Impacts of ocean acidification on respiratory gas exchange and acid–base balance in a marine teleost, Opsanus beta

The oceanic carbonate system is changing rapidly due to rising atmospheric CO₂, with current levels expected to rise to between 750 and 1,000 μatm by 2100, and over 1,900 μatm by year 2300. The effects of elevated CO₂ on marine calcifying organisms have been extensively studied; however, effects of imminent CO₂ levels on teleost acid–base and respiratory physiology have yet to be examined. Examination of these physiological processes, using a paired experimental design, showed that 24 h exposure to 1,000 and 1,900 μatm CO₂ resulted in a characteristic compensated respiratory acidosis response in the gulf toadfish (Opsanus beta). Time course experiments showed the onset of acidosis occurred after 15 min of exposure to 1,900 and 1,000 μatm CO₂, with full compensation by 2 and 4 h, respectively. 1,900-μatm exposure also resulted in significantly increased intracellular white muscle pH after 24 h. No effect of 1,900 μatm was observed on branchial acid flux; however, exposure to hypercapnia and HCO₃ ⁻ free seawater compromised compensation. This suggests branchial HCO₃ ⁻ uptake rather than acid extrusion is part of the compensatory response to low-level hypercapnia. Exposure to 1,900 μatm resulted in downregulation in branchial carbonic anhydrase and slc4a2 expression, as well as decreased Na⁺/K⁺ ATPase activity after 24 h of exposure. Infusion of bovine carbonic anhydrase had no effect on blood acid–base status during 1,900 μatm exposures, but eliminated the respiratory impacts of 1,000 μatm CO₂. The results of the current study clearly show that predicted near-future CO₂ levels impact respiratory gas transport and acid–base balance. While the full physiological impacts of increased blood HCO₃ ⁻ are not known, it seems likely that chronically elevated blood HCO₃ ⁻ levels could compromise several physiological systems and furthermore may explain recent reports of increased otolith growth during exposure to elevated CO₂

Review of climate change impacts on marine fish and shellfish around the UK and Ireland

1. Recent and projected future changes in the temperature and chemistry of marine waters around the UK and Ireland are having, and will in the future have, effects on the phenology, productivity and distribution of marine fish and shellfish. However, the overall consequences are still hard to predict because behaviour, genetic adaptation, habitat dependency and the impacts of fishing on species, result in complex species’ responses that may be only partially explained by simple climate envelope predictions.
2. There is a broad body of evidence that climatic fluctuations are playing an important role in changing fish distributions and abundances, which is discernible against the background of trends in abundance due to fishing. During warm periods, southern species have tended to become more prominent and northern species less abundant. However, the changes in distribution are often more complicated than might be expected from a simple climate envelope approach, partly due to ocean circulation patterns which create invasion routes for southern water species into the North Sea from the south and from the north via the continental shelf west of Britain and Ireland.
3. The eventual population-scale impacts of ocean acidification on fish and shellfish are currently very difficult to predict. However, the scant evidence suggests that indirect food web effects arising from the enhanced sensitivity of calcifying planktonic organisms may be important, and the direct effect on fish sensory systems leading to subtle influences on behaviour with possible population-level implications are possible.
4. In British waters, the lesser sandeel (Ammodytes marinus) is identified as being at particular risk from climate change. Owing to its strict association with coarse sandy sediments it is unable to adapt its distribution to compensate for warming sea temperatures. Sandeels are a key link in the food web, linking primary and zooplankton production to top predators.

Effects of ocean acidification on visual risk assessment in coral reef fishes

Summary

1. With the global increase in CO₂ emissions, there is a pressing need for studies aimed at understanding the effects of ocean acidification on marine ecosystems. Several studies have reported that exposure to CO₂ impairs chemosensory responses of juvenile coral reef fishes to predators. Moreover, one recent study pointed to impaired responses of reef fish to auditory cues that indicate risky locations. These studies suggest that altered behaviour following exposure to elevated CO₂ is caused by a systemic effect at the neural level.

2. The goal of our experiment was to test whether juvenile damselfish Pomacentrus amboinensis exposed to different levels of CO₂ would respond differently to a potential threat, the sight of a large novel coral reef fish, a spiny chromis, Acanthochromis polyancanthus, placed in a watertight bag.

3. Juvenile damselfish exposed to 440 (current day control), 550 or 700 μatm CO₂ did not differ in their response to the chromis. However, fish exposed to 850 μatm showed reduced antipredator responses; they failed to show the same reduction in foraging, activity and area use in response to the chromis. Moreover, they moved closer to the chromis and lacked any bobbing behaviour typically displayed by juvenile damselfishes in threatening situations.

4. Our results are the first to suggest that response to visual cues of risk may be impaired by CO₂ and provide strong evidence that the multi-sensory effects of CO₂ may stem from systematic effects at the neural level.

Effects of ocean acidification on statolith calcification and prey capture in early life cuttlefish, Sepia officinalis

The influence of elevated seawater pCO2 on statolith calcification and prey capture was investigated in the early life stages of the common cuttlefish, Sepia officinalis. Cuttlefish were reared at 15°C and 35 psu in a flow-through seawater system under three pCO2 conditions, 700 µatm (control), 1400 µatm , and 4000 µatm during 63 days in June to August 2009. Both, embryonic and hatchling cuttlefish raised under 4000 µatm showed significantly reduced statolith calcification, whereas those grown under control and 1400 µatm did not. Reduced calcification was demonstrated by comparing 18 transects characterizing the anterior surface of the statoliths. The statolith morphometrics that showed the most remarkable changes between the different pCO2 conditions were total statolith length, rostrum transects, wing area and statolith weight. Statolith microstructure was significantly affected by irregularly arranged statoconia, which were typical in the statolith wing area, replacing the highly compact and well-arranged crystals in normal growing statoliths. This abnormal crystal structure can have profound effects on statolith density and consequently on its normal functioning as a tool for buoyancy, acceleration and movement. Changes in statolith morphology and microstructure may influence the prey capture efficiency of the early life cuttlefish. At 4000 µatm they showed a reduced ability to capture prey and were not able to successfully launch attacks against prey organisms. In order to verify these observations, a second experiment was conducted over 85 days in May to August 2010. Preliminary results showed that statolith morphology and microstructure differed again in the 4000 µatm group. On the other hand, prey capture ability of the hatchlings showed recovery during the experiment, indicating a possible acclimation.

Effects of ocean acidification on learning in coral reef fishes

Ocean acidification has the potential to cause dramatic changes in marine ecosystems. Larval damselfish exposed to concentrations of CO₂ predicted to occur in the mid- to late-century show maladaptive responses to predator cues. However, there is considerable variation both within and between species in CO₂ effects, whereby some individuals are unaffected at particular CO₂ concentrations while others show maladaptive responses to predator odour. Our goal was to test whether learning via chemical or visual information would be impaired by ocean acidification and ultimately, whether learning can mitigate the effects of ocean acidification by restoring the appropriate responses of prey to predators. Using two highly efficient and widespread mechanisms for predator learning, we compared the behaviour of pre-settlement damselfish Pomacentrus amboinensis that were exposed to 440 µatm CO₂ (current day levels) or 850 µatm CO₂, a concentration predicted to occur in the ocean before the end of this century. We found that, regardless of the method of learning, damselfish exposed to elevated CO₂ failed to learn to respond appropriately to a common predator, the dottyback, Pseudochromis fuscus. To determine whether the lack of response was due to a failure in learning or rather a short-term shift in trade-offs preventing the fish from displaying overt antipredator responses, we conditioned 440 or 700 µatm-CO₂ fish to learn to recognize a dottyback as a predator using injured conspecific cues, as in Experiment 1. When tested one day post-conditioning, CO₂ exposed fish failed to respond to predator odour. When tested 5 days post-conditioning, CO₂ exposed fish still failed to show an antipredator response to the dottyback odour, despite the fact that both control and CO₂-treated fish responded to a general risk cue (injured conspecific cues). These results indicate that exposure to CO₂ may alter the cognitive ability of juvenile fish and render learning ineffective.

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.

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

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 function. Impaired olfactory function makes larval fish attracted to odours they normally avoid, including ones from predators and unfavourable habitats. These behavioural alterations have significant effects on mortality that may have far-reaching implications for population replenishment, community structure and ecosystem function. 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.

Effect of ocean acidification on early life stages of Atlantic herring (Clupea harengus L.)(update)

Due to atmospheric accumulation of anthropogenic CO₂ the partial pressure of carbon dioxide (pCO₂) in surface seawater increases and the pH decreases. This process known as ocean acidification might have severe effects on marine organisms and ecosystems. The present study addresses the effect of ocean acidification on early developmental stages, the most sensitive stages in life history, of the Atlantic herring (Clupea harengus L.). Eggs of the Atlantic herring were fertilized and incubated in artificially acidified seawater (pCO₂ 1260, 1859, 2626, 2903, 4635 μatm) and a control treatment (pCO₂ 480 μatm) until the main hatch of herring larvae occurred. The development of the embryos was monitored daily and newly hatched larvae were sampled to analyze their morphometrics, and their condition by measuring the RNA/DNA ratios. Elevated pCO₂ neither affected the embryogenesis nor the hatch rate. Furthermore the results showed no linear relationship between pCO₂ and total length, dry weight, yolk sac area and otolith area of the newly hatched larvae. For pCO₂ and RNA/DNA ratio, however, a significant negative linear relationship was found. The RNA concentration at hatching was reduced at higher pCO₂ levels, which could lead to a decreased protein biosynthesis. The results indicate that an increased pCO₂ can affect the metabolism of herring embryos negatively. Accordingly, further somatic growth of the larvae could be reduced. This can have consequences for the larval fish, since smaller and slow growing individuals have a lower survival potential due to lower feeding success and increased predation mortality. The regulatory mechanisms necessary to compensate for effects of hypercapnia could therefore lead to lower larval survival. Since the recruitment of fish seems to be determined during the early life stages, future research on the factors influencing these stages are of great importance in fisheries science.

Effects of climate change on fish reproduction and early life history stages

Seasonal change in temperature has a profound effect on reproduction in fish. Increasing temperatures cue reproductive development in spring-spawning species, and falling temperatures stimulate reproduction in autumn-spawners. Elevated temperatures truncate spring spawning, and delay autumn spawning. Temperature increases will affect reproduction, but the nature of these effects will depend on the period and amplitude of the increase and range from phase-shifting of spawning to complete inhibition of reproduction. This latter effect will be most marked in species that are constrained in their capacity to shift geographic range. Studies from a range of taxa, habitats and temperature ranges all show inhibitory effects of elevated temperature albeit about different environmental set points. The effects are generated through the endocrine system, particularly through the inhibition of ovarian oestrogen production. Larval fishes are usually more sensitive than adults to environmental fluctuations, and might be especially vulnerable to climate change. In addition to direct effects on embryonic duration and egg survival, temperature also influences size at hatching, developmental rate, pelagic larval duration and survival. A companion effect of marine climate change is ocean acidification, which may pose a significant threat through its capacity to alter larval behaviour and impair sensory capabilities. This in turn impacts on population replenishment and connectivity patterns of marine fishes.

Severe tissue damage in Atlantic cod larvae under increasing ocean acidification

Ocean acidification, caused by increasing atmospheric concentrations of CO₂, is one of the most critical anthropogenicthreats to marine life. Changes in seawater carbonate chemistry have the potential to disturb calcification, acid–base regulation, blood circulation and respiration, as well as the nervous system of marine organisms, leading to long-term effects such as reduced growth rates and reproduction. In teleost fishes, early life-history stages are particularly vulnerable as they lack specialized internal pH regulatory mechanisms. So far, impacts of relevant CO₂ concentrations on larval fish have been found in behaviour and otolith size, mainly in tropical, non-commercial species. Here we show detrimental effects of ocean acidification on the development of a mass-spawning fish species of high commercial importance. We reared Atlantic cod larvae at three levels of CO₂, (1) present day, (2) end of next century and (3) an extreme, coastal upwelling scenario, in a long-term ( 2.5 1/2 months) mesocosm experiment. Exposure to CO₂ resulted in severe to lethal tissue damage in many internal organs, with the degree of damage increasing with CO₂ concentration. As larval survival is the bottleneck to recruitment, ocean acidification has the potential to act as an additional source of natural mortality, affecting populations of already exploited fish stocks.