Sue-Ann Watson

Near-future carbon dioxide levels alter fish behaviour by interfering with neurotransmitter function

A study of two species of coral reef fish demonstrates that the anticipated increase in atmospheric carbon dioxide directly interferes with neurotransmitter function in their larvae, a hitherto unrecognized problem for marine fishes. Predicted future CO2 levels have been found to alter sensory responses and behaviour of marine fishes. Changes include increased boldness and activity, loss of behavioural lateralization, altered auditory preferences and impaired olfactory function1,2,3,4,5. Impaired olfactory function makes larval fish attracted to odours they normally avoid, including ones from predators and unfavourable habitats1,3. These behavioural alterations have significant effects on mortality that may have far-reaching implications for population replenishment, community structure and ecosystem function2,6. However, the underlying mechanism linking high CO2 to these diverse responses has been unknown. Here we show that abnormal olfactory preferences and loss of behavioural lateralization exhibited by two species of larval coral reef fish exposed to high CO2 can be rapidly and effectively reversed by treatment with an antagonist of the GABA-A receptor. GABA-A is a major neurotransmitter receptor in the vertebrate brain. Thus, our results indicate that high CO2 interferes with neurotransmitter function, a hitherto unrecognized threat to marine populations and ecosystems. Given the ubiquity and conserved function of GABA-A receptors, we predict that rising CO2 levels could cause sensory and behavioural impairment in a wide range of marine species, especially those that tightly control their acid–base balance through regulatory changes in HCO3− and Cl− levels.

Early Larval Development of the Sydney Rock Oyster Saccostrea glomerata Under Near-Future Predictions of CO2-Driven Ocean Acidification

ABSTRACT Anthropogenic emissions of carbon dioxide (CO2) from fossil fuel combustion and deforestation are rapidly increasing the atmospheric concentration of CO2 and reducing the pH of the oceans. This study shows that predicted near-future levels of ocean acidification have significant negative effects on early larval development of the Sydney rock oyster Saccostrea glomerata (Gould, 1850). CO2 was added to seawater to produce pH levels set at 8.1 (control), 7.8, and 7.6 (actual pH values were 8.11, 7.81, and 7.64, respectively). These treatments represent present-day surface ocean pH, as well as upper (&Dgr; pH ≈ -0.3) and lower (&Dgr; pH ≈ -0.5) pH predictions for the surface oceans in 2100. With decreasing pH, survival of S. glomerata larvae decreased, and growth and development were retarded. Larval survival decreased by 43% at pH 7.8 and by 72% at pH 7.6. Antero-posterior measurement (APM) was reduced by 6.3% at pH 7.8 and 8.7% at pH 7.6, and dorso-ventral measurement (DVM) was reduced by 5.1% atpH 7.8 and 7.5% at pH 7.6. The percentage of empty shells remaining from dead larvae decreased by 16% atpH 7.8 and by 90% at pH 7.6 indicating that the majority of empty shells dissolved within 7 days at pH 7.6. Scanning electron microscope images of 8-day-old larvae show abnormalities on the shell surface at low pH suggesting (1) problems with shell deposition, (2) retarded periostracum formation, and/or (3) increased shell dissolution. Larval life-history stages are considered particularly susceptible to climate change, and this study shows that S. glomerata larvae are sensitive to a high-CO2 world and are, specifically, negatively affected by exposure to pH conditions predicted for the worlds oceans for the year 2100.

Impaired learning of predators and lower prey survival under elevated CO2: A consequence of neurotransmitter interference

Ocean acidification is one of the most pressing environmental concerns of our time, and not surprisingly, we have seen a recent explosion of research into the physiological impacts and ecological consequences of changes in ocean chemistry. We are gaining considerable insights from this work, but further advances require greater integration across disciplines. Here, we showed that projected near-future CO2 levels impaired the ability of damselfish to learn the identity of predators. These effects stem from impaired neurotransmitter function; impaired learning under elevated CO2 was reversed when fish were treated with gabazine, an antagonist of the GABA-A receptor - a major inhibitory neurotransmitter receptor in the brain of vertebrates. The effects of CO2 on learning and the link to neurotransmitter interference were manifested as major differences in survival for fish released into the wild. Lower survival under elevated CO2 , as a result of impaired learning, could have a major influence on population recruitment.

Marine mollusc predator-escape behaviour altered by near-future carbon dioxide levels

Ocean acidification poses a range of threats to marine invertebrates; however, the potential effects of rising carbon dioxide (CO2) on marine invertebrate behaviour are largely unknown. Marine gastropod conch snails have a modified foot and operculum allowing them to leap backwards rapidly when faced with a predator, such as a venomous cone shell. Here, we show that projected near-future seawater CO2 levels (961 µatm) impair this escape behaviour during a predator–prey interaction. Elevated-CO2 halved the number of snails that jumped from the predator, increased their latency to jump and altered their escape trajectory. Physical ability to jump was not affected by elevated-CO2 indicating instead that decision-making was impaired. Antipredator behaviour was fully restored by treatment with gabazine, a GABA antagonist of some invertebrate nervous systems, indicating potential interference of neurotransmitter receptor function by elevated-CO2, as previously observed in marine fishes. Altered behaviour of marine invertebrates at projected future CO2 levels could have potentially far-reaching implications for marine ecosystems.

Ocean acidification slows retinal function in a damselfish through interference with GABAA receptors

Vision is one of the most efficient senses used by animals to catch prey and avoid predators. Therefore, any deficiency in the visual system could have important consequences for individual performance. We examined the effect of CO2 levels projected to occur by the end of this century on retinal responses in a damselfish, by determining the threshold of its flicker electroretinogram (fERG). The maximal flicker frequency of the retina was reduced by continuous exposure to elevated CO2, potentially impairing the capacity of fish to react to fast events. This effect was rapidly counteracted by treatment with a GABA antagonist (gabazine), indicating that GABAA receptor function is disrupted by elevated CO2. In addition to demonstrating the effects of elevated CO2 on fast flicker fusion of marine fishes, our results show that the fish retina could be a model system to study the effects of high CO2 on neural processing.

Elevated CO2 Affects Predator-Prey Interactions through Altered Performance

Recent research has shown that exposure to elevated carbon dioxide (CO2) affects how fishes perceive their environment, affecting behavioral and cognitive processes leading to increased prey mortality. However, it is unclear if increased mortality results from changes in the dynamics of predator-prey interactions or due to prey increasing activity levels. Here we demonstrate that ocean pCO2 projected to occur by 2100 significantly effects the interactions of a predator-prey pair of common reef fish: the planktivorous damselfish Pomacentrus amboinensis and the piscivorous dottyback Pseudochromis fuscus. Prey exposed to elevated CO2 (880 µatm) or a present-day control (440 µatm) interacted with similarly exposed predators in a cross-factored design. Predators had the lowest capture success when exposed to elevated CO2 and interacting with prey exposed to present-day CO2. Prey exposed to elevated CO2 had reduced escape distances and longer reaction distances compared to prey exposed to present-day CO2 conditions, but this was dependent on whether the prey was paired with a CO2 exposed predator or not. This suggests that the dynamics of predator-prey interactions under future CO2 environments will depend on the extent to which the interacting species are affected and can adapt to the adverse effects of elevated CO2.

Marine invertebrate skeleton size varies with latitude, temperature and carbonate saturation: implications for global change and ocean acidification

There is great concern over the future effects of ocean acidification on marine organisms, especially for skeletal calcification, yet little is known of natural variation in skeleton size and composition across the globe, and this is a prerequisite for identifying factors currently controlling skeleton mass and thickness. Here, taxonomically controlled latitudinal variations in shell morphology and composition were investigated in bivalve and gastropod molluscs, brachiopods, and echinoids. Total inorganic content, a proxy for skeletal CaCO3 , decreased with latitude, decreasing seawater temperature, and decreasing seawater carbonate saturation state (for CaCO3 as calcite (Ωcal )) in all taxa. Shell mass decreased with latitude in molluscs and shell inorganic content decreased with latitude in buccinid gastropods. Shell thickness decreased with latitude in buccinid gastropods (excepting the Australian temperate buccinid) and echinoids, but not brachiopods and laternulid clams. In the latter, the polar species had the thickest shell. There was no latitudinal trend in shell thickness within brachiopods. The variation in trends in shell thickness by taxon suggests that in some circumstances ecological factors may override latitudinal trends. Latitudinal gradients may produce effects similar to those of future CO2 -driven ocean acidification on CaCO3 saturation state. Responses to latitudinal trends in temperature and saturation state may therefore be useful in informing predictions of organism responses to ocean acidification over long-term adaptive timescales.

Elevated CO2 enhances aerobic scope of a coral reef fish

The oceans are absorbing excess atmospheric CO2, and this is causing ocean acidification. Surprisingly, one coral reef damselfish exhibits enhanced aerobic performance after living at projected future ocean CO2 levels for 17 days. Identifying both the winners and losers under climate change scenarios is vital to conserving marine biodiversity.

Interactive effects of ocean acidification and rising sea temperatures alter predation rate and predator selectivity in reef fish communities

Ocean warming and acidification are serious threats to marine life. While each stressor alone has been studied in detail, their combined effects on the outcome of ecological interactions are poorly understood. We measured predation rates and predator selectivity of two closely related species of damselfish exposed to a predatory dottyback. We found temperature and CO2 interacted synergistically on overall predation rate, but antagonistically on predator selectivity. Notably, elevated CO2 or temperature alone reversed predator selectivity, but the interaction between the two stressors cancelled selectivity. Routine metabolic rates of the two prey showed strong species differences in tolerance to CO2 and not temperature, but these differences did not correlate with recorded mortality. This highlights the difficulty of linking species-level physiological tolerance to resulting ecological outcomes. This study is the first to document both synergistic and antagonistic effects of elevated CO2 and temperature on a crucial ecological process like predator-prey dynamics.

Increased CO2 stimulates reproduction in a coral reef fish.

Ocean acidification is predicted to negatively impact the reproduction of many marine species, either by reducing fertilization success or diverting energy from reproductive effort. While recent studies have demonstrated how ocean acidification will affect larval and juvenile fishes, little is known about how increasing partial pressure of carbon dioxide (pCO(2)) and decreasing pH might affect reproduction in adult fishes. We investigated the effects of near-future levels of pCO(2) on the reproductive performance of the cinnamon anemonefish, Amphiprion melanopus, from the Great Barrier Reef, Australia. Breeding pairs were held under three CO(2) treatments [Current-day Control (430 μatm), Moderate (584 μatm) and High (1032 μatm)] for a 9-month period that included the summer breeding season. Unexpectedly, increased CO(2) dramatically stimulated breeding activity in this species of fish. Over twice as many pairs bred in the Moderate (67% of pairs) and High (55%) compared to the Control (27%) CO(2) treatment. Pairs in the High CO(2) group produced double the number of clutches per pair and 67% more eggs per clutch compared to the Moderate and Control groups. As a result, reproductive output in the High group was 82% higher than that in the Control group and 50% higher than that in the Moderate group. Despite the increase in reproductive activity, there was no difference in adult body condition among the three treatment groups. There was no significant difference in hatchling length between the treatment groups, but larvae from the High CO(2) group had smaller yolks than Controls. This study provides the first evidence of the potential effects of ocean acidification on key reproductive attributes of marine fishes and, contrary to expectations, demonstrates an initially stimulatory (hormetic) effect in response to increased pCO(2). However, any long-term consequences of increased reproductive effort on individuals or populations remain to be determined.