Effects of past, present, and future ocean carbon dioxide concentrations on the growth and survival of larval shellfish

Abstract

The combustion of fossil fuels has enriched levels of CO 2 in the world's oceans and decreased ocean pH. Although the continuation of these processes may alter the growth, survival, and diversity of marine organisms that synthesize CaCO 3 shells, the effects of ocean acidification since the dawn of the industrial revolution are not clear. Here we present experiments that examined the effects of the ocean's past, present, and future (21st and 22nd centuries) CO 2 concentrations on the growth, survival, and condition of larvae of two species of commercially and ecologically valuable bivalve shellfish (Mercenaria mercenaria and Argopecten irradians). Larvae grown under near preindustrial CO 2 concentrations (250 ppm) displayed significantly faster growth and metamorphosis as well as higher survival and lipid accumulation rates compared with individuals reared under modern day CO 2 levels. Bivalves grown under near preindustrial CO 2 levels displayed thicker, more robust shells than individuals grown at present CO 2 concentrations, whereas bivalves exposed to CO 2 levels expected later this century had shells that were malformed and eroded. These results suggest that the ocean acidification that has occurred during the past two centuries may be inhibiting the development and survival of larval shellfish and contributing to global declines of some bivalve populations.bivalve larvae | climate change | ocean acidification M ore than 8 Pg of carbon dioxide (CO 2 ) is released annually into our planet's atmosphere via the combustion of fossil fuels (1). About one-third of anthropogenically derived CO 2 has entered the world's oceans during the past two centuries (2) and atmospheric and surface ocean CO 2 levels are expected to reach ∼750 ppm by 2100 (3, 4). CO 2 entering the ocean decreases the availability of carbonate ions (CO 3 −2 ) and reduces ocean pH, a process known as ocean acidification. These changes in ocean chemistry may have dire consequences for ocean animals that produce hard parts made from calcium carbonate (CaCO 3 ). The experimental enrichment of CO 2 to levels expected in the coming century has been shown to dramatically alter the growth, survival, and morphology of numerous calcifying organisms including coccolithophores, coral reefs, crustose coralline algae, echinoderms, foraminifera, and pteropods (5-7). Many shellfish also produce calcareous shells, and juvenile and adult clams, mussels, and oysters have been shown to be adversely affected by elevated CO 2 (8-12). The earliest life history stages of shellfish, larvae, have been shown to be especially vulnerable to high CO 2 , displaying large declines in survival and delays in metamorphosis at levels predicted to occur later this century, suggesting recruitment of these populations may be adversely impacted by ocean acidification (12)(13)(14).Although it is clear that calcifying ocean animals such as shellfish are sensitive to the increases in CO 2 projected for the future, the extent to which the rise in CO 2 that has occurred since the dawn of ...

The Impact of Ocean Acidification on Reproduction, Early Development and Settlement of Marine Organisms

“…Prolonging the length of larval life is generally considered negatively because it increases the chance of predation in the water column, particularly in the absence of properly calcified shells and skeletons and reduces the time available to settle. Furthermore, reduced larval size can reduce the feeding efficiency of larvae [33,67], and smaller larvae are more susceptible to starvation because they encounter comparatively less food [33,[107][108][109]. There are also implications for energetics of larvae and larval dispersal.…”

“…There are also implications for energetics of larvae and larval dispersal. Altered energetics may influence metamorphosis as found in bivalves [67] with impaired metamorphosis [67,91] and flow on effects [10] to post settlement mortality. Therefore, even sub-lethal effects of elevated CO 2 can severely alter the composition and fitness of larvae and given the high mortality rates of larvae in the water column [6] and during the transition to benthic settlers, small perturbations to larvae potentially may have large alterations to settlement dynamics, post-settlement mortality, recruitment and ultimately adult populations.…”

“…A number of studies have found a delay in development or less development (the oysters Crassostrea gigas and Saccostrea glomerata [33,35,39]; the mussel M. galloprovincialis [57]; gastropod Littorina obtusata [63]), morphological shell abnormalities such as convex hinge and mantle protrusion and impacts on calcification size and growth rate (the oyster Crassostrea gigas [33,35,39]; the mussel M. galloprovincialis [57]; gastropod, Littorina obtusata shorter lateral, but longer spiral shell length [63] and Saccostrea glomerata [35,39,64]), decreases in shell length and thickness in the mussel (Mytilus edulis [65]), hatching rate (gastropod, Littorina obtusata [63], mussel Mytilus edulis [65]), degraded shells (mussel Mytilus edulis [65], polar pteropod Limacina helicina [66]) decreased rate of metamorphosis, shell thickness and loss of hinge integrity (bay scallop Argopecten irradians and the hard clam Mercenaria mercenaria [67]) and in the Mediterranean pteropod Cavolinia inflexa [68] shells were absent after 13 days due to dissolution, yet larvae displayed "normal" swimming action (Table S2). In rare instances there have been positive instead of negative impacts of elevated CO 2 .…”

Effects of ocean acidification on immune responses of the Pacific oyster Crassostrea gigas

“…Over the past 10 years, accumulating evidence suggests that OA could result in delayed embryonic development [8,9], decreased larval growth [10,11] and increased mortality [12] of many marine mollusks. Moreover, OA stress has also been found to affect many physiological processes, such as calcification [13], energy metabolism [14] and behavior [15,16] of calcifying organisms.…”

The oyster genome reveals stress adaptation and complexity of shell formation

“…Molluscs have vital roles in the functioning of marine, freshwater and terrestrial ecosystems, and have had major effects on humans, primarily as food sources but also as sources of dyes, decorative pearls and shells, vectors of parasites, and biofouling or destructive agents. Many molluscs are important fishery and aquaculture species, as well as models for studying neurobiology, biomineralization, ocean acidification and adaptation to coastal environments under climate change 2,3 . As the most speciose member of the Lophotrochozoa, phylum Mollusca is central to our understanding of the biology and evolution of this superphylum of protostomes.…”