Effects of ocean warming and acidification on survival, growth and skeletal development in the early benthic juvenile sea urchin (Heliocidaris erythrogramma)

Co-occurring ocean warming, acidification and reduced carbonate mineral saturation have significant impacts on marine biota, especially calcifying organisms. The effects of these stressors on development and calcification in newly metamorphosed juveniles (ca. 0.5 mm test diam) of the intertidal sea urchin Heliocidaris erythrogramma, an ecologically important species in temperate Australia, were investigated in context with present and projected future conditions. Habitat temperature and pH/pCO₂ were documented to place experiments in a biologically and ecologically relevant context. These parameters fluctuated diurnally up to 10°C and 0.45 pH units. The juveniles were exposed to three temperature (21°C, 23°C, 25°C) and four pH (8.1, 7.8, 7.6, 7.4) treatments in all combinations, representing ambient sea surface conditions (21°C, pH 8.1; pCO₂ 397; Ω_Ca 4.7; Ω_Ar 3.1), near-future projected change (+2-4°C, -0.3-0.5 pH units; pCO₂ 400-1820; Ω_Ca 5.0-1.6; Ω_Ar 3.3-1.1), and extreme conditions experienced at low tide (+4°C, -0.3-07 pH units; pCO₂ 2850-2967; Ω_Ca 1.1-1.0; Ω_Ar 0.7-0.6). The lowest pH treatment (pH 7.4) was used to assess tolerance levels. Juvenile survival and test growth were resilient to current and near-future warming and acidification. Spine development, however, was negatively effected by near-future increased temperature (+2-4°C) and extreme acidification (pH 7.4), with a complex interaction between stressors. Near-future warming was the more significant stressor. Spine tips were dissolved in the pH 7.4 treatments. Adaptation to fluctuating temperature-pH conditions in the intertidal may convey resilience to juvenile H. erythrogramma to changing ocean conditions, however, ocean warming and acidification may shift baseline intertidal temperature and pH/pCO₂ to levels that exceed tolerance limits.

Food availability and pCO2 impacts on planulation, juvenile survival, and calcification of the azooxanthellate scleractinian coral, Balanophyllia elegans

Ocean acidification, the assimilation of atmospheric CO₂ by the oceans that decreases the pH and CaCO₃ saturation state (Ω) of seawater, is projected to have severe consequences for calcifying organisms. Strong evidence suggests that tropical reef-building corals containing algal symbionts (zooxanthellae) will experience dramatic declines in calcification over the next century. The responses of azooxanthellate corals to ocean acidification are less well understood, and because they cannot obtain extra photosynthetic energy from symbionts, they provide a system for studying the direct effects of acidification on the energy available for calcification. The orange cup coral Balanophyllia elegans is a solitary, azooxanthellate scleractinian species common on the California coast where it thrives in the low pH waters of an upwelling regime. During an 8 month study, we addressed the effects of three pCO₂ treatments (410, 770, and 1230 μatm) and two feeding frequencies (High Food and Low Food) on adult Balanophyllia elegans planulation (larval release) rates, and on the survival, growth, and calcification of their juvenile offspring. Planulation rates were affected by food level but not pCO₂, while juvenile survival was highest under 410 μatm and High Food conditions. Our results suggest that feeding rate has a greater impact on calcification of B. elegans than pCO₂. Net calcification was positive even at 1230 μatm (~ 3 times current atmospheric pCO₂), although the increase from 410 to 1230 μatm reduced overall calcification by ~ 25–45%, and reduced skeletal density by ~ 35–45%. Higher pCO₂ also altered aragonite crystal morphology significantly. We discuss how feeding frequency affects azooxanthellate coral calcification, and how B. elegans may respond to ocean acidification in coastal upwelling waters.

Potential acidification impacts on zooplankton in CCS leakage scenarios

Carbon capture and storage (CCS) technologies involve localized acidification of significant volumes of seawater, inhabited mainly by planktonic species. Knowledge on potential impacts of these techniques on the survival and physiology of zooplankton, and subsequent consequences for ecosystem health in targeted areas, is scarce. The recent literature has a focus on anthropogenic greenhouse gas emissions into the atmosphere, leading to enhanced absorption of CO₂ by the oceans and a lowered seawater pH, termed ocean acidification. These studies explore the effects of changes in seawater chemistry, as predicted by climate models for the end of this century, on marine biota. Early studies have used unrealistically severe CO₂/pH values in this context, but are relevant for CCS leakage scenarios. Little studied meso- and bathypelagic species of the deep sea may be especially vulnerable, as well as vertically migrating zooplankton, which require significant residence times at great depths as part of their life cycle.

Interactive effects of ocean acidification and warming on sediment-dwelling marine calcifiers

The increase in human activities, such as the burning of fossil fuels, has elevated the concentration of atmospheric carbon dioxide and warmed the planet through the greenhouse effect. In addition, approximately 30% of the CO2 produced by human activities has dissolved into the oceans, lowering pH and reducing the abundance, and hence the availability, of carbonate ions (CO3 2-), which are essential for calcium carbonate deposition. Of great concern is the impact to photosynthetic marine calcifiers, elevated CO2 and temperature is expected to have a negative impact on the health and survivorship of calcifying marine organisms. This thesis explores the effects of elevated CO2 and temperature on the microenvironment, photosynthetic efficiency, calcification and biomechanical properties in important sediment producers on coral reefs. The reef-building and sedimentdwelling organisms, Halimeda and symbiont-bearing foraminifera are prominent, coexisting taxa in shallow coral reefs and play a vital role in tropical and subtropical ecosystems as producers of sediment and habitats and food sources for other marine organisms. However, there is limited evidence of the effects of ocean warming and acidification in these two keystone species. Irradiance alone was not found to influence photosynthetic efficiency, photoprotective mechanisms and calcification in Halimeda macroloba, Halimeda cylindracea and Halimeda opuntia (Chapter 2). There is also limited knowledge of foraminiferal biology on coral reefs, especially the symbiotic relationship between the protest host and algal symbionts. Marginopora vertebralis, the dominant tropical foraminifera, shows phototactic behavior, which is a unique mechanism for ensuring symbionts experience an ideal light environment. The diurnal photosynthetic responses of in hospite symbiont photosynthesis was linked to host movement and aided in preventing photoinhibition and bleaching by moving away from over-saturating irradiance, to more optimal light fields (Chapter 3). With this greater understanding of Halimeda and foraminiferan biology and photosynthesis, the impacts of ocean warming and acidification on photosynthesis and calcification were then tested (Chapter 4, 5 and 6). Impacts of ocean acidification and warming were investigated through exposure to a combination of four temperature (28, 30, 32, 34°C) and four pCO2 levels (380, 600, 1000, 2000 µatm; equivalent to future climate change scenarios for the current and the years 2065, 2100 and 2200 and simulating the IPCC A1F1 predictions) (Chapter 4). Elevated CO2 and temperature caused a decline in photosynthetic efficiency (FV/FM), calcification and growth in all species. After five weeks at 34°C under all CO2 levels, all species died. The elevated CO2 and temperature greatly affect the CaCO3 crystal formation with reductions in density and width. M. vertebralis experienced the greatest inhibition to crystal formation, suggesting that this high Mg-calcite depositing species is more sensitive to lower pH and higher temperature than aragonite-forming Halimeda species. Exposure to elevated temperature alone or reduced pH alone decreased photosynthesis and calcification in these species. However, there was a strong synergistic effect of elevated temperature and reduced pH, with dramatic reductions in photosynthesis and calcification in all three species. This study suggested that the elevated temperature of 32°C and the pCO2 concentration of 1000 µatm are the upper limit for survival of these species art our site of collection (Heron Island on the Great Barrier Reef, Australia). Microsensors enabled the detection of O2 surrounding specimens at high spatial and temporal resolutions and revealed a 70-80% in decrease in O2 production under elevated CO2 and temperature (1200 µatm 32°C) in Halimeda (Chapter 5) and foraminifera (Chapter 6). The results from O2 microprofiles support the photosynthetic pigment and chlorophyll fluorescence data, showing decreasing O2 production with declining chlorophyll a and b concentrations and a decrease in photosynthetic efficiency under ocean acidification and/or temperature stress. This revealed that photosynthesis and calcification are closely coupled with reductions in photosynthetic efficiency leading to reductions in calcification. Reductions in carbonate availability reduced calcification and that can lead to weakened calcified structures. Elevations in water temperature is expected to augment this weakening, resulting in decreased mechanical integrity and increased susceptibility to storm- and herbivory-induced mortality in Halimeda sp. The morphological and biomechanical properties in H. macroloba and H. cylindracea at different wave exposures were then investigated in their natural reef habitats (Chapter 7). The results showed that both species have morphological (e.g. blade surface area, holdfast volume) and biomechanical (e.g. force required to uproot, force required to break thalli) adaptations to different levels of hydrodynamic exposure. The mechanical integrity and skeletal mineralogy of Halimeda was then investigated in response to future climate change scenarios (Chapter 7). The biomechanical properties (shear strength and punch strength) significantly declined in the more heavily calcified H. cylindracea at 32ºC and 1000 µatm, whereas were variable in less heavily calcified H. macroloba, indicating different responses between Halimeda species. An increase in less-soluble low Mgcalcite was observed under elevated CO2 conditions. Significant changes in Mg:Ca and Sr:Ca ratios under elevated CO2 and temperature conditions suggested that calcification was affected at the ionic level. It is concluded that Halimeda is biomechanically sensitive to elevated temperature and more acidic oceans and may lead to increasing susceptibility to herbivory and higher risk of thallus breakage or removal from the substrate. Experimental results throughout the thesis revealed that ocean acidification and warming have negative impacts on photosynthetic efficiency, productivity, calcification and mechanical integrity, which is likely to lead to increased mortality in these species under a changing climate. A loss of these calcifying keystone species will have a dramatic impact on carbonate accumulation, sediment turnover, and coral reef community and habitat structure.

Early exposure of bay scallops (Argopecten irradians) to high CO2 causes a decrease in larval shell growth

Ocean acidification, characterized by elevated pCO₂ and the associated decreases in seawater pH and calcium carbonate saturation state (Ω), has a variable impact on the growth and survival of marine invertebrates. Larval stages are thought to be particularly vulnerable to environmental stressors, and negative impacts of ocean acidification have been seen on fertilization as well as on embryonic, larval, and juvenile development and growth of bivalve molluscs. We investigated the effects of high CO₂ exposure (resulting in pH = 7.39, Ω_ar = 0.74) on the larvae of the bay scallop Argopecten irradians from 12 h to 7 d old, including a switch from high CO₂ to ambient CO₂ conditions (pH = 7.93, Ω_ar = 2.26) after 3 d, to assess the possibility of persistent effects of early exposure. The survival of larvae in the high CO₂ treatment was consistently lower than the survival of larvae in ambient conditions, and was already significantly lower at 1 d. Likewise, the shell length of larvae in the high CO₂ treatment was significantly smaller than larvae in the ambient conditions throughout the experiment and by 7 d, was reduced by 11.5%. This study also demonstrates that the size effects of short-term exposure to high CO₂ are still detectable after 7 d of larval development; the shells of larvae exposed to high CO₂ for the first 3 d of development and subsequently exposed to ambient CO₂ were not significantly different in size at 3 and 7 d than the shells of larvae exposed to high CO₂ throughout the experiment.

Effects of seawater temperature and pH on the boring rates of the sponge Cliona celata in scallop shells

Warmer, more acidic water resulting from greenhouse gas emissions could influence ecosystem processes like bioerosion of calcifying organisms. Based on summer-maxima values (temperature = 26 °C; pH = 8.1) at a collection site in New York (40°56″ N, 72°30″ W), explants of the boring sponge Cliona celata Grant, 1826 were grown for 133 days on scallop shells in seawater ranging from current values to one scenario predicted for the year 2100 (T = 31 °C; pH = 7.8). High water temperature had little effect on sponge growth, survival, or boring rates. Lower pH slightly reduced sponge survival, while greatly influencing shell boring. At pH = 7.8, sponges bored twice the number of papillar holes and removed two times more shell weight than at pH = 8.1. Greater erosion resulted in weaker scallop shells. This study suggests that lower seawater pH may increase boring rates of C. celata in shellfish, with potentially severe implications for wild and farmed shellfish populations.

Predicting the response of molluscs to the impact of ocean acidification

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.

Effects of ocean acidification on juvenile red king crab (Paralithodes camtschaticus) and tanner crab (Chionoecetes bairdi) growth, condition, calcification, and survival

Ocean acidification, a decrease in the pH in marine waters associated with rising atmospheric CO₂ levels, is a serious threat to marine ecosystems. In this paper, we determine the effects of long-term exposure to near-future levels of ocean acidification on the growth, condition, calcification, and survival of juvenile red king crabs, Paralithodes camtschaticus, and Tanner crabs, Chionoecetes bairdi. Juveniles were reared in individual containers for nearly 200 days in flowing control (pH 8.0), pH 7.8, and pH 7.5 seawater at ambient temperatures (range 4.4–11.9 °C). In both species, survival decreased with pH, with 100% mortality of red king crabs occurring after 95 days in pH 7.5 water. Though the morphology of neither species was affected by acidification, both species grew slower in acidified water. At the end of the experiment, calcium concentration was measured in each crab and the dry mass and condition index of each crab were determined. Ocean acidification did not affect the calcium content of red king crab but did decrease the condition index, while it had the opposite effect on Tanner crabs, decreasing calcium content but leaving the condition index unchanged. This suggests that red king crab may be able to maintain calcification rates, but at a high energetic cost. The decrease in survival and growth of each species is likely to have a serious negative effect on their populations in the absence of evolutionary adaptation or acclimatization over the coming decades.

Short- and long-term consequences of larval stage exposure to constantly and ephemerally elevated carbon dioxide for marine bivalve populations (update)

While larval bivalves are highly sensitive to ocean acidification, the basis for this sensitivity and the longer-term implications of this sensitivity are unclear. Experiments were performed to assess the short-term (days) and long-term (months) consequences of larval stage exposure to varying CO₂ concentrations for calcifying bivalves. Higher CO₂ concentrations depressed both calcification rates assessed using ⁴⁵Ca uptake and RNA : DNA ratios in Mercenaria mercenaria and Argopecten irradians larvae with RNA : DNA ratios being highly correlated with larval growth rates (r²>0.9). These findings suggested that high CO₂ has a cascading negative physiological impact on bivalve larvae stemming in part from lower calcification rates. Exposure to elevated CO₂ during the first four days of larval development significantly depressed A. irradians larval survival rates, while a 10-day exposure later in larval development did not, demonstrating the extreme CO₂ sensitivity of bivalve larvae during first days of development. Short- (weeks) and long-term (10 month) experiments revealed that individuals surviving exposure to high CO₂ during larval development grew faster when exposed to normal CO₂ as juveniles compared to individuals reared under ambient CO₂ as larvae. These increased growth rates could not, however, overcome size differences established during larval development, as size deficits of individuals exposed to even moderate levels of CO₂ as larvae were evident even after 10 months of growth under normal CO₂ concentrations. This “legacy effect” emphasizes the central role larval stage CO₂ exposure can play in shaping the success of modern-day bivalve populations.

Environmental salinity modulates the effects of elevated CO2 levels on juvenile hard shell clams, Mercenaria mercenaria

Ocean acidification due to increasing atmospheric CO₂ concentrations results in a decrease in seawater pH and shifts in the carbonate chemistry that can negatively affect marine organisms. Marine bivalves such as the hard shell clams Mercenaria mercenaria serve as ecosystem engineers in estuaries and coastal zones of the western Atlantic and, as for many marine calcifiers, are sensitive to the impacts of ocean acidification. In estuaries, the effects of ocean acidification can be exacerbated by low buffering capacity of brackish waters, acidic inputs from freshwaters and land, and/or the negative effects of salinity on organisms’ physiology. We determined the interactive effects of 21 weeks of exposure to different levels of CO₂ (~395, 800 and 1500 µatm corresponding to pH of 8.2, 8.1 and 7.7 respectively) and salinity (32 vs. 16) on biomineralization, shell properties and energy metabolism of juveniles of the hard shell clam M. mercenaria. Low salinity had profound effects on survival, energy metabolism and biomineralization of hard shell clams and modulated their responses to elevated P_CO2. Negative effects of low salinity in juvenile clams were mostly due to the strongly elevated basal energy demand indicating energy deficiency that led to reduced growth, elevated mortality and impaired shell maintenance (evidenced by the extensive damage to the periostracum). The effects of elevated P_CO2 on physiology and biomineralization of hard shell clams were more complex. Elevated P_CO2 (~800-1500 µatm) had no significant effects on standard metabolic rates (indicative of the basal energy demand), but affected growth and shell mechanical properties in juvenile clams. Moderate hypercapnia (~800 µatm P_CO2) increased shell and tissue growth and reduced mortality of juvenile clams in high salinity exposures; however, these effects were abolished under the low salinity conditions or at high P_CO2 (~1500 µatm). Mechanical properties of the shell (measured as microhardness and fracture toughness of the shells) were negatively affected by elevated CO₂ alone or in combination with low salinity, which may have important implications for protection against predators or environmental stressors. Our data indicate that environmental salinity can strongly modulate responses to ocean acidification in hard shell clams and thus should be taken into account when predicting the effects of ocean acidification on estuarine bivalves.