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Behaviour and sensory performance of marine fishes are impaired at CO sub(2) levels projected to occur in the ocean in the next 50-100 years, and there is limited potential for within-generation acclimation to elevated CO sub(2) (refs , ). However, whether fish behaviour can acclimate or adapt to elevated CO sub(2) over multiple generations remains unanswered. We tested for transgenerational acclimation of reef fish olfactory preferences and behavioural lateralization at moderate (656 mu atm) and high (912 mu atm) end-of-century CO sub(2) projections. Juvenile spiny damselfish, Acanthochromis polyacanthus, from control parents (446 mu atm) exhibited an innate avoidance to chemical alarm cue (CAC) when reared in control conditions. In contrast, juveniles lost their innate avoidance of CAC and even became strongly attracted to CAC when reared at elevated CO sub(2) levels. Juveniles from parents maintained at mid-CO sub(2) and high-CO sub(2) levels also lost their innate avoidance of CAC when reared in elevated CO sub(2), demonstrating no capacity for transgenerational acclimation of olfactory responses. Behavioural lateralization was also disrupted for juveniles reared under elevated CO sub(2), regardless of parental conditioning. Our results show minimal potential for transgenerational acclimation in this fish, suggesting that genetic adaptation will be necessary to overcome the effects of ocean acidification on behaviour.

Predicting the impacts of climate change to biological systems requires an understanding of the ability for species to acclimate to the projected environmental change through phenotypic plasticity. Determining the effects of higher temperatures on individual performance is made more complex by the potential for environmental conditions experienced in previous and current generations to independently affect phenotypic responses to high temperatures. We used a model coral reef fish (Acanthochromis polyacanthus) to investigate the influence of thermal conditions experienced by two generations on reproductive output and the quality of offspring produced by adults. We found that more gradual warming over two generations, +1.5°C in the first generation and then +3.0°C in the second generation, resulted in greater plasticity of reproductive attributes, compared to fish that experienced the same increase in one generation. Reproduction ceased at the projected future summer temperature (31.5°C) when fish experienced +3.0°C for two generations. Additionally, we found that transgenerational plasticity to +1.5°C induced full restoration of thermally affected reproductive and offspring attributes, which was not possible with developmental plasticity alone. Our results suggest that transgenerational effects differ depending on the absolute thermal change and in which life stage the thermal change is experienced.

Ocean acidification impairs reef fish behaviour. This study shows offspring of spiny damselfish sensitive to high CO 2 levels have different brain molecular responses to those of tolerant individuals, suggesting individual variation may allow adaptation. The impact of ocean acidification on marine ecosystems will depend on species capacity to adapt 1 , 2 . Recent studies show that the behaviour of reef fishes is impaired at projected CO 2 levels 3 , 4 ; however, individual variation exists that might promote adaptation. Here, we show a clear signature of parental sensitivity to high CO 2 in the brain molecular phenotype of juvenile spiny damselfish, Acanthochromis polyacanthus , primarily driven by circadian rhythm genes. Offspring of CO 2 -tolerant and CO 2 -sensitive parents were reared at near-future CO 2 (754 μatm) or present-day control levels (414 μatm). By integrating 33 brain transcriptomes and proteomes with a de novo assembled genome we investigate the molecular responses of the fish brain to increased CO 2 and the expression of parental tolerance to high CO 2 in the offspring molecular phenotype. Exposure to high CO 2 resulted in differential regulation of 173 and 62 genes and 109 and 68 proteins in the tolerant and sensitive groups, respectively. Importantly, the majority of differences between offspring of tolerant and sensitive parents occurred in high CO 2 conditions. This transgenerational molecular signature suggests that individual variation in CO 2 sensitivity could facilitate adaptation of fish populations to ocean acidification.

Climate change is predicted to increase ocean temperatures and alter plankton communities that are food for many marine fishes. To examine the effects of increased sea surface temperature and fluctuating food levels on reef-fish reproduction, breeding pairs of the coral reef damselfishAcanthochromis polyacanthuswere maintained for a full summer breeding season in an orthogonal experiment comprising 3 temperature and 2 food levels. Water temperatures were the current-day average summer temperature for the collection location (28.5°C) and temperatures predicted to become close to the average for this region over the next 50 to 100 yr (30.0 and 31.5°C). Pairs were fed either a high or low quantity diet based on average and minimum feeding rates in the wild. Both water temperature and food supply affected reproductive output. Fewer pairs bred at elevated water temperatures and no pairs reproduced at either of the higher temperatures on the lower quantity diet. Furthermore, eggs produced were smaller at 30.0 and 31.5°C compared to those at 28.5°C. Histological analysis of the gonads and steroid hormone measurement did not reveal any apparent differences in patterns of oogenesis among treatments. However, spermatogenesis was reduced at high temperatures despite some increases in plasma androgen levels. Reduced breeding rate at warmer temperatures combined with reduced sperm production indicates the potential for significant declines inA. polyacanthuspopulations as the ocean warms.

Reduced water quality, in particular increases in suspended sediments, has been linked to declines in fish abundance on coral reefs. Changes in gill structure induced by suspended sediments have been hypothesized to impair gill function and may provide a mechanistic basis for the observed declines; yet, evidence for this is lacking. We exposed juveniles of three reef fish species (Amphiprion melanopus, Amphiprion percula and Acanthochromis polyacanthus) to suspended sediments (0–180 mg l−1) for 7 days and examined changes in gill structure and metabolic performance (i.e. oxygen consumption). Exposure to suspended sediments led to shorter gill lamellae in A. melanopus and A. polyacanthus and reduced oxygen diffusion distances in all three species. While A. melanopus exhibited impaired oxygen uptake after suspended sediment exposure, i.e. decreased maximum and increased resting oxygen consumption rates resulting in decreased aerobic scope, the oxygen consumption rates of the other two species remained unaffected. These findings imply that species sensitive to changes in gill structure such as A. melanopus may decline in abundance as reefs become more turbid, whereas species that are able to maintain metabolic performance despite suspended sediment exposure, such as A. polyacanthus or A. percula, may be able to persist or gain a competitive advantage.

Understanding the capacity of organisms to cope with projected global warming through acclimation and adaptation is critical to predicting their likely future persistence. While recent research has shown that developmental acclimation of metabolic attributes to ocean warming is possible, our understanding of the plasticity of key fitness-associated traits, such as reproductive performance, is lacking. We show that while the reproductive ability of a tropical reef fish is highly sensitive to increases in water temperature, reproductive capacity at +1.5°C above present-day was improved to match fish maintained at present-day temperatures when fish complete their development at the higher temperature. However, reproductive acclimation was not observed in fish reared at +3.0°C warmer than present-day, suggesting limitations to the acclimation possible within one generation. Surprisingly, the improvements seen in reproduction were not predicted by the oxygen- and capacity-limited thermal tolerance hypothesis. Specifically, pairs reared at +1.5°C, which showed the greatest capacity for reproductive acclimation, exhibited no acclimation of metabolic attributes. Conversely, pairs reared at +3.0°C, which exhibited acclimation in resting metabolic rate, demonstrated little capacity for reproductive acclimation. Our study suggests that understanding the acclimation capacity of reproductive performance will be critically important to predicting the impacts of climate change on biological systems.

Examining the functional response of predators can provide insight into the role of predation in structuring prey populations and ecological communities. This study explored feeding behaviour and functional responses of planktivorous damselfishes when offered captive reared larvae of crown-of-thorns starfish, Acanthaster sp., with the aim of determining whether these predators could ever play a role in moderating outbreaks of Acanthaster sp. We examined predatory behaviour of 11 species of planktivorous damselfish, testing: (1) the relationship between predator size and predation rate, both within and among fish species; (2) consumption rates on larvae of Acanthaster sp. versus larvae of a common, co-occurring coral reef asteroid Linckia laevigata ; (3) maximal feeding rates upon both Acanthaster sp. and L. laevigata ; and (4) functional responses of planktivorous fishes to increasing densities of Acanthaster sp. Consumption rates of crown-of-thorns larvae by damselfishes were independent of predator size; however, there was a significant negative relationship between predator size and consumption rate of L. laevigata , when pooling across all predatory species. Some damselfishes, including Acanthochromis polyacanthus and Amblyglyphidodon curacao , consumed larval Acanthaster sp. at a greater rate than for L. laevigata. Most predatory species (all except A. curacao and Pomacentrus amboinensis ) exhibited a Type II functional response whereby the increasing feeding rate decelerated with increasing prey density. In addition to revealing that a wide range of planktivorous fishes can prey upon larvae of Acanthaster sp., these data suggest that planktivorous damselfishes may have the capacity to buffer against population fluctuations of Acanthaster sp. Importantly, predators with Type II functional responses often contribute to stability of prey populations, though planktivorous fishes may be swamped by an abnormally high influx of larvae, potentially contributing to the characteristic population fluctuations of Acanthaster sp.

Many “client” coral reef fishes have their ectoparasites removed by the “cleaner” wrasse Labroides dimidiatus in mutualistic interactions. Clients regularly receiving cleaning services reportedly benefit from increased growth and cognitive performance, but the underlying physiological changes that covary with such benefits are unknown. Here, we tested whether reduced access to cleaning services affects physiological state in two species of damselfish, Amblyglyphidodon curacao and Acanthochromis polyacanthus. We performed an in situ removal experiment on the Great Barrier Reef, Australia, whereby 47% of cleaners on a natural reef were removed. Since cleaners occupy defined territories (called “cleaning stations”), this removal created areas where small, resident clients, including A. polyacanthus and A. amblyglyphidodon, had no access to cleaning services. One month following cleaner removal, we measured body condition and collected blood samples from both damselfish species from territories with and without access to cleaners. Blood was used for estimating haematocrit levels, hormonal analyses, and immune cell counts. We tested for correlations among all these parameters to explore potential trade-offs in terms of growth, aerobic capacity, immune activation, and/or reproduction as a result of the loss of cleaning benefits. In both species, we found that fish without access to cleaners had lower haematocrit, testosterone levels, and lymphocyte counts than fish with access. There were no significant changes in fish body condition, leukocytes, granulocytes, or plasma cortisol levels between fish with access to cleaners or not. However, testosterone levels correlated negatively with the proportion of granulocytes in the blood of fish with access to cleaners. Our results suggest that even a relatively short-term reduction in access to cleaning services can have negative physiological outcomes for clients. Thus, the presence of cleaners on coral reefs appears to have important benefits for coral reef fish community health.

The relationships among animal form, function and performance are complex, and vary across environments. Therefore, it can be difficult to identify morphological and/or physiological traits responsible for enhancing performance in a given habitat. In fishes, differences in swimming performance across water flow gradients are related to morphological variation among and within species. However, physiological traits related to performance have been less well studied. We experimentally reared juvenile damselfish, Acanthochromis polyacanthus, under different water flow regimes to test 1) whether aspects of swimming physiology and morphology show plastic responses to water flow, 2) whether trait divergence correlates with swimming performance and 3) whether flow environment relates to performance differences observed in wild fish. We found that maximum metabolic rate, aerobic scope and blood haematocrit were higher in wave-reared fish compared to fish reared in low water flow. However, pectoral fin shape, which tends to correlate with sustained swimming performance, did not differ between rearing treatments or collection sites. Maximum metabolic rate was the best overall predictor of individual swimming performance; fin shape and fish total length were 3.3 and 3.7 times less likely than maximum metabolic rate to explain differences in critical swimming speed. Performance differences induced in fish reared in different flow environments were less pronounced than in wild fish but similar in direction. Our results suggest that exposure to water motion induces plastic physiological changes which enhance swimming performance in A. polyacanthus. Thus, functional relationships between fish morphology and performance across flow habitats should also consider differences in physiology.

Increased levels of dissolved carbon dioxide (CO₂) drive ocean acidification and have been predicted to increase the energy use of marine fishes via physiological and behavioural mechanisms. This notion is based on a theoretical framework suggesting that detrimental effects on energy use are caused by plasma acid–base disruption in response to hypercapnic acidosis, potentially in combination with a malfunction of the gamma aminobutyric acid type A (GABAA) receptors in the brain. However, the existing empirical evidence testing these effects primarily stems from studies that exposed fish to elevated CO₂ for a few days and measured a small number of traits. We investigated a range of energetic traits in juvenile spiny chromis damselfish (Acanthochromis polyacanthus) over 3 months of acclimation to projected end-of-century CO₂ levels (~ 1000 µatm). Somatic growth and otolith size and shape were unaffected by the CO₂ treatment across 3 months of development in comparison with control fish (~ 420 µatm). Swimming activity during behavioural assays was initially higher in the elevated CO₂ group, but this effect dissipated within ~ 25 min following handling. The transient higher activity of fish under elevated CO₂ was not associated with a detectable difference in the rate of oxygen uptake nor was it mediated by GABAA neurotransmitter interference because treatment with a GABAA antagonist (gabazine) did not abolish the CO₂ treatment effect. These findings contrast with several short-term studies by suggesting that end-of-century levels of CO₂ may have negligible direct effects on the energetics of at least some species of fish.