Non-calcifying larvae in a changing ocean: warming, not acidification/hypercapnia, is the dominant stressor on development of the sea star Meridiastra calcar

Climate change driven ocean warming and acidification is potentially detrimental to the sensitive planktonic life stages of benthic marine invertebrates. Research has focused on the effects of acidification on calcifying larvae with a paucity of data on species with alternate developmental strategies and on the interactive effects of warming and acidification. To determine the impact of climate change on a conspicuous component of the intertidal fauna of southeast Australia, the development of the non-calcifying lecithotrophic larvae of the sea star Meridiastra calcar was investigated in the setting of predicted ocean warming (+2-4°C) and acidification (-0.4-0.6 pH units) for 2100 and beyond in all combinations of stressors. Temperature and pH were monitored in the habitat of M. calcar to place experiments in context with current environmental conditions. There was no effect of temperature or pH on cleavage stage embryos but later development (gastrula-larvae) was negatively effected by a +2°-4°C warming and there was a negative effect of -0.6 pH units on embryos reaching the hatched gastrula stage. Mortality and abnormal development in larvae increased significantly even with +2°C warming and larval growth was impaired at +4°C. For the range of temperature and pH conditions tested, there were no interactive effects of stressors across all stages monitored. For M. calcar, warming not acidification was the dominant stressor. A regression model incorporating data from this study and projected increasing SST for the region suggests an increase in larval mortality to 70% for M. calcar by 2100 in the absence of acclimation and adaptation. The broad distribution of this species in eastern Australia encompassing subtropical to cold temperate thermal regimes provides the possibility that local M. calcar populations may be sustained in a warming world through poleward migration of thermotolerant propagules, facilitated by the strong southward flow of the East Australian Current.

Effect of ocean acidification and temperature increase on the planktonic foraminifer Neogloboquadrina pachyderma (sinistral)

The present study investigated the effects of ocean acidification and temperature increase on Neogloboquadrina pachyderma (sinistral), the dominant planktonic foraminifer in the Arctic Ocean. Due to the naturally low concentration of CO32− in the Arctic, this foraminifer could be particularly sensitive to the forecast changes in seawater carbonate chemistry. To assess potential responses to ocean acidification and climate change, perturbation experiments were performed on juvenile and adult specimens by manipulating seawater to mimic the present-day carbon dioxide level and a future ocean acidification scenario (end of the century) under controlled (in situ) and elevated temperatures (1 and 4 °C, respectively). Foraminifera mortality was unaffected under all the different experiment treatments. Under low pH, N. pachyderma (s) shell net calcification rates decreased. This decrease was higher (30 %) in the juvenile specimens than decrease observed in the adults (21 %) ones. However, decrease in net calcification was moderated when both, pH decreased and temperature increased simultaneously. When only temperature increased, a net calcification rate for both life stages was not affected. These results show that forecast changes in seawater chemistry would impact calcite production in N. pachyderma (s), possibly leading to a reduction of calcite flux contribution and consequently a decrease in biologic pump efficiency.

Biometry and dissolution features of the benthic foraminiferal species Ammonia aomoriensis at high pCO2

Culturing experiments, simulating a projected future rise in atmospheric CO2 concentrations, were performed with the benthic foraminifer Ammonia aomoriensis from Flensburg Fjord, southwestern Baltic Sea. The experiments simulated a future rise in atmospheric CO2. We exposed living specimens to five seawater pCO2 levels ranging from 618 µatm (pH 7.9) to 3130 µatm (pH 7.2) for six weeks. Growth rates and mortality differed significantly between pCO2 treatments. The highest increase of mean test diameter by 19% was observed at 618 µatm. At partial pressures >1829 µatm, the mean test diameter decreased during the experiment by up to 22% at 3130 µatm. At pCO2 levels of 618 and 751 µatm, the tests of A. aomoriensis were found intact after the experiment. The last chambers of specimens incubated at 929 and 1829 µatm were severely damaged by corrosion. Visual inspection of specimens incubated at 3130 µatm revealed wall dissolution of all outer chambers, and only the inner organic lining stayed intact. Our results demonstrate that pCO2 values of 929 µatm and above cause reduced growth of A. aomoriensis and lead to shell dissolution in Baltic Sea waters. The bottom waters in Flensburg Fjord and adjacent areas regularly experience pCO2 levels in this range during summer and fall. Therefore, increasing atmospheric CO2-concentrations are likely to extend and intensify these periods of undersaturation. This may eventually slow down calcification in A. aomoriensis to the extent that net carbonate precipitation terminates. The possible disappearance of this species from the Baltic Sea and other areas prone to seasonal undersaturation would likely cause significant shifts in shallow water benthic ecosystems in the near future.

Impact of ocean acidification and elevated temperatures on early juveniles of the polar shelled pteropod Limacina helicina: mortality, shell degradation, and shell growth (update)

Due to their aragonitic shell, thecosome pteropods may be particularly vulnerable to ocean acidification driven by anthropogenic CO2 emissions. This applies specifically to species inhabiting Arctic surface waters that are projected to become temporarily and locally undersaturated with respect to aragonite as early as 2016. This study investigated the effects of rising partial pressure of CO2 (pCO2) and elevated temperature on pre-winter juveniles of the polar pteropod Limacina helicina. After a 29 day experiment in September/October 2009 at three different temperatures and under pCO2 scenarios projected for this century, mortality, shell degradation, shell diameter and shell increment were investigated. Temperature and pCO2 had a significant effect on mortality, but temperature was the overriding factor. Shell diameter, shell increment and shell degradation were significantly impacted by pCO2 but not by temperature. Mortality was 46% higher at 8 °C than at in situ temperature (3 °C), and 14% higher at 1100 μatm than at 230 μatm. Shell diameter and increment were reduced by 10 and 12% at 1100 μatm and 230 μatm, respectively, and shell degradation was 41% higher at elevated compared to ambient pCO2. We conclude that pre-winter juveniles will be negatively affected by both rising temperature and pCO2 which may result in a possible decline in abundance of the overwintering population, the basis for next year’s reproduction.

Elevated level of carbon dioxide affects metabolism and shell formation in oysters Crassostrea virginica

Estuarine organisms are exposed to periodic strong fluctuations in seawater pH driven by biological carbon dioxide (CO2) production, which may in the future be further exacerbated by the ocean acidification associated with the global rise in CO2. Calcium carbonate-producing marine species such as mollusks are expected to be vulnerable to acidification of estuarine waters, since elevated CO2 concentration and lower pH lead to a decrease in the degree of saturation of water with respect to calcium carbonate, potentially affecting biomineralization. Our study demonstrates that the increase in CO2 partial pressure (pCO2) in seawater and associated decrease in pH within the environmentally relevant range for estuaries have negative effects on physiology, rates of shell deposition and mechanical properties of the shells of eastern oysters Crassostrea virginica (Gmelin). High CO2 levels (pH ~7.5, pCO2 ~3500 µatm) caused significant increases in juvenile mortality rates and inhibited both shell and soft-body growth compared to the control conditions (pH ~8.2, pCO2 ~380 µatm). Furthermore, elevated CO2 concentrations resulted in higher standard metabolic rates in oyster juveniles, likely due to the higher energy cost of homeostasis. The high CO2 conditions also led to changes in the ultrastructure and mechanical properties of shells, including increased thickness of the calcite laths within the hypostracum and reduced hardness and fracture toughness of the shells, indicating that elevated CO2 levels have negative effects on the biomineralization process. These data strongly suggest that the rise in CO2 can impact physiology and biomineralization in marine calcifiers such as eastern oysters, threatening their survival and potentially leading to profound ecological and economic impacts in estuarine ecosystems.

Structural and geochemical alterations in the Mg calcite bryozoan Myriapora truncata under elevated seawater pCO2 simulating ocean acidification

The possible effects of ocean acidification on the calcareous skeleton of the Mediterranean bryozoan Myriapora truncata (Pallas, 1766) were studied by transplanting live and dead colonies into an area of natural volcanic CO2 vents at Ischia (Gulf of Naples, Tyrrhenian Sea), Italy. Morphology and geochemistry were compared between colonies from normal (mean pH = 8.07, min. pH 7.95), below-normal (mean pH 7.66, min. pH 7.32) and acidic (mean pH 7.43, min. pH 6.83) conditions after colonies had been exposed in situ for 45 and 128 days. Both distal (juvenile) and proximal (adult) parts of the branches were investigated. Skeletons of live colonies in acidic pH site after 45 days of exposure were less corroded than those of dead colonies, suggesting that the organic tissues enveloping the skeleton play a protective role. Colonies remained alive at the below-normal and acidic pH sites during the 45-day experiment but corrosion was very striking after 128 days, with colonies from the acidic site showing significant loss of skeleton. Compared to the control, these colonies also had lower levels of Mg (mean 8 versus 9.5 wt% Mg) within their skeletons. Electron microprobe mapping showed Mg to be higher in the outer layers of the skeletal walls in colonies from the normal pH site. Corrosion of outer layers of the walls probably explains the lower Mg level found in colonies exposed to acidic conditions. As solubility of calcite increases with Mg content, the enrichment of Mg in outer layers of the skeleton should enhance the vulnerability of Myriapora truncata to dissolution. These findings raise concerns over the survival of bryozoans with Mg calcite skeletons in the face of predicted decreases in oceanic pH levels.

Effects of pH on asexual reproduction and statolith formation of the scyphozoan, Aurelia labiata

Although anthropogenic influences such as global warming, overfishing, and eutrophication may contribute to jellyfish blooms, little is known about the effects of ocean acidification on jellyfish. Most medusae form statoliths of calcium sulfate hemihydrate that are components of their balance organs (statocysts). This study was designed to test the effects of pH (7.9, within the average current range, 7.5, expected by 2100, and 7.2, expected by 2300) combined with two temperatures (9 and 15°C) on asexual reproduction and statolith formation of the moon jellyfish, Aurelia labiata. Polyp survival was 100% after 122 d in seawater in all six temperature and pH combinations. Because few polyps at 9°C strobilated, and temperature effects on budding were consistent with published results, we did not analyze data from those three treatments further. At 15°C, there were no significant effects of pH on the numbers of ephyrae or buds produced per polyp or on the numbers of statoliths per statocyst; however, statolith size was significantly smaller in ephyrae released from polyps reared at low pH. Our results indicate that A. labiata polyps are quite tolerant of low pH, surviving and reproducing asexually even at the lowest tested pH; however, the effects of small statoliths on ephyra fitness are unknown. Future research on the behavior of ephyrae with small statoliths would further our understanding of how ocean acidification may affect jellyfish survival in nature.

The subtle effects of sea water acidification on the amphipod Gammarus locusta

We report an investigation of the effects of increases in pCO2 on the survival, growth and molecular physiology of the neritic amphipod Gammarus locusta which has a cosmopolitan distribution in estuaries. Amphipods were reared from juvenile to mature adult in laboratory microcosms at three different levels of pH in nominal range 8.1–7.6. Growth rate was estimated from weekly measures of body length. At sexual maturity the amphipods were sacrificed and assayed for changes in the expression of genes coding for a heat shock protein (hsp70 gene) and the metabolic enzyme glyceraldehyde-3-phosphate dehydrogenase (gapdh gene). The data show that the growth and survival of this species is not significantly impacted by a decrease in sea water pH of up to 0.5 units. Quantitative real-time PCR analysis indicated that there was no significant effect of growth in acidified sea water on the sustained expression of the hsp70 gene. There was a consistent and significant increase in the expression of the gapdh gene at a pH of ~7.5 which, when combined with observations from other workers, suggests that metabolic changes may occur in response to acidification. It is concluded that sensitive assays of tissue physiology and molecular biology should be routinely employed in future studies of the impacts of sea water acidification as subtle effects on the physiology and metabolism of coastal marine species may be overlooked in conventional gross “end-point” studies of organism growth or mortality.

Death by dissolution: Sediment saturation state as a mortality factor for juvenile bivalves

We show that death by dissolution is an important size-dependent mortality factor for juvenile bivalves. Utilizing a new experimental design, we were able to replicate saturation states in sediments after values frequently encountered by Mercenaria mercenaria in coastal deposits (Waragonite = 0.4 and 0.6). When 0.2-mm M. mercenaria were reared in sediments at Waragonite = 0.4 and 0.6, significant daily losses of living individuals occurred (14.0% and 14.4% d-1, respectively), relative to supersaturated-control sediments (3.9% d-1). For 0.4- mm M. mercenaria, significant mortality occurred under the most undersaturated conditions (Waragonite = 0.4, mortality = 9.6% d-1), although mortality at Waragonite = 0.6 was not significant (mortality= 2.7% d-1; control-saturated mortality = 0.2% d-1). For the largest size-class investigated, 0.6 mm, we show significant mortality for clams under the most undersaturated sediments (Waragonite = 0.4, 2.8% d-1). To test if buffered sediments would increase survivorship of juvenile bivalves during periods of recruitment, we manually manipulated sediment saturation state by adding crushed Mya arenaria shell to a mud flat in West Bath, Maine, U.S.A. Although we increased the average sediment saturation state within retrieved cores from W = 0.25 ± 0.01 to only 0.53 ± 0.06, numbers of live M. arenaria in buffered sediment increased almost three-fold in 2 weeks. Buffering muds against the metabolic acids that cause lowered saturation states may represent a potentially important management strategy to decrease dissolution mortality.