Impacts of ocean warming and acidification on the larval development of the barnacle Amphibalanus improvisus

The world’s oceans are warming and becoming more acidic. Both stressors, singly or in combination, impact marine species, and ensuing effects might be particularly serious for early life stages. To date most studies have focused on ocean acidification (OA) effects in fully marine environments, while little attention has been devoted to more variable coastal ecosystems, such as the Western Baltic Sea. Since natural spatial and temporal variability of environmental conditions such as salinity, temperature or pCO₂ impose more complex stresses upon organisms inhabiting these habitats, species can be expected to be more tolerant to OA (or warming) than fully marine taxa. We present data on the variability of salinity, temperature and pH within the Kiel Fjord and on the responses of the barnacle Amphibalanus improvisus from this habitat to simulated warming and OA during its early development. Nauplii and cyprids were exposed to different temperature (12, 20 and 27 °C) and pCO₂ (nominally 400, 1250 and 3250 μatm) treatments for 8 and 4 weeks, respectively. Survival, larval duration and settlement success were monitored. Warming affected larval responses more strongly than OA. Increased temperatures favored survival and development of nauplii but decreased survival of cyprids. OA had no effect upon survival of nauplii but enhanced their development at low (12 °C) and high (27 °C) temperatures. In contrast, at the intermediate temperature (20 °C), nauplii were not affected even by 3250 μatm pCO₂. None of the treatments significantly affected settlement success of cyprids. These experiments show a remarkable tolerance of A. improvisus larvae to 1250 μatm pCO₂, the level of OA predicted for the end of the century.

Ocean acidification-induced food quality deterioration constrains trophic transfer

Our present understanding of ocean acidification (OA) impacts on marine organisms caused by rapidly rising atmospheric carbon dioxide (CO2) concentration is almost entirely limited to single species responses. OA consequences for food web interactions are, however, still unknown. Indirect OA effects can be expected for consumers by changing the nutritional quality of their prey. We used a laboratory experiment to test potential OA effects on algal fatty acid (FA) composition and resulting copepod growth. We show that elevated CO2 significantly changed the FA concentration and composition of the diatom Thalassiosira pseudonana, which constrained growth and reproduction of the copepod Acartia tonsa. A significant decline in both total FAs (28.1 to 17.4 fg cell−1) and the ratio of long-chain polyunsaturated to saturated fatty acids (PUFA:SFA) of food algae cultured under elevated (750 µatm) compared to present day (380 µatm) pCO2 was directly translated to copepods. The proportion of total essential FAs declined almost tenfold in copepods and the contribution of saturated fatty acids (SFAs) tripled at high CO2. This rapid and reversible CO2-dependent shift in FA concentration and composition caused a decrease in both copepod somatic growth and egg production from 34 to 5 eggs female−1 day−1. Because the diatom-copepod link supports some of the most productive ecosystems in the world, our study demonstrates that OA can have far-reaching consequences for ocean food webs by changing the nutritional quality of essential macromolecules in primary producers that cascade up the food web.

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.

The Pacific oyster, Crassostrea gigas, shows negative correlation to naturally elevated carbon dioxide levels: implications for near-term ocean acidification effects

We report results from an oyster hatchery on the Oregon coast, where intake waters experienced variable carbonate chemistry (aragonite saturation state < 0.8 to > 3.2; pH < 7.6 to > 8.2) in the early summer of 2009. Both larval production and midstage growth (∼ 120 to ∼ 150 µm) of the oyster Crassostrea gigas were significantly negatively correlated with the aragonite saturation state of waters in which larval oysters were spawned and reared for the first 48 h of life. The effects of the initial spawning conditions did not have a significant effect on early-stage growth (growth from D-hinge stage to ∼ 120 µm), suggesting a delayed effect of water chemistry on larval development.

Effects of pH and temperature on fertilization and early development in the sea urchin, Lytechinus pictus

Increasingly high levels of anthropogenic CO2 are quickly dissolving into the ocean and altering its chemistry. The Intergovernmental Panel on Climate Change (IPCC) estimates for near-future temperature and pH levels in our oceans are of great concern. Current research has focused on assessing how organisms will respond to the acidification and warming temperatures. Some marine invertebrates that spawn their gametes into the ocean have shown vulnerability to these changes resulting in decreased fertilization success. This paper examines the effects of these variables on fertilization success and early development of the sea urchin, Lytechinus pictus. Spawning was induced under multiple combinations of temperatures and pCO2. Fertilization success was determined by the proportion of eggs that showed successful early development. While later development of L. pictus has been previously investigated, this is the first study to investigate their fertilization success with increased ocean temperature and acidification. Fertilization success increased with rising temperatures although aberrant development also increased with temperature over time. If the expected future ocean conditions are capable of affecting early development, urchin populations may show a decline, potentially causing ecological problems.

Temperate and cold water sea urchin species in an acidifying world: coping with change?

Anthropogenic carbon dioxide (CO2) emissions are increasing the atmospheric CO2 concentration and the oceans are absorbing around 1/3 them. The CO2 hydrolysis increases the H+ concentration, decreasing the pH, while the proportions of the HCO3- and CO32- ions are also affected. This process already led to a decrease of 0.1 pH units in surface seawater. According to “business-as-usual” models, provided by the Intergovernmental Panel on Climate Change (IPCC), the pH is expected to decrease 0.3-0.5 units by 2100 and 0.7-0.8 by 2300. As a result the surface ocean carbonates chemistry will also change: with increasing pCO2, dissolved inorganic carbon will increase and the equilibrium of the carbonate system will shift to higher CO2 and HCO3– levels, while CO32– concentration will decrease. Surface seawaters will progressively become less saturated towards calcite and aragonite saturation state and some particular polar and cold water regions could even become completely undersaturated within the next 50 years.

Responses of marine organisms to environmental hypercapnia, i.e. to an excess of CO2 in the aquatic environment, can be extremely variable and the degree of sensitivity varies between species and life stages. Sea urchins are key stone species in many marine ecosystems. They are considered to be particularly vulnerable to ocean acidification effects not only due to the nature of their skeleton (magnesium calcite) whose solubility is similar or higher than that of aragonite, but also because they lack an efficient ion regulatory machinery, being therefore considered poor acid-base regulators. Populations from polar regions are expected to be at an even higher risk since the carbonate chemical changes in surface ocean waters are happening there at a faster rate.

The goal of this work was to study the effects of low seawater pH exposure of different life stages of sea urchins, in order to better understand how species from different environments and/or geographic origins would respond and if there would be scope for possible adaptation and/or acclimatization.

Forecasted CO2 modifies the influence of light in shaping subtidal habitat

Some abiotic conditions are well known to play disproportionately large roles in shaping contemporary assemblages, yet their roles may not continue to have similar magnitudes of effect into the future. We tested whether forecasted levels of CO2 could alter the strength of influence of an abiotic factor (i.e., light intensity) well known for its strength of influence on the subtidal ecology of photosynthetic organisms. We investigated these dynamics in two subtidal algal species that form contrasting associations with kelp forests, one negatively associated with kelp canopies (turf-forming brown algae, Feldmannia spp.) and the other positively associated with kelp as understory (calcifying red crustose algae, Lithophyllum sp.). Using an experimental approach, we assessed the independent and combined effects of [CO2] (control and elevated) and light (shade, low ultraviolet B [UVB], full light) on growth, recruitment, and relative electron transport rate (rETR). Under control [CO2], the effects of light corresponded to the relative light environments of the two groups of algae. The influence of light on the percentage cover and biomass of understory crusts was substantially reduced under elevated [CO2], which caused crusts to grow less. While elevated [CO2] had the opposite effect of positively influencing turf cover and biomass, it had the same effect of reducing the structuring effects of light and UVB. Hence, if we are to predict the ecological consequences of future CO2 conditions, the role of contemporary processes cannot be assumed to produce similar effects relative to other processes, which will change with a changing climate.

Unshelled abalone and corrupted urchins: development of marine calcifiers in a changing ocean

The most fragile skeletons produced by benthic marine calcifiers are those that larvae and juveniles make to support their bodies. Ocean warming, acidification, decreased carbonate saturation and their interactive effects are likely to impair skeletogenesis. Failure to produce skeleton in a changing ocean has negative implications for a diversity of marine species. We examined the interactive effects of warming and acidification on an abalone (Haliotis coccoradiata) and a sea urchin (Heliocidaris erythrogramma) reared from fertilization in temperature and pH/pCO2 treatments in a climatically and regionally relevant setting. Exposure of ectodermal (abalone) and mesodermal (echinoid) calcifying systems to warming (+2°C to 4°C) and acidification (pH 7.6–7.8) resulted in unshelled larvae and abnormal juveniles. Haliotis development was most sensitive with no interaction between stressors. For Heliocidaris, the percentage of normal juveniles decreased in response to both stressors, although a +2°C warming diminished the negative effect of low pH. The number of spines produced decreased with increasing acidification/pCO2, and the interactive effect between stressors indicated that a +2°C warming reduced the negative effects of low pH. At +4°C, the developmental thermal tolerance was breached. Our results show that projected near-future climate change will have deleterious effects on development with differences in vulnerability in the two species.

The response of two ecologically important Antarctic invertebrates (Sterechinus neumayeri and Parborlasia corrugatus) to reduced seawater pH: effects on fertilisation and embryonic development

Ocean acidification, or the lowering of seawater pH, is caused by sequestration of atmospheric CO2 into the oceans. This study investigated the effects of present-day pH 8.0, predicted ocean surface pH for the years 2100 and 2300 (pH 7.7 and pH 7.3, respectively) and an extreme pH (pH 7.0) on fertilisation and embryogenesis in the Antarctic nemertean worm Parborlasia corrugatus and sea urchin Sterechinus neumayeri. Fertilisation success was not affected by pH in P. corrugatus across a range of sperm concentrations. Fertilisation success in S. neumayeri declined significantly in pH 7.0 and 7.3 seawater, but only at a low sperm concentration. Seawater pH had no effect on the rate of egg cleavage in S. neumayeri, or the proportion of abnormal embryos 1-day post-fertilisation. P. corrugatus embryogenesis was also relatively robust to pH changes, with a significant effect detected only when the seawater pH was decreased to 7.0. While fertilisation and early cell division were relatively robust, later development through to the gastrula was sensitive to pH. In S. neumayeri, an effect of pH on development was evident by the gastrula stage, while there were significantly more abnormal P. corrugatus embryos in pH 7.0 up to the blastula stage, and in pH 7.0 and pH 7.3 at the coeloblastula stage. Our results are similar to the observations on other marine invertebrate species where fertilisation and early embryonic development are generally robust to lowered seawater pH, while the older coeloblastula and gastrula stages are more responsive. We also found no evidence to suggest that Antarctic species are more adversely affected by lower seawater pH compared with the findings for non-Antarctic counterparts. We conclude that in the two species we examined, near-future decreases in pH (decreases of ≈0.3–0.5 pH units) may not have a significant effect on fertilisation and early embryogenesis, while predicted longer term decreases (decreases of ≈0.7–0.77 pH units) could reduce fertilisation success in S. neumayeri if sperm concentrations are low and may increase abnormalities in P. corrugatus during later embryogenesis.

Elevated pCO2 increases sperm limitation and risk of polyspermy in the red sea urchin Strongylocentrotus franciscanus

Anthropogenic carbon dioxide (CO2) emissions and the resultant acidification of surface ocean waters are predicted to have far-reaching consequences for biological processes in the marine environment. For example, because changes in pH and pCO2 can alter sperm performance, ocean acidification may be accompanied by reductions in the success of fertilization in marine broadcast spawners. Several studies have attempted to determine the effects of elevated pCO2 on marine invertebrate fertilization success, albeit with differing results. These conflicts may stem from the use of inappropriate sperm–egg contact times and, in several cases, the lack of measurements over a range of sperm concentrations extending from sperm-limited conditions to polyspermy scenarios. In our study, we used biologically realistic sperm–egg contact times and a full range of sperm concentrations to assess the effect of elevated pCO2 on fertilization in the broadcast spawning sea urchin, Strongylocentrotus franciscanus. Fertilization experiments were carried out in seawater bubbled with CO2 to 400 (control), 800, and 1800 ppm. Using a fertilization kinetics model, we estimate that elevated pCO2 levels both increased sperm limitation and reduced the efficiency of fast blocks to polyspermy. Thus, elevated pCO2 decreased the range of sperm concentrations over which high fertilization success was likely. Given the inherent difficulties in achieving high fertilization success in broadcast spawners, raised pCO2 levels are likely to exacerbate low fertilization success in low-density populations or in areas with high water turbulence.