Over the next century, elevated quantities of atmospheric CO 2 are expected to penetrate into the oceans, causing a reduction in pH (-0.3/-0.4 pH unit in the surface ocean) and in the concentration of carbonate ions (so-called ocean acidification). Of growing concern are the impacts that this will have on marine and estuarine organisms and ecosystems. Marine shelled molluscs, which colonized a large latitudinal gradient and can be found from intertidal to deep-sea habitats, are economically and ecologically important species providing essential ecosystem services including habitat structure for benthic organisms, water purification and a food source for other organisms. The effects of ocean acidification on the growth and shell production by juvenile and adult shelled molluscs are variable among species and even within the same species, precluding the drawing of a general picture. This is, however, not the case for pteropods, with all species tested so far, being negatively impacted by ocean acidification. The blood of shelled molluscs may exhibit lower pH with consequences for several physiological processes (e.g. respiration, excretion, etc.) and, in some cases, increased mortality in the long term. While fertilization may remain unaffected by elevated pCO 2 , embryonic and larval development will be highly sensitive with important reductions in size and decreased survival of larvae, increases in the number of abnormal larvae and an increase in the developmental time. There are big gaps in the current understanding of the biological consequences of an Communicated by S. Dupont.Frédéric Gazeau and Laura M. Parker have contributed equally to this work.Electronic supplementary material The online version of this article
It is essential to predict the impact of elevated Pco 2 on marine organisms and habitats to anticipate the severity and consequences of future ocean chemistry change. Despite the importance of carry-over effects in the evolutionary history of marine organisms, few studies have considered links between life-history stages when determining how marine organisms will respond to elevated Pco 2 , and none have considered the link between adults and their offspring. Herein, we exposed adults of wild and selectively bred Sydney rock oysters, Saccostrea glomerata to elevated Pco 2 during reproductive conditioning and measured the development, growth and survival response of their larvae. We found that elevated Pco 2 had a negative impact on larvae of S. glomerata causing a reduction in growth, rate of development and survival. Exposing adults to elevated Pco 2 during reproductive conditioning, however, had positive carry-over effects on larvae. Larvae spawned from adults exposed to elevated Pco 2 were larger and developed faster, but displayed similar survival compared with larvae spawned from adults exposed to ambient Pco 2 . Furthermore, selectively bred larvae of S. glomerata were more resilient to elevated Pco 2 than wild larvae. Measurement of the standard metabolic rate (SMR) of adult S. glomerata showed that at ambient Pco 2 , SMR is increased in selectively bred compared with wild oysters and is further increased during exposure to elevated Pco 2 . This study suggests that sensitive marine organisms may have the capacity to acclimate or adapt to elevated Pco 2 over the next century and a change in energy turnover indicated by SMR may be a key process involved.
Elevations in atmospheric carbon dioxide (CO2) are anticipated to acidify oceans because of fundamental changes in ocean chemistry created by CO2 absorption from the atmosphere. Over the next century, these elevated concentrations of atmospheric CO2 are expected to result in a reduction of the surface ocean waters from 8.1 to 7.7 units as well as a reduction in carbonate ion (CO32−) concentration. The potential impact that this change in ocean chemistry will have on marine and estuarine organisms and ecosystems is a growing concern for scientists worldwide. While species-specific responses to ocean acidification are widespread across a number of marine taxa, molluscs are one animal phylum with many species which are particularly vulnerable across a number of life-history stages. Molluscs make up the second largest animal phylum on earth with 30,000 species and are a major producer of CaCO3. Molluscs also provide essential ecosystem services including habitat structure and food for benthic organisms (i.e., mussel and oyster beds), purification of water through filtration and are economically valuable. Even sub lethal impacts on molluscs due to climate changed oceans will have serious consequences for global protein sources and marine ecosystems.
This study investigated the synergistic effects of ocean acidification (caused by elevations in the partial pressure of carbon dioxide pCO 2 ) and temperature on the fertilization and embryonic development of the economically and ecologically important Sydney rock oyster, Saccostrea glomerata (Gould 1850). As pCO 2 increased, fertilization significantly decreased. The temperature of 26 1C was the optimum temperature for fertilization, as temperature increased and decreased from this optimum, fertilization decreased. There was also an effect of pCO 2 and temperature on embryonic development. Generally as pCO 2 increased, the percentage and size of D-veligers decreased and the percentage of Dveligers that were abnormal increased. The optimum temperature was 26 1C and embryonic development decreased at temperatures that were above and below this temperature. Abnormality of D-veligers was greatest at 1000 ppm and 18 and 30 1C (! 90%) and least at 375 ppm and 26 1C ( 4%). Finally prolonged exposure of elevated pCO 2 and temperature across early developmental stages led to fewer D-veligers, more abnormality and smaller sizes in elevated CO 2 environments and may lead to lethal effects at suboptimal temperatures. Embryos that were exposed to the pCO 2 and temperature treatments for fertilization and embryonic development had fewer D-veligers, greater percentage of abnormality and reduced size than embryos that were exposed to the treatments for embryonic development only. Further at the elevated temperature of 30 1C and 750-1000 ppm, there was no embryonic development. The results of this study suggest that predicted changes in ocean acidification and temperature over the next century may have severe implications for the distribution and abundance of S. glomerata as well as possible implications for the reproduction and development of other marine invertebrates.
Predicting the impact of warming and acidifying on oceans on the early development life history stages of invertebrates although difficult, is essential in order to anticipate the severity and consequences of future climate change. This review summarises the current literature and meta-analyses on the early life-history stages of invertebrates including fertilisation, larval development and the implications for dispersal and settlement of populations. Although fertilisation appears robust to near future predictions of ocean acidification, larval development is much more vulnerable and across invertebrate groups, evidence indicates that the impacts may be severe. This is especially for those many marine organisms which start to calcify in their larval and/or juvenile stages. Species-specificity and variability in responses and current gaps in the literature are highlighted, including the need for studies to investigate the total effects of climate change including the synergistic impact of temperature, and the need for long-term multigenerational experiments to determine whether vulnerable invertebrate species have the capacity to adapt to elevations in atmospheric CO 2 over the next century.
Ocean acidification (OA) is predicted to have widespread implications for marine organisms, yet the capacity for species to acclimate or adapt over this century remains unknown. Recent transgenerational studies have shown that for some marine species, exposure of adults to OA can facilitate positive carryover effects to their larval and juvenile offspring that help them to survive in acidifying oceanic conditions. But whether these positive carryover effects can persist into adulthood or the next generation is unknown. Here we tested whether positive carryover effects found in larvae of the oyster, Saccostrea glomerata following transgenerational exposure to elevated CO2, could persist into adulthood and whether subsequent transgenerational exposure of adults to elevated CO2 would facilitate similar adaptive responses in the next generation of larvae and juveniles. Following our previous transgenerational exposure of parental adults and first generation (F1) larvae to ambient (385 μatm) and elevated (856 μatm) CO2, newly settled F1 juveniles were transferred to the field at ambient CO2 for 14 months, until they reached reproductive maturity. At this time, the F1 adults were returned to the laboratory and the previous transgenerational CO2 exposure was repeated to produce F2 offspring. We found that the capacity of adults to regulate extracellular pH at elevated CO2 was improved if they had a prior history of transgenerational exposure to elevated CO2. In addition, subsequent transgenerational exposure of these adults led to an increase in the resilience of their larval and juvenile offspring. Offspring with a history of transgenerational exposure to elevated CO2 had a lower percentage abnormality, faster development rate, faster shell growth and increased heart rate at elevated CO2 compared with F2 offspring with no prior history of exposure to elevated CO2. Our results suggest that positive carryover effects originating during parental and larval exposure will be important in mediating some of the impacts of OA for later life-history stages and generations.
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