Future ocean acidification will be amplified by hypoxia in coastal habitats

Ocean acidification is elicited by anthropogenic carbon dioxide emissions and resulting oceanic uptake of excess CO₂ and might constitute an abiotic stressor powerful enough to alter marine ecosystem structures. For surface waters in gas-exchange equilibrium with the atmosphere, models suggest increases in CO₂ partial pressure (pCO₂) from current values of ca. 390 μatm to ca. 700–1,000 μatm by the end of the century. However, in typically unequilibrated coastal hypoxic regions, much higher pCO₂ values can be expected, as heterotrophic degradation of organic material is necessarily related to the production of CO₂ (i.e., dissolved inorganic carbon). Here, we provide data and estimates that, even under current conditions, maximum pCO₂ values of 1,700–3,200 μatm can easily be reached when all oxygen is consumed at salinities between 35 and 20, respectively. Due to the nonlinear nature of the carbonate system, the approximate doubling of seawater pCO₂ in surface waters due to ocean acidification will most strongly affect coastal hypoxic zones as pCO₂ during hypoxia will increase proportionally: we calculate maximum pCO₂ values of ca. 4,500 μatm at a salinity of 20 (T = 10 °C) and ca. 3,400 μatm at a salinity of 35 (T = 10 °C) when all oxygen is consumed. Upwelling processes can bring these CO₂-enriched waters in contact with shallow water ecosystems and may then affect species performance there as well. We conclude that (1) combined stressor experiments (pCO₂ and pO₂) are largely missing at the moment and that (2) coastal ocean acidification experimental designs need to be closely adjusted to carbonate system variability within the specific habitat. In general, the worldwide spread of coastal hypoxic zones also simultaneously is a spread of CO₂-enriched zones. The magnitude of expected changes in pCO₂ in these regions indicates that coastal systems may be more endangered by future global climate change than previously thought.     

Impact of ocean acidification in the metabolism and swimming behavior of the dolphinfish (Coryphaena hippurus) early larvae

Since the industrial revolution, [CO₂]_atm has increased from 280 μatm to levels now exceeding 380 μatm and is expected to rise to 730–1,020 μatm by the end of this century. The consequent changes in the ocean’s chemistry (e.g., lower pH and availability of the carbonate ions) are expected to pose particular problems for marine organisms, especially in the more vulnerable early life stages. The aim of this study was to investigate how the future predictions of ocean acidification may compromise the metabolism and swimming capabilities of the recently hatched larvae of the tropical dolphinfish (Coryphaena hippurus). Here, we show that the future environmental hypercapnia (ΔpH 0.5; 0.16 % CO₂, ~1,600 μatm) significantly (p < 0.05) reduced oxygen consumption rate up to 17 %. Moreover, the swimming duration and orientation frequency also decreased with increasing pCO₂ (50 and 62.5 %, respectively). We argue that these hypercapnia-driven metabolic and locomotory challenges may potentially influence recruitment, dispersal success, and the population dynamics of this circumtropical oceanic top predator.     

Effects of pCO2 on physiology and skeletal mineralogy in a tidal pool coralline alga Corallina elongata

Marine organisms inhabiting environments where pCO₂/pH varies naturally are suggested to be relatively resilient to future ocean acidification. To test this hypothesis, the effect of elevated pCO₂ was investigated in the articulated coralline red alga Corallina elongata from an intertidal rock pool on the north coast of Brittany (France), where pCO₂ naturally varied daily between 70 and 1000 μatm. Metabolism was measured on algae in the laboratory after they had been grown for 3 weeks at pCO₂ concentrations of 380, 550, 750 and 1000 μatm. Net and gross primary production, respiration and calcification rates were assessed by measurements of oxygen and total alkalinity fluxes using incubation chambers in the light and dark. Calcite mol % Mg/Ca (mMg/Ca) was analysed in the tips, branches and basal parts of the fronds, as well as in new skeletal structures produced by the algae in the different pCO₂ treatments. Respiration, gross primary production and calcification in light and dark were not significantly affected by increased pCO₂. Algae grown under elevated pCO₂ (550, 750 and 1000 μatm) formed fewer new structures and produced calcite with a lower mMg/Ca ratio relative to those grown under 380 μatm. This study supports the assumption that C. elongata from a tidal pool, where pCO₂ fluctuates over diel and seasonal cycles, is relatively robust to elevated pCO₂ compared to other recently investigated coralline algae.     

Effects of ocean acidification on the early developmental stages of the horned turban,Turbo cornutus

To estimate the impact of CO₂-driven ocean acidification on the early life stages of gastropods, the effects of increased partial pressure of seawater carbon dioxide (pCO₂) (800–2,000 μatm) on the early developmental stages and larval shell length of the commercially important gastropod, the horned turban snail, Turbo cornutus were investigated. Increase in experimental seawater pCO₂ had an increasingly negative impact on the early developmental rate; the proportion of embryos or larvae displaying retarded development increased at higher pCO₂. The proportion of embryos that developed to the 4-cell stage at 2 h after fertilization decreased linearly with increasing pCO₂. At ~1,000 μatm pCO₂, retarded development was observed in ~50 % of larvae. No embryos developed to the 4-cell stage at 2,000 μatm pCO₂ within 2 h of fertilization. A similar trend continued until 24–26 h after fertilization; the proportion of larvae attaining veliger stage by 24–26 h also decreased with increasing pCO₂. The shell length of T. cornutus veligers decreased gradually as seawater pCO₂ increased, but markedly decreased in seawater under nearly unsaturated and unsaturated conditions (≤1.04) of the aragonite saturation state (Ω _aragonite). The results indicate that increased pCO₂ seawater has a progressive and acute effect on embryonic and larval T. cornutus, and imply that the extended early developmental period and/or the downsized larval shell produced by ocean acidification will have a negative impact on survival, settlement and recruitment well into the future.     

Fertilisation, embryogenesis and larval development in the tropical intertidal sand dollar Arachnoides placenta in response to reduced seawater pH

We examined the response of the tropical sand dollar Arachnoides placenta to reduced seawater pH in experiments spanning ca. 50 % of the planktonic larval duration. A. placenta inhabits intertidal sandy beaches where we observed a minimum in situ pH range 0.06 pH units (pH 8.10–8.16). The responses of gametes and larvae to seawater pH were tested in vitro in ambient (pH 8.14, pCO₂ = 525.7 μatm, total alkalinity = 2,651 μmol kg soln^?1) and three reduced pH seawater treatments (7.8–7.0). Percentage fertilisation decreased significantly with decreasing pH across a range of sperm/egg ratios (4:1 up to 4,000:1). A. placenta reached the advanced pluteus stage in 4 days, and during this time, we saw no difference in survival rate of larvae between the ambient (67 %) and pH 7.79 (72 %) treatments. Four-day survival was, however, reduced to 44 and 11 % in the pH 7.65 and 7.12 treatments, respectively. Larval development and morphometrics varied among pH treatments. Embryos reared in pH 7.12 exhibited arrested development. Larvae reared at pH 7.65 showed delayed development and greater mortality compared with those reared at pH 7.79 and 8.14. When larval morphometrics are compared among larvae of the same size, differences in larval width and total arm length between pH treatments disappear. These results suggest that variation in larval size among the three highest pH treatments at a given time are likely the result of slower development and apparent shrinkage of surviving larvae and not direct changes in larval shape. There were no differences in the percentage inorganic content (a proxy for calcification) in larvae reared in either an ambient or a pH 7.7 treatment. The responses of fertilisation and development to decreased pH/increased pCO₂ in A. placenta are within the range of those reported for other intertidal and subtidal echinoid species from colder latitudes.     

Tolerance of juvenile barnacles (Amphibalanus improvisus) to warming and elevated pCO2

We investigated the impacts of warming and elevated pCO₂ on newly settled Amphibalanus improvisus from Kiel Fjord, an estuarine ecosystem characterized by significant natural pCO₂ variability. In two experiments, juvenile barnacles were maintained at two temperature and three pCO₂ levels (20/24 °C, 700–2,140 μatm) for 8 weeks in a batch culture and at four pCO₂ levels (20 °C, 620–2,870 μatm) for 12 weeks in a water flow-through system. Warming as well as elevated pCO₂ hardly affected growth or the condition index of barnacles, although some factor combinations led to temporal significances in enhanced or reduced growth with an increase in pCO₂. While warming increased the shell strength of A. improvisus individuals, elevated pCO₂ had only weak effects. We demonstrate a strong tolerance of juvenile A. improvisus to mean acidification levels of about 1,000 μatm pCO₂ as is already naturally experienced by the investigated barnacle population.     

Structural and functional vulnerability to elevated pCO2 in marine benthic communities

The effect of elevated pCO₂/low pH on marine invertebrate benthic biodiversity, community structure and selected functional responses which underpin ecosystem services (such as community production and calcification) was tested in a medium-term (30 days) mesocosm experiment in June 2010. Standardised intertidal macrobenthic communities, collected (50.3567°N, 4.1277°W) using artificial substrate units (ASUs), were exposed to one of seven pH treatments (8.05, 7.8. 7.6, 7.4, 7.2, 6.8 and 6.0). Community net calcification/dissolution rates, as well as changes in biomass, community structure and diversity, were measured at the end of the experimental period. Communities showed significant changes in structure and reduced diversity in response to reduced pH: shifting from a community dominated by calcareous organisms to one dominated by non-calcareous organisms around either pH 7.2 (number of individuals and species) or pH 7.8 (biomass). These results were supported by a reduced total weight of CaCO₃ structures in all major taxa at lowered pH and a switch from net calcification to net dissolution around pH 7.4 (Ω_calc = 0.78, Ω_ara = 0.5). Overall community soft tissue biomass did not change with pH and high mortality was observed only at pH 6.0, although molluscs and arthropods showed significant decreases in soft tissue. This study supports and refines previous findings on how elevated pCO₂ can induce changes in marine biodiversity, underlined by differential vulnerability of different phyla. In addition, it shows significant elevated pCO₂-/low pH-dependent changes in fundamental community functional responses underpinning changes in ecosystem services.     

Effect of increasing sea water pCO2 on the northern Atlantic krill species Nyctiphanes couchii

Surprisingly little is known about potential effects of ocean acidification on krill of the Northern Hemisphere as ecologically very important food web component. Sub-adult individuals of the northern Atlantic krill species Nyctiphanes couchii (caught at Austevoll near Bergen, Norway, in January 2013) were exposed in the laboratory to four different levels of pCO₂ (430, 800, 1,100, and 1,700 µatm) for 5 weeks in order to assess potential changes in a set of biological response variables. Survival decreased and the frequency of moulting-related deaths increased with increasing pCO₂. Survival was considerably reduced at relatively high pCO₂ of 1,700 µatm and tended to be negatively affected at 1,100 µatm pCO₂. However, the experimental results show no significant effects of pCO₂ on inter-moult period and growth at pCO₂ levels below 1,100 µatm. No differences in length measurements of the carapace and uropod were observed across pCO₂ levels, indicating no effect of changing carbonate chemistry on the morphology of those calciferous parts of the exoskeleton. The results suggest that sub-adult N. couchii may not suffer dramatically from predicted near-future changes in pCO₂. However, potential detrimental effects on the moulting process and associated higher mortality at 1,100 µatm pCO₂ cannot be excluded. Further experiments are needed in order to investigate whether early life stages of N. couchii show a different sensitivity to elevated sea water pCO₂ and whether those results are transferable to other krill species of the Northern Hemisphere.     

Effects of elevated pCO2 and the effect of parent acclimation on development in the tropical Pacific sea urchin Echinometra mathaei

Effects of acclimation to projected near-future ocean acidification (OA) conditions on physiology, reproduction and development were investigated in the tropical sea urchin Echinometra mathaei. Following 6 weeks in control or one of the three elevated pCO₂ (pH_NIST 7.5–8.1; pCO₂ ~485–1,770 μatm) conditions, adult urchins exhibited a slight decline of growth in low pH treatments and moderately reduced respiration at intermediate levels. At 7 weeks, gametes from adults were used to produce larvae that were reared in their respective parental treatments. To assess whether larvae from acclimated parents are more resilient to elevated pCO₂ than those not acclimated, larvae from control animals were also reared in the elevated pCO₂ treatments. There was no difference in female ‘spawnability’ and oocyte size between treatments, but male spawning ability was reduced in increased pCO₂ conditions. In elevated pCO₂ treatments, the percentage of normal larvae and larval size decreased in the progeny of control- and elevated pCO₂-acclimated parents, and arm asymmetry increased. Thus, acclimation of the parents did not make the progeny more resilient or sensitive to OA effects. Negative effects of increased pCO₂ on reproduction and development may impact on recruitment and population maintenance of this species.     

Tough as a rock-boring urchin: adult Echinometra sp. EE from the Red Sea show high resistance to ocean acidification over long-term exposures

Ocean acidification, a process caused by the continuous rise of atmospheric CO₂ levels, is expected to have a profound impact on marine invertebrates. Findings of the numerous studies conducted in this field indicate high variability in species responses to future ocean conditions. This study aimed at understanding the effects of long-term exposure to elevated pCO₂ conditions on the performance of adult Echinometra sp. EE from the Gulf of Aqaba (Red Sea). During an 11-month incubation under high pCO₂ (1,433 μatm, pH_NBS 7.7) and control (435 μatm, pH_NBS 8.1) conditions, we examined the urchins’ somatic and gonadal growth, gametogenesis and skeletal microstructure. Somatic and gonadal growths were exhibited with no significant differences between the treatments. In addition, all urchins in the experiment completed a full reproductive cycle, typical of natural populations, with no detectable impact of increased pCO₂ on the timing, duration or progression of the cycle. Furthermore, scanning electron microscopy imaging of urchin tests and spines revealed no signs of the usual observed effects of acidosis, such as skeletal dissolution, widened stereom pores or non-smoothed structures. Our results, which yielded no significant impact of the high pCO₂ treatment on any of the examined processes in the urchins studied, suggest high resistance of adult Echinometra sp. EE to near future ocean acidification conditions. With respect to other findings in this area, the outcome of this study provides an example of the complicated and diverse responses of echinoids to the predicted environmental changes.     

Elevated CO2 affects the behavior of an ecologically and economically important coral reef fish

We tested the effect of near-future CO₂ levels (≈490, 570, 700, and 960 μatm CO₂) on the olfactory responses and activity levels of juvenile coral trout, Plectropomus leopardus, a piscivorous reef fish that is also one of the most important fisheries species on the Great Barrier Reef, Australia. Juvenile coral trout reared for 4 weeks at 570 μatm CO₂ exhibited similar sensory responses and behaviors to juveniles reared at 490 μatm CO₂ (control). In contrast, juveniles reared at 700 and 960 μatm CO₂ exhibited dramatically altered sensory function and behaviors. At these higher CO₂ concentrations, juveniles became attracted to the odor of potential predators, as has been observed in other reef fishes. They were more active, spent less time in shelter, ventured further from shelter, and were bolder than fish reared at 490 or 570 μatm CO₂. These results demonstrate that behavioral impairment of coral trout is unlikely if pCO₂ remains below 600 μatm; however, at higher levels, there are significant impacts on juvenile performance that are likely to affect survival and energy budgets, with consequences for predator–prey interactions and commercial fisheries.     

Long-term and trans-life-cycle effects of exposure to ocean acidification in the green sea urchin Strongylocentrotus droebachiensis

Anthropogenic CO₂ emissions are acidifying the world’s oceans. A growing body of evidence demonstrates that ocean acidification can impact survival, growth, development and physiology of marine invertebrates. Here, we tested the impact of long-term (up to 16 months) and trans-life-cycle (adult, embryo/larvae and juvenile) exposure to elevated pCO₂ (1,200 μatm, compared to control 400 μatm) on the green sea urchin Strongylocentrotus droebachiensis. Female fecundity was decreased 4.5-fold when acclimated to elevated pCO₂ for 4 months during reproductive conditioning, while no difference was observed in females acclimated for 16 months. Moreover, adult pre-exposure for 4 months to elevated pCO₂ had a direct negative impact on subsequent larval settlement success. Five to nine times fewer offspring reached the juvenile stage in cultures using gametes collected from adults previously acclimated to high pCO₂ for 4 months. However, no difference in larval survival was observed when adults were pre-exposed for 16 months to elevated pCO₂. pCO₂ had no direct negative impact on juvenile survival except when both larvae and juveniles were raised in elevated pCO₂. These negative effects on settlement success and juvenile survival can be attributed to carry-over effects from adults to larvae and from larvae to juveniles. Our results support the contention that adult sea urchins can acclimate to moderately elevated pCO₂ in a matter of a few months and that carry-over effects can exacerbate the negative impact of ocean acidification on larvae and juveniles.     

Elevated pCO2 causes developmental delay in early larval Pacific oysters, Crassostrea gigas

Increasing atmospheric CO₂ equilibrates with surface seawater, elevating the concentration of aqueous hydrogen ions. This process, ocean acidification, is a future and contemporary concern for aquatic organisms, causing failures in Pacific oyster (Crassostrea gigas) aquaculture. This experiment determines the effect of elevated pCO₂ on the early development of C. gigas larvae from a wild Pacific Northwest population. Adults were collected from Friday Harbor, Washington, USA (48°31.7′N, 12°1.1′W) and spawned in July 2011. Larvae were exposed to Ambient (400 μatm CO₂), MidCO₂ (700 μatm), or HighCO₂ (1,000 μatm). After 24 h, a greater proportion of larvae in the HighCO₂ treatment were calcified as compared to Ambient. This unexpected observation is attributed to increased metabolic rate coupled with sufficient energy resources. Oyster larvae raised at HighCO₂ showed evidence of a developmental delay by 3 days post-fertilization, which resulted in smaller larvae that were less calcified.     

Ocean acidification and warming alter photosynthesis and calcification of the symbiont-bearing foraminifera Marginopora vertebralis

The impact of elevated CO₂ and temperature on photosynthesis and calcification in the symbiont-bearing benthic foraminifer Marginopora vertebralis was studied. Individual specimens of M. vertebralis were collected from Heron Island on the southern Great Barrier Reef (Australia). They were maintained for 5 weeks at different temperatures (28, 32 °C) and pCO₂ (400, 1,000 µatm) levels spanning a range of current and future climate-change scenarios. The photosynthetic capacity of M. vertebralis was measured with O₂ microsensors and a pulse-amplitude-modulated chlorophyll (Chl) fluorometer, in combination with estimates of Chl a and Chl c ₂ concentrations and calcification rates. After 5 weeks, control specimens remained unaltered for all parameters. Chlorophyll a concentrations significantly decreased in the specimens at 1,000 µatm CO₂ for both temperatures, while no change in Chl c ₂ concentration was observed. Photoinhibition was observed under elevated CO₂ and temperature, with a 70–80 % decrease in the maximum quantum yield of PSII. There was no net O₂ production at elevated temperatures in both CO₂ treatments as compared to the control temperature, supporting that temperature has more impact on photosynthesis and O₂ flux than changes in ambient CO₂. Photosynthetic pigment loss and a decrease in photochemical efficiency are thus likely to occur with increased temperature. The elevated CO₂ and high temperature treatment also lead to a reduction in calcification rate (from +0.1 to >?0.1 % day^?1). Thus, both calcification and photosynthesis of the major sediment-producing foraminifer M. vertebralis appears highly vulnerable to elevated temperature and ocean acidification scenarios predicted in climate-change models.     

Brooded coral larvae differ in their response to high temperature and elevated pCO2 depending on the day of release

To evaluate the effects of temperature and pCO₂ on coral larvae, brooded larvae of Pocillopora damicornis from Nanwan Bay, Taiwan (21°56.179′N, 120°44.85′E), were exposed to ambient (419–470 μatm) and high (604–742 μatm) pCO₂ at ~25 and ~29 °C in two experiments conducted in March 2010 and March 2012. Larvae were sampled from four consecutive lunar days (LD) synchronized with spawning following the new moon, incubated in treatments for 24 h, and measured for respiration, maximum photochemical efficiency of PSII (F _v/F _m), and mortality. The most striking outcome was a strong effect of time (i.e., LD) on larvae performance: respiration was affected by an LD × temperature interaction in 2010 and 2012, as well as an LD × pCO₂ × temperature interaction in 2012; F _v/F _m was affected by LD in 2010 (but not 2012); and mortality was affected by an LD × pCO₂ interaction in 2010, and an LD × temperature interaction in 2012. There were no main effects of pCO₂ in 2010, but in 2012, high pCO₂ depressed metabolic rate and reduced mortality. Therefore, differences in larval performance depended on day of release and resulted in varying susceptibility to future predicted environmental conditions. These results underscore the importance of considering larval brood variation across days when designing experiments. Subtle differences in experimental outcomes between years suggest that transgenerational plasticity in combination with unique histories of exposure to physical conditions can modulate the response of brooded coral larvae to climate change and ocean acidification.     

Ocean acidification induces budding in larval sea urchins

Ocean acidification (OA), the reduction of ocean pH due to hydration of atmospheric CO₂, is known to affect growth and survival of marine invertebrate larvae. Survival and transport of vulnerable planktonic larval stages play important roles in determining population dynamics and community structures in coastal ecosystems. Here, we show that larvae of the purple urchin, Strongylocentrotus purpuratus, underwent high-frequency budding (release of blastula-like particles) when exposed to elevated pCO₂ level (>700 μatm). Budding was observed in >50 % of the population and was synchronized over short periods of time (~24 h), suggesting this phenomenon may be previously overlooked. Although budding can be a mechanism through which larval echinoids asexually reproduce, here, the released buds did not develop into viable clones. OA-induced budding and the associated reduction in larval size suggest new hypotheses regarding physiological and ecological tradeoffs between short-term benefits (e.g. metabolic savings and predation escape) and long-term costs (e.g. tissue loss and delayed development) in the face of climate change.     

Decreased pH does not alter metamorphosis but compromises juvenile calcification of the tube worm Hydroides elegans

Using CO₂ perturbation experiments, we examined the pre- and post-settlement growth responses of a dominant biofouling tubeworm (Hydroides elegans) to a range of pH. In three different experiments, embryos were reared to, or past, metamorphosis in seawater equilibrated to CO₂ values of about 480 (control), 980, 1,480, and 2,300 μatm resulting in pH values of around 8.1 (control), 7.9, 7.7, and 7.5, respectively. These three decreased pH conditions did not affect either embryo or larval development, but both larval calcification at the time of metamorphosis and early juvenile growth were adversely affected. During the 24-h settlement assay experiment, half of the metamorphosed larvae were unable to calcify tubes at pH 7.9 while almost no tubes were calcified at pH 7.7. Decreased ability to calcify at decreased pH may indicate that these calcifying tubeworms may be one of the highly threatened species in the future ocean.     

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.     

Microstructure of the paper nautilus (Argonauta nodosa) shell and the novel application of electron backscatter diffraction (EBSD) to address effects of ocean acidification

Electron backscatter diffraction (EBSD) is a powerful microscopic technique to characterise the crystallography of biomineralisation. Here, we use high-resolution EBSD to characterise one of the least studied shells in the ocean, the female argonaut brood chamber, and to examine the changes in shell microstructure in response to incubation in decreased pH conditions. The thin (225 μm) shell of Argonauta nodosa is magnesium calcite with an average magnesium content of ca. 5.1 Wt % MgCO₃. EBSD and scanning electron microscopy (SEM) revealed that calcification of the shell is bidirectional with formation of irregular crystalline grains. Following a 2 week incubation in a range of pH treatments (pH, 8.1–7.2), shell fragment weight decreased by dissolution in pH ≤ 7.8. EBSD and SEM revealed altered shell crystallography and microstructure at pH ≤ 7.4 due to preferential etching down crystallite grain boundaries and a change in crystalline orientation on both the inner and outer shell surfaces. Our study highlights the value of EBSD for the detailed examination of biogenic carbonates and its potential use in the field of ocean acidification research.