Ocean acidification and responses to predators: can sensory redundancy reduce the apparent impacts of elevated CO2 on fish?

Carbon dioxide (CO₂) levels in the atmosphere and surface ocean are rising at an unprecedented rate due to sustained and accelerating anthropogenic CO₂ emissions. Previous studies have documented that exposure to elevated CO₂ causes impaired antipredator behavior by coral reef fish in response to chemical cues associated with predation. However, whether ocean acidification will impair visual recognition of common predators is currently unknown. This study examined whether sensory compensation in the presence of multiple sensory cues could reduce the impacts of ocean acidification on antipredator responses. When exposed to seawater enriched with levels of CO₂ predicted for the end of this century (880 μatm CO₂), prey fish completely lost their response to conspecific alarm cues. While the visual response to a predator was also affected by high CO_2, it was not entirely lost. Fish exposed to elevated CO_2, spent less time in shelter than current‐day controls and did not exhibit antipredator signaling behavior (bobbing) when multiple predator cues were present. They did, however, reduce feeding rate and activity levels to the same level as controls. The results suggest that the response of fish to visual cues may partially compensate for the lack of response to chemical cues. Fish subjected to elevated CO₂ levels_, and exposed to chemical and visual predation cues simultaneously, responded with the same intensity as controls exposed to visual cues alone. However, these responses were still less than control fish simultaneously exposed to chemical and visual predation cues. Consequently, visual cues improve antipredator behavior of CO₂ exposed fish, but do not fully compensate for the loss of response to chemical cues. The reduced ability to correctly respond to a predator will have ramifications for survival in encounters with predators in the field, which could have repercussions for population replenishment in acidified oceans.     

Effects of acidification on olfactory-mediated behaviour in freshwater and marine ecosystems: a synthesis

For many aquatic organisms, olfactory-mediated behaviour is essential to the maintenance of numerous fitness-enhancing activities, including foraging, reproduction and predator avoidance. Studies in both freshwater and marine ecosystems have demonstrated significant impacts of anthropogenic acidification on olfactory abilities of fish and macroinvertebrates, leading to impaired behavioural responses, with potentially far-reaching consequences to population dynamics and community structure. Whereas the ecological impacts of impaired olfactory-mediated behaviour may be similar between freshwater and marine ecosystems, the underlying mechanisms are quite distinct. In acidified freshwater, molecular change to chemical cues along with reduced olfaction sensitivity appear to be the primary causes of olfactory-mediated behavioural impairment. By contrast, experiments simulating future ocean acidification suggest that interference of high CO₂ with brain neurotransmitter function is the primary cause for olfactory-mediated behavioural impairment in fish. Different physico-chemical characteristics between marine and freshwater systems are probably responsible for these distinct mechanisms of impairment, which, under globally rising CO₂ levels, may lead to strikingly different consequences to olfaction. While fluctuations in pH may occur in both freshwater and marine ecosystems, marine habitat will remain alkaline despite future ocean acidification caused by globally rising CO₂ levels. In this synthesis, we argue that ecosystem-specific mechanisms affecting olfaction need to be considered for effective management and conservation practices.     

Divergent responses of Atlantic cod to ocean acidification and food limitation

In order to understand the effect of global change on marine fishes, it is imperative to quantify the effects on fundamental parameters such as survival and growth. Larval survival and recruitment of the Atlantic cod (Gadus morhua) were found to be heavily impaired by end‐of‐century levels of ocean acidification. Here, we analysed larval growth among 35–36 days old surviving larvae, along with organ development and ossification of the skeleton. We combined CO₂ treatments (ambient: 503 µatm, elevated: 1,179 µatm) with food availability in order to evaluate the effect of energy limitation in addition to the ocean acidification stressor. As expected, larval size (as a proxy for growth) and skeletogenesis were positively affected by high food availability. We found significant interactions between acidification and food availability. Larvae fed ad libitum showed little difference in growth and skeletogenesis due to the CO₂ treatment. Larvae under energy limitation were significantly larger and had further developed skeletal structures in the elevated CO₂ treatment compared to the ambient CO₂ treatment. However, the elevated CO₂ group revealed impairments in critically important organs, such as the liver, and had comparatively smaller functional gills indicating a mismatch between size and function. It is therefore likely that individual larvae that had survived acidification treatments will suffer from impairments later during ontogeny. Our study highlights important allocation trade‐off between growth and organ development, which is critically important to interpret acidification effects on early life stages of fish.     

Antagonistic effects of ocean acidification and warming on hunting sharks

Ocean warming and acidification alter the physiological performance and behaviour of many small‐bodied fishes, yet the potential interactive effects of these stressors on larger predators remains poorly understood. In particular, the combined effects of elevated temperature on metabolism and of elevated CO₂ on the behaviour of large predators may not only affect their foraging behaviour, but also the communities in which their prey live. We used a factorial design to assess how projected warming and acidification create synergies or antagonisms between physiological and behavioural processes, such as swimming activity and feeding behaviour through odour tracking and vision. Temperature increased swimming activity during feeding, independent of CO₂. Although temperature also increased motivational drive to locate and accept prey, elevated CO₂ negated chemical and visual behavioural responses that enable effective hunting. Fundamental to these effects was the negligible effect of high CO₂ in isolation, but its power to negate the positive effects of temperature when brought in conjunction. The reduced potential to locate prey due to the interactive effects of ocean acidification and warming, in combination with increases in energetic demand, suggests that energetic tradeoffs will be needed for sharks to sustain themselves at an individual and population level in a future ocean.     

Elevated carbon dioxide alters the plasma composition and behaviour of a shark

Increased carbon emissions from fossil fuels are increasing the pCO₂ of the ocean surface waters in a process called ocean acidification. Elevated water pCO₂ can induce physiological and behavioural effects in teleost fishes, although there appear to be large differences in sensitivity between species. There is currently no information available on the possible responses to future ocean acidification in elasmobranch fishes. We exposed small-spotted catsharks (Scyliorhinus canicula) to either control conditions or a year 2100 scenario of 990 μatm pCO₂ for four weeks. We did not detect treatment effects on growth, resting metabolic rate, aerobic scope, skin denticle ultrastructure or skin denticle morphology. However, we found that the elevated pCO₂ group buffered internal acidosis via accumulation with an associated increase in Na⁺, indicating that the blood chemistry remained altered despite the long acclimation period. The elevated pCO₂ group also exhibited a shift in their nocturnal swimming pattern from a pattern of many starts and stops to more continuous swimming. Although CO₂-exposed teleost fishes can display reduced behavioural asymmetry (lateralization), the CO₂-exposed sharks showed increased lateralization. These behavioural effects may suggest that elasmobranch neurophysiology is affected by CO₂, as in some teleosts, or that the sharks detect CO₂ as a constant stressor, which leads to altered behaviour. The potential direct effects of ocean acidification should henceforth be considered when assessing future anthropogenic effects on sharks.     

Ocean acidification boosts reproduction in fish via indirect effects

Ocean acidification affects species populations and biodiversity through direct negative effects on physiology and behaviour. The indirect effects of elevated CO₂ are less well known and can sometimes be counterintuitive. Reproduction lies at the crux of species population replenishment, but we do not know how ocean acidification affects reproduction in the wild. Here, we use natural CO₂ vents at a temperate rocky reef and show that even though ocean acidification acts as a direct stressor, it can indirectly increase energy budgets of fish to stimulate reproduction at no cost to physiological homeostasis. Female fish maintained energy levels by compensation: They reduced activity (foraging and aggression) to increase reproduction. In male fish, increased reproductive investment was linked to increased energy intake as mediated by intensified foraging on more abundant prey. Greater biomass of prey at the vents was linked to greater biomass of algae, as mediated by a fertilisation effect of elevated CO₂ on primary production. Additionally, the abundance and aggression of paternal carers were elevated at the CO₂ vents, which may further boost reproductive success. These positive indirect effects of elevated CO₂ were only observed for the species of fish that was generalistic and competitively dominant, but not for 3 species of subordinate and more specialised fishes. Hence, species that capitalise on future resource enrichment can accelerate their reproduction and increase their populations, thereby altering species communities in a future ocean.

Ocean acidification affects species populations and diversity through direct negative effects on physiology and behavior, but the indirect effects are less clear. Using volcanic carbon dioxide vents as natural analogues of future ocean acidification, this study shows that elevated CO2 can stimulate fish reproduction in the wild through increased food abundance, leading to increased energy budgets at no cost to physiological homeostasis.     

Atlantic cod actively avoid CO<Subscript>2</Subscript> and predator odour,even after long-term CO<Subscript>2</Subscript> exposure

Introduction

The rising atmospheric CO₂ level is continuously driving the dissolution of more CO₂ into the oceans, and some emission scenarios project that the surface waters may reach 1000 μatm by the end of the century. It is not known if fish can detect moderately elevated CO₂ levels, and if they avoid areas with high CO₂. If so, avoidance behaviour to water with high CO₂ could affect movement patterns and migrations of fish in the future. It is also being increasingly recognized that fish behaviour can be altered by exposure to CO₂. Therefore this study investigated how long-term exposure to elevated pCO₂ affects predator avoidance and CO₂ avoidance in juvenile Atlantic cod (Gadus morhua). The fish were exposed to control water or CO₂-enriched water (1000 μatm) for six weeks before being subjected to tests of behaviour.

Results

Despite long term exposure to elevated pCO₂ the cod still strongly avoided the smell of a predator. These data are surprising because several coral reef fish have demonstrated reversal of olfactory responses after CO₂ exposure, turning avoidance of predator cues into preference for predator cues. Fish from both treatment groups also demonstrated strong avoidance of CO₂ when presented with the choice of control or CO₂-acidified water, indicating that habituation to the CO₂ sensory stimuli is negligible.

Conclusions

As Atlantic cod maintained normal behavioural responses to olfactory cues, they may be tolerant to CO₂-induced behavioural changes. The results also suggest that despite the long-term exposure to CO₂-acidified water, the fish still preferred the control water over CO₂-acidified water. Therefore, in the future, fish may alter their movements and migrations in search of waters with a lower CO₂ content.

     

Elevated CO2 affects embryonic development and larval phototaxis in a temperate marine fish

As an effect of anthropogenic CO₂ emissions, the chemistry of the world's oceans is changing. Understanding how this will affect marine organisms and ecosystems are critical in predicting the impacts of this ongoing ocean acidification. Work on coral reef fishes has revealed dramatic effects of elevated oceanic CO₂ on sensory responses and behavior. Such effects may be widespread but have almost exclusively been tested on tropical reef fishes. Here we test the effects elevated CO₂ has on the reproduction and early life history stages of a temperate coastal goby with paternal care by allowing goby pairs to reproduce naturally in an aquarium with either elevated (ca 1400 μatm) CO₂ or control seawater (ca 370 μatm CO₂). Elevated CO₂ did not affect the occurrence of spawning nor clutch size, but increased embryonic abnormalities and egg loss. Moreover, we found that elevated CO₂ significantly affected the phototactic response of newly hatched larvae. Phototaxis is a vision‐related fundamental behavior of many marine fishes, but has never before been tested in the context of ocean acidification. Our findings suggest that ocean acidification affects embryonic development and sensory responses in temperate fishes, with potentially important implications for fish recruitment.     

鱼类对海洋升温与酸化的响应

自工业革命以来,空气中人为排放CO₂量增加,引起温室效应,导致地球表面温度升高和海水升温;同时,由于海-气界面气体交换,大气中CO₂部分溶解于海洋,引起海洋酸化。海洋升温加快鱼体内生化反应和代谢速率,并通过影响生长、觅食和繁殖等生命过程中能量供给,间接影响到鱼类种群分布、群落结构及生态系统的功能。而海水酸化会干扰海洋鱼类仔稚鱼的感觉和行为,增加其被捕食率,并削弱其野外生存能力,可能威胁自然种群补给量。综述了海洋升温、海洋酸化及其两者共同作用对海洋鱼类的影响,为预测鱼类响应全球海洋环境变化的响应趋势提供相关依据。     

Shifting from Right to Left: The Combined Effect of Elevated CO2 and Temperature on Behavioural Lateralization in a Coral Reef Fish

Recent studies have shown that elevated CO₂ can affect the behaviour of larval and juvenile fishes. In particular, behavioural lateralization, an expression of brain functional asymmetries, is affected by elevated CO₂ in both coral reef and temperate fishes. However, the potentially interacting effects of rising temperatures and CO₂ on lateralization are unknown. Here, we tested the combined effect of near-future elevated-CO₂ concentrations (930 µatm) and temperature variation on behavioural lateralization of a marine damselfish, Pomacentrus wardi. Individuals exposed to one of four treatments (two CO₂ levels and two temperatures) were observed in a detour test where they made repeated decisions about turning left or right. Individuals exposed to current CO₂ and ambient temperature levels showed a significant right-turning bias at the population level. This biased was reversed (i.e. to the left side) in fish exposed to the elevated-CO₂ treatment. Increased temperature attenuated this effect, resulting in lower values of relative lateralization. Consequently, rising temperature and elevated CO₂ may have different and interactive effects on behavioural lateralization and therefore future studies on the effect of climate change on brain functions need to consider both these critical variables in order to assess the potential consequences for the ecological interactions of marine fishes.     

Effects of ocean acidification on Antarctic marine organisms: A meta‐analysis

Southern Ocean waters are among the most vulnerable to ocean acidification. The projected increase in the CO₂ level will cause changes in carbonate chemistry that are likely to be damaging to organisms inhabiting these waters. A meta‐analysis was undertaken to examine the vulnerability of Antarctic marine biota occupying waters south of 60°S to ocean acidification. This meta‐analysis showed that ocean acidification negatively affects autotrophic organisms, mainly phytoplankton, at CO₂ levels above 1,000 μatm and invertebrates above 1,500 μatm, but positively affects bacterial abundance. The sensitivity of phytoplankton to ocean acidification was influenced by the experimental procedure used. Natural, mixed communities were more sensitive than single species in culture and showed a decline in chlorophyll a concentration, productivity, and photosynthetic health, as well as a shift in community composition at CO₂ levels above 1,000 μatm. Invertebrates showed reduced fertilization rates and increased occurrence of larval abnormalities, as well as decreased calcification rates and increased shell dissolution with any increase in CO₂ level above 1,500 μatm. Assessment of the vulnerability of fish and macroalgae to ocean acidification was limited by the number of studies available. Overall, this analysis indicates that many marine organisms in the Southern Ocean are likely to be susceptible to ocean acidification and thereby likely to change their contribution to ecosystem services in the future. Further studies are required to address the poor spatial coverage, lack of community or ecosystem‐level studies, and the largely unknown potential for organisms to acclimate and/or adapt to the changing conditions.     

Ocean acidification impairs crab foraging behaviour

Anthropogenic elevation of atmospheric CO₂ is driving global-scale ocean acidification, which consequently influences calcification rates of many marine invertebrates and potentially alters their susceptibility to predation. Ocean acidification may also impair an organism''s ability to process environmental and biological cues. These counteracting impacts make it challenging to predict how acidification will alter species interactions and community structure. To examine effects of acidification on consumptive and behavioural interactions between mud crabs (Panopeus herbstii) and oysters (Crassostrea virginica), oysters were reared with and without caged crabs for 71 days at three pCO₂ levels. During subsequent predation trials, acidification reduced prey consumption, handling time and duration of unsuccessful predation attempt. These negative effects of ocean acidification on crab foraging behaviour more than offset any benefit to crabs resulting from a reduction in the net rate of oyster calcification. These findings reveal that efforts to evaluate how acidification will alter marine food webs should include quantifying impacts on both calcification rates and animal behaviour.     

Rising CO2 concentrations affect settlement behaviour of larval damselfishes

Reef fish larvae actively select preferred benthic habitat, relying on olfactory, visual and acoustic cues to discriminate between microhabitats at settlement. Recent studies show exposure to elevated carbon dioxide (CO₂) impairs olfactory cue recognition in larval reef fishes. However, whether this alters the behaviour of settling fish or disrupts habitat selection is unknown. Here, the effect of elevated CO₂ on larval behaviour and habitat selection at settlement was tested in three species of damselfishes (family Pomacentridae) that differ in their pattern of habitat use: Pomacentrus amboinensis (a habitat generalist), Pomacentrus chrysurus (a rubble specialist) and Pomacentrus moluccensis (a live coral specialist). Settlement-stage larvae were exposed to current-day CO₂ levels or CO₂ concentrations that could occur by 2100 (700 and 850 ppm) based on IPCC emission scenarios. First, pair-wise choice tests were performed using a two-channel flume chamber to test olfactory discrimination between hard coral, soft coral and coral rubble habitats. The habitat selected by settling fish was then compared among treatments using a multi-choice settlement experiment conducted overnight. Finally, settlement timing between treatments was compared across two lunar cycles for one of the species, P. chrysurus. Exposure to elevated CO₂ disrupted the ability of larvae to discriminate between habitat odours in olfactory trials. However, this had no effect on the habitats selected at settlement when all sensory cues were available. The timing of settlement was dramatically altered by CO₂ exposure, with control fish exhibiting peak settlement around the new moon, whereas fish exposed to 850 ppm CO₂ displaying highest settlement rates around the full moon. These results suggest larvae can rely on other sensory information, such as visual cues, to compensate for impaired olfactory ability when selecting settlement habitat at small spatial scales. However, rising CO₂ could cause larvae to settle at unfavourable times, with potential consequences for larval survival and population replenishment.     

Ocean acidification alters foraging behaviour in Dungeness crab through impairment of the olfactory pathway

Crustacean olfaction is fundamental to most aspects of living and communicating in aquatic environments and more broadly, for individual- and population-level success. Accelerated ocean acidification from elevated CO₂ threatens the ability of crabs to detect and respond to important olfactory-related cues. Here, we demonstrate that the ecologically and economically important Dungeness crab (Metacarcinus magister) exhibits reduced olfactory-related antennular flicking responses to a food cue when exposed to near-future CO₂ levels, adding to the growing body of evidence of impaired crab behaviour. Underlying this altered behaviour, we find that crabs have lower olfactory nerve sensitivities (twofold reduction in antennular nerve activity) in response to a food cue when exposed to elevated CO₂. This suggests that near-future CO₂ levels will impact the threshold of detection of food by crabs. We also show that lower olfactory nerve sensitivity in elevated CO₂ is accompanied by a decrease in the olfactory sensory neuron (OSN) expression of a principal chemosensory receptor protein, ionotropic receptor 25a (IR25a) which is fundamental for odorant coding and olfactory signalling cascades. The OSNs also exhibit morphological changes in the form of decreased surface areas of their somata. This study provides the first evidence of the effects of high CO₂ levels at multiple levels of biological organization in marine crabs, linking physiological and cellular changes with whole animal behavioural responses.     

Effects of ocean acidification increase embryonic sensitivity to thermal extremes in Atlantic cod,Gadus morhua

Thermal tolerance windows serve as a powerful tool for estimating the vulnerability of marine species and their life stages to increasing temperature means and extremes. However, it remains uncertain to which extent additional drivers, such as ocean acidification, modify organismal responses to temperature. This study investigated the effects of CO₂‐driven ocean acidification on embryonic thermal sensitivity and performance in Atlantic cod, Gadus morhua, from the Kattegat. Fertilized eggs were exposed to factorial combinations of two PCO₂ conditions (400 μatm vs. 1100 μatm) and five temperature treatments (0, 3, 6, 9 and 12 °C), which allow identifying both lower and upper thermal tolerance thresholds. We quantified hatching success, oxygen consumption (MO₂) and mitochondrial functioning of embryos as well as larval morphometrics at hatch and the abundance of acid–base‐relevant ionocytes on the yolk sac epithelium of newly hatched larvae. Hatching success was high under ambient spawning conditions (3–6 °C), but decreased towards both cold and warm temperature extremes. Elevated PCO₂ caused a significant decrease in hatching success, particularly at cold (3 and 0 °C) and warm (12 °C) temperatures. Warming imposed limitations to MO₂ and mitochondrial capacities. Elevated PCO₂ stimulated MO₂ at cold and intermediate temperatures, but exacerbated warming‐induced constraints on MO₂, indicating a synergistic interaction with temperature. Mitochondrial functioning was not affected by PCO₂. Increased MO₂ in response to elevated PCO₂ was paralleled by reduced larval size at hatch. Finally, ionocyte abundance decreased with increasing temperature, but did not differ between PCO₂ treatments. Our results demonstrate increased thermal sensitivity of cod embryos under future PCO₂ conditions and suggest that acclimation to elevated PCO₂ requires reallocation of limited resources at the expense of embryonic growth. We conclude that ocean acidification constrains the thermal performance window of embryos, which has important implication for the susceptibility of cod to projected climate change.     

Differences in neurochemical profiles of two gadid species under ocean warming and acidification

Background

Exposure to future ocean acidification scenarios may alter the behaviour of marine teleosts through interference with neuroreceptor functioning. So far, most studies investigated effects of ocean acidification on the behaviour of fish, either isolated or in combination with environmental temperature. However, only few physiological studies on this issue were conducted despite the putative neurophysiological origin of the CO₂-induced behavioural changes. Here, we present the metabolic consequences of long-term exposure to projected ocean acidification (396–548 μatm PCO₂ under control and 915–1272 μatm under treatment conditions) and parallel warming in the brain of two related fish species, polar cod (Boreogadus saida, exposed to 0 °C, 3 °C, 6 °C and 8 °C) and Atlantic cod (Gadus morhua, exposed to 3 °C, 8 °C, 12 °C and 16 °C). It has been shown that B. saida is behaviourally vulnerable to future ocean acidification scenarios, while G. morhua demonstrates behavioural resilience.

Results

We found that temperature alters brain osmolyte, amino acid, choline and neurotransmitter concentrations in both species indicating thermal responses particularly in osmoregulation and membrane structure. In B. saida, changes in amino acid and osmolyte metabolism at the highest temperature tested were also affected by CO₂, possibly emphasizing energetic limitations. We did not observe changes in neurotransmitters, energy metabolites, membrane components or osmolytes that might serve as a compensatory mechanism against CO₂ induced behavioural impairments. In contrast to B. saida, such temperature limitation was not detected in G. morhua; however, at 8 °C, CO₂ induced an increase in the levels of metabolites of the glutamate/GABA-glutamine cycle potentially indicating greater GABAergic activity in G.morhua. Further, increased availability of energy-rich substrates was detected under these conditions.

Conclusions

Our results indicate a change of GABAergic metabolism in the nervous system of Gadus morhua close to the optimum of the temperature range. Since a former study showed that juvenile G. morhua might be slightly more behaviourally resilient to CO₂ at this respective temperature, we conclude that the observed change of GABAergic metabolism could be involved in counteracting OA induced behavioural changes. This may serve as a fitness advantage of this respective species compared to B. saida in a future warmer, more acidified polar ocean.

     

Elevated CO2 impairs olfactory‐mediated neural and behavioral responses and gene expression in ocean‐phase coho salmon (Oncorhynchus kisutch)

Elevated concentrations of CO₂ in seawater can disrupt numerous sensory systems in marine fish. This is of particular concern for Pacific salmon because they rely on olfaction during all aspects of their life including during their homing migrations from the ocean back to their natal streams. We investigated the effects of elevated seawater CO₂ on coho salmon (Oncorhynchus kisutch) olfactory‐mediated behavior, neural signaling, and gene expression within the peripheral and central olfactory system. Ocean‐phase coho salmon were exposed to three levels of CO₂, ranging from those currently found in ambient marine water to projected future levels. Juvenile coho salmon exposed to elevated CO₂ levels for 2 weeks no longer avoided a skin extract odor that elicited avoidance responses in coho salmon maintained in ambient CO₂ seawater. Exposure to these elevated CO₂ levels did not alter odor signaling in the olfactory epithelium, but did induce significant changes in signaling within the olfactory bulb. RNA‐Seq analysis of olfactory tissues revealed extensive disruption in expression of genes involved in neuronal signaling within the olfactory bulb of salmon exposed to elevated CO₂, with lesser impacts on gene expression in the olfactory rosettes. The disruption in olfactory bulb gene pathways included genes associated with GABA signaling and maintenance of ion balance within bulbar neurons. Our results indicate that ocean‐phase coho salmon exposed to elevated CO₂ can experience significant behavioral impairments likely driven by alteration in higher‐order neural signal processing within the olfactory bulb. Our study demonstrates that anadromous fish such as salmon may share a sensitivity to rising CO₂ levels with obligate marine species suggesting a more wide‐scale ecological impact of ocean acidification.     

Ocean acidification boosts larval fish development but reduces the window of opportunity for successful settlement

Locating appropriate settlement habitat is a crucial step in the life cycle of most benthic marine animals. In marine fish, this step involves the use of multiple senses, including audition, olfaction and vision. To date, most investigations of larval fish audition focus on the hearing thresholds to various frequencies of sounds without testing an ecological response to such sounds. Identifying responses to biologically relevant sounds at the development stage in which orientation is most relevant is fundamental. We tested for the existence of ontogenetic windows of reception to sounds that could act as orientation cues with a focus on vulnerability to alteration by human impacts. Here we show that larvae of a catadromous fish species (barramundi, Lates calcarifer) were attracted towards sounds from settlement habitat during a surprisingly short ontogenetic window of approximately 3 days. Yet, this auditory preference was reversed in larvae reared under end-of-century levels of elevated CO₂, such that larvae are repelled from cues of settlement habitat. These future conditions also reduced the swimming speeds and heightened the anxiety levels of barramundi. Unexpectedly, an acceleration of development and onset of metamorphosis caused by elevated CO₂ were not accompanied by the earlier onset of attraction towards habitat sounds. This mismatch between ontogenetic development and the timing of orientation behaviour may reduce the ability of larvae to locate habitat or lead to settlement in unsuitable habitats. The misinterpretation of key orientation cues can have implications for population replenishment, which are only exacerbated when ontogenetic development decouples from the specific behaviours required for location of settlement habitats.     

Temperature and CO2 additively regulate physiology,morphology and genomic responses of larval sea urchins,Strongylocentrotus purpuratus

Ocean warming and ocean acidification, both consequences of anthropogenic production of CO₂, will combine to influence the physiological performance of many species in the marine environment. In this study, we used an integrative approach to forecast the impact of future ocean conditions on larval purple sea urchins (Strongylocentrotus purpuratus) from the northeast Pacific Ocean. In laboratory experiments that simulated ocean warming and ocean acidification, we examined larval development, skeletal growth, metabolism and patterns of gene expression using an orthogonal comparison of two temperature (13°C and 18°C) and pCO₂ (400 and 1100 μatm) conditions. Simultaneous exposure to increased temperature and pCO₂ significantly reduced larval metabolism and triggered a widespread downregulation of histone encoding genes. pCO₂ but not temperature impaired skeletal growth and reduced the expression of a major spicule matrix protein, suggesting that skeletal growth will not be further inhibited by ocean warming. Importantly, shifts in skeletal growth were not associated with developmental delay. Collectively, our results indicate that global change variables will have additive effects that exceed thresholds for optimized physiological performance in this keystone marine species.