosystem functioning. Most exist in aquatic environments. In the sea, they also colonize bivalve molluscs are suspension-feeders that clear seston a large latitudinal gradient and can be found from intertidal particles greater than *1to7lm from the water column to deep-sea habitats (e.g. Tunnicliffe et al. 2009). (Winter 1978). They have major effects on the degradation As detailed in the following section, shelled molluscs of pelagic organic matter and divert energy flow from provide essential ecosystem services including the forma- planktonic to benthic food webs. By filtering phytoplank- tion of habitat structure for benthic organisms (e.g. mussel ton and other planktonic particles, bivalves assist in and oyster beds), water purification as well as being a food ‘‘clearing’’ the water (Asmus and Asmus 1991) and 123 Mar Biol increasing the penetration of light in the water column. The no attempt to estimate their contribution to the carbon resulting enhanced light availability is essential for the cycle on a global scale. In contrast to benthic shelled growth of macro- or micro-phytobenthic plants and algae, molluscs, there have been attempts to estimate the contri- which therefore benefit from bivalves in coastal ecosys- bution of shell production by pteropods (planktonic gas- tems (e.g. Miller et al. 1996; Newell and Koch 2004). tropods with a shell made out of aragonite) although these Feeding behaviours in gastropoda are more diverse as estimates are wide-ranging, from 10 to 50 % of the total marine gastropods include some that are herbivores,
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