Fertilization success of an arctic sea urchin species, Strongylocentrotus droebachiensis (O. F. Müller, 1776) under CO2-induced ocean acidification

Sea urchins as broadcasting spawners, release their gametes into open water for fertilization, thus being particularly vulnerable to ocean acidification. In this study, we assessed the effects of different pH scenarios on fertilization success of Strongylocentrotus droebachiensis, collected at Spitsbergen, Arctic. We achieved acidification by bubbling CO₂ into filtered seawater using partial pressures (pCO₂) of 180, 380, 980, 1400 and 3000 μatm}. Untreated filtered seawater was used as control. We recorded fertilization rates and diagnosed morphological aberrations after post-fertilization periods of 1 h and 3 h under different exposure conditions in experiments with and without pre-incubation of the eggs prior to fertilization. In parallel, we conducted measurements of intracellular pH changes using BCECF/AM in unfertilized eggs exposed to a range of acidified seawater. We observed increasing rates of polyspermy in relation to higher seawater pCO₂, which might be due to failures in the formation of the fertilization envelope. In addition, our experiments showed anomalies in fertilized eggs: incomplete lifting-off of the fertilization envelope and blebs of the hyaline layer. Other drastic malformations consisted of constriction, extrusion, vacuolization or degeneration (observed as a gradient from the cortex to the central region of the cell) of the egg cytoplasm, and irregular cell divisions until 2- to 4-cell stages. The intracellular pH (pH_i) decreased significantly from 1400 μatm on. All results indicate a decreasing fertilization success at CO₂ concentrations from 1400 μatm upwards. Exposure time to low pH might be a threatening factor for the cellular buffer capacity, viability, and development after fertilization.

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.

Impact of ocean acidification on metabolism and energetics during early life stages of the intertidal porcelain crab Petrolisthes cinctipes

Absorption of elevated atmospheric CO₂ is causing surface ocean pH to decline, a process known as ocean acidification (OA). To date, few studies have assessed the physiological impacts of OA on early life-history stages of intertidal organisms, which transition from habitats with fluctuating pH (intertidal zone) to relatively stable (pelagic zone) pH environments. We used the intertidal crab Petrolisthes cinctipes to determine whether metabolic responses to year 2300 predictions for OA vary among early developmental stages and to examine whether the effects were more pronounced in larval stages developing in the open ocean. Oxygen consumption rate, total protein, dry mass, total lipids and C/N were determined in late-stage embryos, zoea I larvae and newly settled juveniles reared in ambient pH (7.93±0.06) or low pH (7.58±0.06). After short-term exposure to low pH, embryos displayed 11% and 6% lower metabolism and dry mass, respectively, which may have an associated bioenergetic cost of delayed development to hatching. However, metabolic responses appeared to vary among broods, suggesting significant parental effects among the offspring of six females, possibly a consequence of maternal state during egg deposition and genetic differences among broods. Larval and juvenile metabolism were not affected by acute exposure to elevated CO₂. Larvae contained 7% less nitrogen and C/N was 6% higher in individuals reared at pH 7.58 for 6 days, representing a possible switch from lipid to protein metabolism under low pH; the metabolic switch appears to fully cover the energetic cost of responding to elevated CO₂. Juvenile dry mass was unaffected after 33 days exposure to low pH seawater. Increased tolerance to low pH in zoea I larvae and juvenile stages may be a consequence of enhanced acid–base regulatory mechanisms, allowing greater compensation of extracellular pH changes and thus preventing decreases in metabolism after exposure to elevated P_CO2. The observed variation in responses of P. cinctipes to decreased pH in the present study suggests the potential for this species to adapt to future declines in near-shore pH.

Effects of ocean acidification on early life-history stages of the intertidal porcelain crab Petrolisthes cinctipes

Intertidal zone organisms naturally experience daily fluctuations in pH, presently reaching values beyond what is predicted for open ocean surface waters from ocean acidification (OA) by the year 2100, and thus present an opportunity to study the pH sensitivity of organisms that are presumably adapted to an acidified environment. The intertidal zone porcelain crab, Petrolisthes cinctipes, was used to study physiological responses to low pH in embryonic, larval and newly recruited juvenile life-history stages. In these crabs, embryonic development occurs in the pH-variable intertidal zone (pH 6.9–9.5), larvae mature in the more stable pelagic environment (pH 7.9–8.2), and juvenile crabs settle back into the pH-variable intertidal zone. We examined survival, cardiac performance, energetics and morphology in embryonic, larval and juvenile crabs exposed to two pH conditions (pH 7.9 and 7.6). Embryos and larvae were split by brood between the pH treatments for 9 days to examine brood-specific responses to low pH. Hatching success did not differ between pH conditions, but ranged from 30% to 95% among broods. Larval survival was not affected by acidification, but juvenile survival was reduced by ~30% after longer (40 days) exposure to low pH. Embryonic and larval heart rates were 37% and 20% lower at low pH, and there was a brood-specific response in embryos. Embryos did not increase in volume under acidified conditions, compared with a 15% increase in ambient conditions. We conclude that sustained exposure to low pH could be detrimental to P. cinctipes embryos and larvae despite the fact that embryos are regularly exposed to naturally fluctuating hypercapnic water in the intertidal zone. Importantly, our results indicate that early life-history stage responses to OA may be brood specific through as yet undetermined mechanisms.

Growth and development of larval bay scallops (Argopecten irradians) in response to early exposure to high CO2

Coastal and estuarine environments experience large variability and rapid shifts in pCO2 levels. Elevated pCO2, or ocean acidification, often negatively affects early life stages of calcifying marine invertebrates, including bivalves, but it is unclear which developmental stage is most sensitive. I hypothesized that initial calcification is a critical stage during which high pCO2 exposure has severe effects on larval growth and development of bay scallop (Argopecten irradians). Using five experiments varying the timing of exposure of embryonic and larval bay scallops to high CO2, this thesis identifies two distinct stages of development during which exposure to high CO2/low pH causes different effects on bay scallop larvae. I show that any exposure to high CO2 consistently reduces survival of bay scallop larvae. I also show that high CO2 exposure during initial calcification (12-24 h post-fertilization) results in significantly smaller shells, relative to ambient conditions, and this size decrease persists through the first week of development. High CO2 exposure at 2-12 h post-­ fertilization (pre-calcification), does not impact shell size, suggesting that the CO2 impact on size is a consequence of water chemistry during calcification. However, high CO2 exposure prior to shell formation (2-12 h post-fertilization) causes a high incidence of larval shell deformity, regardless of CO2 conditions during initial calcification. This impact does not occur in response to high CO2 exposure after the 2-12 h period. The observations of two critical stages in early development has implications for both field and hatchery populations. If field populations were able to time their spawning to occur during the night, larvae would undergo initial calcification during the daytime, when CO2 conditions are more favorable, resulting in larger veliger larvae. Hatcheries could invest minimal resources to monitor and modify water chemistry only during the first day of development to ensure larva are exposed to favorable conditions during that critical period.

Sex in murky waters : anthropogenic disturbance of sexual selection in pipefish

Animals experience variation in their environment because of natural changes. However, due to anthropogenic disturbance, the speed and severity of these changes have recently increased. This thesis investigates how reproductive behaviours may be affected by human induced environmental change. In specific, I investigate how visual and chemical changes in the aquatic environment, caused by eutrophication, affect mating systems and sexual selection in fish. Broad-nosed- and straight-nosed pipefish, which both have been studied in detail for a long period, were used as model organisms. These two species are particularly suitable model organisms since they perform complex courtship behaviours, including the advertisement of ornaments and a nuptial dance. Further, two distinct populations were studied, one on the Swedish west coast and one in the Baltic Sea, as these two locations vary in the degree and extent of environmental disturbance, in particular turbidity. I found that changes in the visual environment had no impact on the development of female sexual ornaments in these sex-role reversed pipefishes, but it hampered adaptive mate choice. Turbidity also had a negative effect on reproductive success in the Baltic Sea population. Changes in the chemical environment in the form of increased pH reduced the probability to mate, while hypoxia did not alter mating propensity. However, hypoxic water delayed the onset of both courting and mating. Hence, human induced change in aquatic environments may alter the processes of sexual selection and population dynamics.

The influence of food supply on the response of Olympia oyster larvae to ocean acidification

Increases in atmospheric carbon dioxide drive accompanying changes in the marine carbonate system as carbon dioxide (CO₂) enters seawater and alters its pH (termed “ocean acidification”). However, such changes do not occur in isolation, and other environmental factors have the potential to modulate the consequences of altered ocean chemistry. Given that physiological mechanisms used by organisms to confront acidification can be energetically costly, we explored the potential for food supply to influence the response of Olympia oyster (Ostrea lurida) larvae to ocean acidification. In laboratory experiments, we reared oyster larvae under a factorial combination of pCO₂ and food level. High food availability offset the negative consequences of elevated pCO₂ on larval shell growth and total dry weight. Low food availability, in contrast, exacerbated these impacts. In both cases, effects of food and pCO₂ interacted additively rather than synergistically, indicating that they operated independently. Despite the potential for abundant resources to counteract the consequences of ocean acidification, impacts were never completely negated, suggesting that even under conditions of enhanced primary production and elevated food availability, impacts of ocean acidification may still accrue in some consumers.

Metabolic costs of larval settlement and metamorphosis in the coral Seriatopora caliendrum under ambient and elevated pCO2

We tested the effects of pCO₂ on Seriatopora caliendrum recruits over the first 5.3 d of post-settlement existence. In March 2011, 11–20 larvae were settled in glass vials (3.2 mL) and incubated at 24.0 °C and ~ 250 μmol quanta m^− 2 s^− 1 while supplied with seawater (at 1.4 mL s^− 1) equilibrated with 51.6 Pa pCO₂ (ambient) or 86.4 Pa pCO₂. At 51.6 Pa pCO₂, mean respiration 7 h post-settlement was 0.056 ± 0.007 nmol O₂ recruit^− 1 min^− 1, but rose quickly to 0.095 ± 0.007 nmol O₂ recruit^− 1 min^− 1 at 3.3 d post-settlement, and thereafter declined to 0.075 ± 0.002 nmol O₂ recruit^− 1 min^− 1 at 5.3 d post-settlement (all ± SE). Elevated pCO₂ depressed respiration of recruits by 19% after 3.3 d and 12% overall (i.e., integrated over 5.3 d), and while it had no effect on corallite area, elevated pCO₂ was associated with weaker adhesion to the glass settlement surface and lower protein biomass. The unique costs of settlement and metamorphosis for S. caliendrum over 5.3 d are estimated to be 257 mJ recruit^− 1 at 51.6 Pa pCO₂, which is less than the energy content of the larvae and recruits.

Meta-analysis reveals complex marine biological responses to the interactive effects of ocean acidification and warming

Ocean acidification and warming are considered two of the greatest threats to marine biodiversity, yet the combined effect of these stressors on marine organisms remains largely unclear. Using a meta-analytical approach, we assessed the biological responses of marine organisms to the effects of ocean acidification and warming in isolation and combination. As expected biological responses varied across taxonomic groups, life-history stages, and trophic levels, but importantly, combining stressors generally exhibited a stronger biological (either positive or negative) effect. Using a subset of orthogonal studies, we show that four of five of the biological responses measured (calcification, photosynthesis, reproduction, and survival, but not growth) interacted synergistically when warming and acidification were combined. The observed synergisms between interacting stressors suggest that care must be made in making inferences from single-stressor studies. Our findings clearly have implications for the development of adaptive management strategies particularly given that the frequency of stressors interacting in marine systems will be likely to intensify in the future. There is now an urgent need to move toward more robust, holistic, and ecologically realistic climate change experiments that incorporate interactions. Without them accurate predictions about the likely deleterious impacts to marine biodiversity and ecosystem functioning over the next century will not be possible.