Metal contamination increases the sensitivity of larvae but not gametes to ocean acidification in the polychaete Pomatoceros lamarckii (Quatrefages)

Ocean acidification is not happening in isolation but against a background of chronic low-level pollution for most coastal marine environments. The reproductive and larval stages of marine invertebrates can be highly sensitive to the impacts of both environmental pollutants and ocean acidification, but very little is currently known regarding the potential impacts of combined contaminant and high CO₂ exposures on the health of marine organisms. Ocean acidification research to date has focused heavily on the responses of calcifying marine invertebrate larvae and algae, and as such the polychaetes as a group, despite their ecological importance, remain understudied. Here, we investigate the effects of elevated seawater CO₂ (pH range 8.1–7.4, plus an extreme pH of 7.2 in the sperm motility experiments), in combination with the environmental pollutant copper (0.002 μM), on the early life history stages of the intertidal polychaete Pomatoceros lamarckii from two populations. P. lamarckii sperm appear to be robust to elevated seawater CO₂. Whilst all three of the sperm motility end points measured showed a response to elevated CO₂, these responses were small and not linear. The percentage of motile sperm and sperm curvilinear velocity were significantly reduced in the lower pH treatments of 7.4 and 7.2, whereas sperm straight-line velocity (VSL) was mostly unaffected except for an increased VSL at pH 8.0. Fertilisation success was investigated using two populations from the South West (UK), one from Torquay and one from Plymouth Sound. Fertilisation success was slightly but significantly reduced at the 7.6 and 7.4 pH treatments for both populations (a 9.0 % reduction in fertilisation success from pH 8.1 to 7.4 for Torquay), but with a greater effect observed in the population from Plymouth Sound (a 13.33 % reduction in fertilisation success). No additional impact of 0.002 μM copper exposure on fertilisation success was found. Larval survival was found to be much more sensitive to elevated CO₂ than sperm function or fertilisation, and a significant interaction with copper exposure was observed. These results demonstrate the potential for polychaete larvae to be affected by predicted ocean acidification conditions and that chronic coastal pollutants, such as copper, have the potential to alter larval susceptibility to ocean acidification conditions.     

Predicted impact of ocean acidification on a marine invertebrate: elevated CO<Subscript>2</Subscript> alters response to thermal stress in sea urchin larvae

Ocean acidification (OA) and the biological consequences of altered seawater chemistry have emerged as a significant environmental threat to healthy marine ecosystems. Because a more acidic ocean interferes with fixation of calcium carbonate to form shells or calcified skeletons, future ocean chemistry may significantly alter the physiology of calcifying marine organisms. These alterations may manifest themselves directly in the calcification process, or have synergistic effects with other environmental factors such as elevated temperatures. New tools permit us to explore subtle changes in gene expression patterns in response to environmental conditions. We raised sea urchins (Strongylocentrotus franciscanus) under conditions simulating future atmospheric CO₂ levels of 540 and 970 ppm. When larvae raised under elevated CO₂ conditions were subjected to 1-h acute temperature stress, their ability to mount a physiological response (as measured by expression of the molecular chaperone hsp70) was reduced relative to those raised under ambient CO₂ conditions. These results represent the first use of gene expression assays to study the effects of OA on sea urchin development. They highlight the importance of looking at multiple environmental factors simultaneously as this approach may reveal previously unsuspected biological impacts of atmospheric changes.     

海洋酸化对鱼类感觉和行为影响的研究进展

海洋酸化是指大气增多的二氧化碳(CO2)溶解于海水而导致海水p H值降低的过程。海洋酸化将改变海水碳酸盐平衡体系,使依赖于原化学环境的多种海洋生物乃至生态系统面临巨大威胁。海洋酸化对钙质生物影响的研究最早引起大家关注,而海洋鱼类具有较完善的酸碱调节机制,大家普遍认为酸化对其影响不大。但在过去的5年中,不少实验证明海洋酸化会影响海洋鱼类仔稚鱼的感觉和行为,减弱其野外的生存能力及增加被捕食率,很可能将威胁自然种群补给量和影响全球的渔业资源量。本文从嗅觉、听觉、视觉及高级意识和相关行为角度,综述近几年海洋酸化对鱼类感觉和行为影响的研究进展,介绍了鱼类神经行为生物学的研究,为全面了解和预测海洋酸化的生态、经济和社会效应提供科学依据。     

The physiological and molecular responses of larvae from the reef-building coral Pocillopora damicornis exposed to near-future increases in temperature and pCO2

Given the threats of greenhouse gas emissions and a changing climate to marine ecosystems, there is an urgent need to better understand the response of not only adult corals, which are particularly sensitive to environmental changes, but also their larvae, whose mechanisms of acclimation to both temperature increases and ocean acidification are not well understood. Brooded larvae from the reef coral Pocillopora damicornis collected from Nanwan Bay, Southern Taiwan, were exposed to ambient or elevated temperature (25 or 29 °C) and pCO₂ (415 or 635 μatm) in a factorial experiment for 9 days, and a variety of physiological and molecular parameters were measured. Respiration and rubisco protein expression decreased in larvae exposed to elevated temperature, while those incubated at high pCO₂ were larger in size. Collectively, these findings highlight the complex metabolic and molecular responses of this life history stage and the need to integrate our understanding across multiple levels of biological organization. Our results also suggest that for this pocilloporid larval life stage, the impacts of elevated temperature are likely a greater threat under near-future predictions for climate change than ocean acidification.     

Growth response of an early successional assemblage of coralline algae and benthic diatoms to ocean acidification

The sustained absorption of anthropogenically released atmospheric CO₂ by the oceans is modifying seawater carbonate chemistry, a process termed ocean acidification (OA). By the year 2100, the worst case scenario is a decline in the average oceanic surface seawater pH by 0.3 units to 7.75. The changing seawater carbonate chemistry is predicted to negatively affect many marine species, particularly calcifying organisms such as coralline algae, while species such as diatoms and fleshy seaweed are predicted to be little affected or may even benefit from OA. It has been hypothesized in previous work that the direct negative effects imposed on coralline algae, and the direct positive effects on fleshy seaweeds and diatoms under a future high CO₂ ocean could result in a reduced ability of corallines to compete with diatoms and fleshy seaweed for space in the future. In a 6-week laboratory experiment, we examined the effect of pH 7.60 (pH predicted to occur due to ocean acidification just beyond the year 2100) compared to pH 8.05 (present day) on the lateral growth rates of an early successional, cold-temperate species assemblage dominated by crustose coralline algae and benthic diatoms. Crustose coralline algae and benthic diatoms maintained positive growth rates in both pH treatments. The growth rates of coralline algae were three times lower at pH 7.60, and a non-significant decline in diatom growth meant that proportions of the two functional groups remained similar over the course of the experiment. Our results do not support our hypothesis that benthic diatoms will outcompete crustose coralline algae under future pH conditions. However, while crustose coralline algae were able to maintain their presence in this benthic rocky reef species assemblage, the reduced growth rates suggest that they will be less capable of recolonizing after disturbance events, which could result in reduced coralline cover under OA conditions.     

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.     

Populations of the Sydney rock oyster, Saccostrea glomerata, vary in response to ocean acidification

Acidifying oceans are predicted to fundamentally alter marine ecosystems. Over the next century, acute studies suggest that the impacts of climate change on marine organisms and ecosystems may be catastrophic. To date, however, little is known about whether the response of marine organisms varies within a species and whether this provides a potential ??adaptive capacity??. Here, we show that selectively bred lines of the ecologically and economically important estuarine mollusc, the Sydney rock oyster Saccostrea glomerata, are more resilient to ocean acidification than the wild populations. When reared at elevated pCO₂, we found a 25% reduction in shell growth of the selectively bred population of the Sydney rock oyster, Saccostrea glomerata, compared to a 64% reduction in shell growth of wild populations. This study shows that there are significantly different sensitivities to ocean acidification even within the same species, providing preliminary evidence that selective breeding may be a solution for important aquaculture industries to overcome the future effects of ocean acidification.     

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.     

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.     

Ocean acidification reduces biomineralization-related gene expression in the sea urchin, Hemicentrotus pulcherrimus

Although recent studies have demonstrated that calcification in a wide range of marine organisms is profoundly affected by CO₂-induced ocean acidification, the mechanism of this phenomenon is still unclear. To clarify the effects of ocean acidification on the calcification process at the molecular level, we evaluated the expression of three biomineralization-related genes in the sea urchin Hemicentrotus pulcherrimus exposed under control, 1,000, and 2,000?ppm CO₂ from egg to pluteus larval stage. We found that the expression of the gene msp130, which is proposed to transport Ca²⁺ to the calcification site, is suppressed by increased CO₂ at pluteus larval stage. Meanwhile, expression of the spicule protein matrix genes SM30 and SM50 was apparently not affected. The results suggest that the combined effects of ocean acidification on the expression of skeletogenesis-related genes as well as the change in seawater carbonate chemistry affect the biomineralization ability of sea urchins.     

Response of sea urchin pluteus larvae (Echinodermata: Echinoidea) to reduced seawater pH: a comparison among a tropical, temperate, and a polar species

Ocean acidification, as a result of increased atmospheric CO₂, is predicted to lower the pH of seawater to between pH 7.6 and 7.8 over the next 100 years. The greatest changes are expected in polar waters. Our research aimed to examine how echinoid larvae are affected by lower pH, and if effects are more pronounced in polar species. We examined the effects of lowered pH on larvae from tropical (Tripneustes gratilla), temperate (Pseudechinus huttoni, Evechinus chloroticus), and a polar species (Sterechinus neumayeri) in a series of laboratory experiments. Larvae were reared in a range of lower pH seawater (pH 6.0, 6.5, 7.0, 7.5, 7.7, 7.8 and ambient), adjusted by bubbling CO₂ gas. The effect of pH on somatic and skeletal growth, calcification index, development and survival were quantified, while SEM examination of the larval skeleton provided information on the effects of seawater pH on the fine-scale skeletal morphology. Lowering pH resulted in a decrease in survival in all species, but only below pH 7.0. The size of larvae were reduced at lowered pH, but the external morphology (shape) was unaffected. Calcification of the larval skeleton was significantly reduced (13.8–36.9% lower) under lowered pH, with the exception of the Antarctic species, which showed no significant difference. SEM examination revealed a degradation of the larval skeletons of Pseudechinus and Evechinus when grown in reduced pH. Sterechinus and Tripneustes showed no apparent difference in the skeletal fine structure under lowered pH. The study confirms the need to look beyond mortality as a single endpoint when considering the effects of ocean acidification that may occur through the 21st century, and instead, look for a suite of more subtle changes, which may indirectly affect the functioning of larval stages.     

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.     

Effects of ocean acidification on invertebrate settlement at volcanic CO2 vents

We present the first study of the effects of ocean acidification on settlement of benthic invertebrates and microfauna. Artificial collectors were placed for 1 month along pH gradients at CO₂ vents off Ischia (Tyrrhenian Sea, Italy). Seventy-nine taxa were identified from six main taxonomic groups (foraminiferans, nematodes, polychaetes, molluscs, crustaceans and chaetognaths). Calcareous foraminiferans, serpulid polychaetes, gastropods and bivalves showed highly significant reductions in recruitment to the collectors as pCO₂ rose from normal (336–341 ppm, pH 8.09–8.15) to high levels (886–5,148 ppm) causing acidified conditions near the vents (pH 7.08–7.79). Only the syllid polychaete Syllis prolifera had higher abundances at the most acidified station, although a wide range of polychaetes and small crustaceans was able to settle and survive under these conditions. A few taxa (Amphiglena mediterranea, Leptochelia dubia, Caprella acanthifera) were particularly abundant at stations acidified by intermediate amounts of CO₂ (pH 7.41–7.99). These results show that increased levels of CO₂ can profoundly affect the settlement of a wide range of benthic organisms.     

Fertilization in a suite of coastal marine invertebrates from SE Australia is robust to near-future ocean warming and acidification

Climate change driven ocean acidification and hypercapnia may have a negative impact on fertilization in marine organisms because of the narcotic effect these stressors exert on sperm. In contrast, warmer, less viscous water may have a positive influence on sperm swimming speed and so ocean warming may enhance fertilization. To address questions on future vulnerabilities we examined the interactive effects of near-future ocean warming and ocean acidification/hypercapnia on fertilization in intertidal and shallow subtidal echinoids (Heliocidaris erythrogramma, H. tuberculata, Tripneustes gratilla, Centrostephanus rodgersii), an asteroid (Patiriella regularis) and an abalone (Haliotis coccoradiata). Batches of eggs from multiple females were fertilized by sperm from multiple males in all combinations of three temperature and three \textpH/P_\textCO2 {\text{pH}}/P_{{{\text{CO}}_{2} }} treatments. Experiments were placed in the setting of projected near-future conditions for southeast Australia, an ocean change hot spot. There was no significant effect of warming and acidification on the percentage of fertilization. These results indicate that fertilization in these species is robust to temperature and \textpH/P_\textCO2 {\text{pH}}/P_{{{\text{CO}}_{2} }} fluctuation. This may reflect adaptation to the marked fluctuation in temperature and pH that characterises their shallow water coastal habitats. Efforts to identify potential impacts of ocean change to the life histories of coastal marine invertebrates are best to focus on more vulnerable embryonic and larval stages because of their long time in the water column where seawater chemistry and temperature have a major impact on development.     

Egg and early larval stages of Baltic cod, Gadus morhua, are robust to high levels of ocean acidification

The accumulation of carbon dioxide in the atmosphere will lower the pH in ocean waters, a process termed ocean acidification (OA). Despite its potentially detrimental effects on calcifying organisms, experimental studies on the possible impacts on fish remain scarce. While adults will most likely remain relatively unaffected by changes in seawater pH, early life-history stages are potentially more sensitive, due to the lack of gills with specialized ion-regulatory mechanisms. We tested the effects of OA on growth and development of embryos and larvae of eastern Baltic cod, the commercially most important fish stock in the Baltic Sea. Cod were reared from newly fertilized eggs to early non-feeding larvae in 5 different experiments looking at a range of response variables to OA, as well as the combined effect of CO₂ and temperature. No effect on hatching, survival, development, and otolith size was found at any stage in the development of Baltic cod. Field data show that in the Bornholm Basin, the main spawning site of eastern Baltic cod, in situ levels of pCO₂ are already at levels of 1,100 μatm with a pH of 7.2, mainly due to high eutrophication supporting microbial activity and permanent stratification with little water exchange. Our data show that the eggs and early larval stages of Baltic cod seem to be robust to even high levels of OA (3,200 μatm), indicating an adaptational response to CO₂.     

Impact of ocean acidification on marine ecosystems: educational challenges and innovations

Population growth and social/technological developments have resulted in the buildup of carbon dioxide (CO₂) in the atmosphere and oceans to the extent that we now see changes in the earth’s climate and ocean chemistry. Ocean acidification is one consequence of these changes, and it is known with certainty that it will continue to increase as we emit more CO₂ into the atmosphere. Ocean acidification is a global issue likely to impact marine organisms, food webs and ecosystems and to be most severely experienced by the people who depend on the goods and services the ocean provides at regional and local levels. However, research is in its infancy and the available data on biological impacts are complex (e.g., species-specific response). Educating future generations on the certainties and uncertainties of the emerging science of ocean acidification and its complex consequences for marine species and ecosystems can provide insights that will help assessing the need to mitigate and/or adapt to future global change. This article aims to present different educational approaches, the different material available and highlight the future challenges of ocean acidification education for both educators and marine biologists.     

Spatio-temporal variability of polychaete colonization at volcanic CO2 vents indicates high tolerance to ocean acidification

Ocean acidification is predicted to have negative effects on marine biota, resulting in the loss of biodiversity and changes in marine ecosystem structure and function. However, some species and life stages may be capable of thriving in low pH conditions, either due to their natural ability to tolerate stressful low pH–high pCO₂ conditions and/or alteration of species interactions caused by changes in pH profiles, or due to evolutionary trade-offs. A better understanding of which species may be capable of tolerating ocean acidification can guide future research into the mechanisms for physiological and ecological resilience to future carbon dioxide (CO₂) conditions. We investigated the colonization of selected polychaete species along a pH gradient originating from shallow, coastal volcanic CO₂ vents (Ischia, Italy). Colonization was quantified by exposing artificial invertebrate collectors attached to the substratum for 30 days during different periods of the year (late spring, fall and late winter). Three species, Amphiglena mediterranea, Platynereis dumerilii and Syllis prolifera, were present and abundant along the gradient throughout the year. All three species were significantly more abundant in the most acidified areas, confirming their high tolerance and capacity to cope with very low pH. Abundances of all three species were compared to data previously collected via collectors suspended in the water column. More individuals were found in the collectors attached to the substratum, suggesting that abundances may have previously been underestimated. This is likely due to the close proximity of these collectors with the natural rocky substratum. All three species exhibited similar temporal variability, consistent with their life cycle and reproductive biology. Our results demonstrate high tolerance of the species for low and variable pH and corroborate their use as robust models to explore the capacity to cope with low pH–high pCO₂ conditions, both in the natural vent systems and in the laboratory.     

Maintenance of coelomic fluid pH in sea urchins exposed to elevated CO2: the role of body cavity epithelia and stereom dissolution

Experimental ocean acidification leads to a shift in resource allocation and to an increased [HCO₃ ^?] within the perivisceral coelomic fluid (PCF) in the Baltic green sea urchin Strongylocentrotus droebachiensis. We investigated putative mechanisms of this pH compensation reaction by evaluating epithelial barrier function and the magnitude of skeleton (stereom) dissolution. In addition, we measured ossicle growth and skeletal stability. Ussing chamber measurements revealed that the intestine formed a barrier for HCO₃ ^? and was selective for cation diffusion. In contrast, the peritoneal epithelium was leaky and only formed a barrier for macromolecules. The ossicles of 6 week high CO₂-acclimatised sea urchins revealed minor carbonate dissolution, reduced growth but unchanged stability. On the other hand, spines dissolved more severely and were more fragile following acclimatisation to high CO₂. Our results indicate that epithelia lining the PCF space contribute to its acid–base regulation. The intestine prevents HCO₃ ^? diffusion and thus buffer leakage. In contrast, the leaky peritoneal epithelium allows buffer generation via carbonate dissolution from the surrounding skeletal ossicles. Long-term extracellular acid–base balance must be mediated by active processes, as sea urchins can maintain relatively high extracellular [HCO₃ ^?]. The intestinal epithelia are good candidate tissues for this active net import of HCO₃ ^? into the PCF. Spines appear to be more vulnerable to ocean acidification which might significantly impact resistance to predation pressure and thus influence fitness of this keystone species.     

Influence of CO<Subscript>2</Subscript>-related seawater acidification on extracellular acid–base balance in the velvet swimming crab <Emphasis Type="Italic">Necora puber</Emphasis>

We investigated the effect of different levels of hypercapnia-induced acidification (pH = 7.96, 7.31, 6.74 and 6.05) on the extracellular acid base balance of a shallow-water crustacean, the velvet swimming crab Necora puber over a period of 16 days. Any extracellular acidosis incurred was completely compensated by an increase in bicarbonate. Bicarbonate was partly, but not wholly, supplied by dissolution of the exoskeleton. This compensation was sustained for 16 days under all experimental treatments with two exceptions. First there was some evidence of extracellular acidosis in crabs after 16 days at pH = 6.74. Second at the lowest environmental pH (6.05) there was a marked uncompensated acidosis after 24 h. Necora puber appears less sensitive to low pH than many other species examined acutely. However, local acidification as a result of ocean CO₂ dispersal or leakage from geological sequestration is likely to compromise even this species.