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。     

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.     

Ocean acidification alters temperature and salinity preferences in larval fish

Ocean acidification alters the way in which animals perceive and respond to their world by affecting a variety of senses such as audition, olfaction, vision and pH sensing. Marine species rely on other senses as well, but we know little of how these might be affected by ocean acidification. We tested whether ocean acidification can alter the preference for physicochemical cues used for dispersal between ocean and estuarine environments. We experimentally assessed the behavioural response of a larval fish (Lates calcarifer) to elevated temperature and reduced salinity, including estuarine water of multiple cues for detecting settlement habitat. Larval fish raised under elevated CO₂ concentrations were attracted by warmer water, but temperature had no effect on fish raised in contemporary CO₂ concentrations. In contrast, contemporary larvae were deterred by lower salinity water, where CO₂-treated fish showed no such response. Natural estuarine water—of higher temperature, lower salinity, and containing estuarine olfactory cues—was only preferred by fish treated under forecasted high CO₂ conditions. We show for the first time that attraction by larval fish towards physicochemical cues can be altered by ocean acidification. Such alterations to perception and evaluation of environmental cues during the critical process of dispersal can potentially have implications for ensuing recruitment and population replenishment. Our study not only shows that freshwater species that spend part of their life cycle in the ocean might also be affected by ocean acidification, but that behavioural responses towards key physicochemical cues can also be negated through elevated CO₂ from human emissions.     

Effect of ocean acidification on growth and otolith condition of juvenile scup,Stenotomus chrysops

Increasing amounts of atmospheric carbon dioxide (CO₂) from human industrial activities are causing changes in global ocean carbonate chemistry, resulting in a reduction in pH, a process termed “ocean acidification.” It is important to determine which species are sensitive to elevated levels of CO₂ because of potential impacts to ecosystems, marine resources, biodiversity, food webs, populations, and effects on economies. Previous studies with marine fish have documented that exposure to elevated levels of CO₂ caused increased growth and larger otoliths in some species. This study was conducted to determine whether the elevated partial pressure of CO₂ (pCO₂) would have an effect on growth, otolith (ear bone) condition, survival, or the skeleton of juvenile scup, Stenotomus chrysops, a species that supports both important commercial and recreational fisheries. Elevated levels of pCO₂ (1200–2600 μatm) had no statistically significant effect on growth, survival, or otolith condition after 8 weeks of rearing. Field data show that in Long Island Sound, where scup spawn, in situ levels of pCO₂ are already at levels ranging from 689 to 1828 μatm due to primary productivity, microbial activity, and anthropogenic inputs. These results demonstrate that ocean acidification is not likely to cause adverse effects on the growth and survivability of every species of marine fish. X‐ray analysis of the fish revealed a slightly higher incidence of hyperossification in the vertebrae of a few scup from the highest treatments compared to fish from the control treatments. Our results show that juvenile scup are tolerant to increases in seawater pCO_2, possibly due to conditions this species encounters in their naturally variable environment and their well‐developed pH control mechanisms.     

Contrasting effects of ocean acidification on reproduction in reef fishes

Differences in the sensitivity of marine species to ocean acidification will influence the structure of marine communities in the future. Reproduction is critical for individual and population success, yet is energetically expensive and could be adversely affected by rising CO₂ levels in the ocean. We investigated the effects of projected future CO₂ levels on reproductive output of two species of coral reef damselfish, Amphiprion percula and Acanthochromis polyacanthus. Adult breeding pairs were maintained at current-day control (446 μatm), moderate (652 μatm) or high CO₂ (912 μatm) for a 9-month period that included the summer breeding season. The elevated CO₂ treatments were consistent with CO₂ levels projected by 2100 under moderate (RCP6) and high (RCP8) emission scenarios. Reproductive output increased in A. percula, with 45–75 % more egg clutches produced and a 47–56 % increase in the number of eggs per clutch in the two elevated CO₂ treatments. In contrast, reproductive output decreased at high CO₂ in Ac. polyacanthus, with approximately one-third as many clutches produced compared with controls. Egg survival was not affected by CO₂ for A. percula, but was greater in elevated CO₂ for Ac. polyacanthus. Hatching success was also greater for Ac. polyacanthus at elevated CO₂, but there was no effect of CO₂ treatments on offspring size. Despite the variation in reproductive output, body condition of adults did not differ between control and CO₂ treatments in either species. Our results demonstrate different effects of high CO₂ on fish reproduction, even among species within the same family. A greater understanding of the variation in effects of ocean acidification on reproductive performance is required to predict the consequences for future populations of marine organisms.     

Adaptive evolution in the coccolithophore Gephyrocapsa oceanica following 1,000 generations of selection under elevated CO2

Coccolithophores are important oceanic primary producers not only in terms of photosynthesis but also because they produce calcite plates called coccoliths. Ongoing ocean acidification associated with changing seawater carbonate chemistry may impair calcification and other metabolic functions in coccolithophores. While short‐term ocean acidification effects on calcification and other properties have been examined in a variety of coccolithophore species, long‐term adaptive responses have scarcely been documented, other than for the single species Emiliania huxleyi. Here, we investigated the effects of ocean acidification on another ecologically important coccolithophore species, Gephyrocapsa oceanica, following 1,000 generations of growth under elevated CO₂ conditions (1,000 μatm). High CO₂‐selected populations exhibited reduced growth rates and enhanced particulate organic carbon (POC) and nitrogen (PON) production, relative to populations selected under ambient CO₂ (400 μatm). Particulate inorganic carbon (PIC) and PIC/POC ratios decreased progressively throughout the selection period in high CO₂‐selected cell lines. All of these trait changes persisted when high CO₂‐grown populations were moved back to ambient CO₂ conditions for about 10 generations. The results suggest that the calcification of some coccolithophores may be more heavily impaired by ocean acidification than previously predicted based on short‐term studies, with potentially large implications for the ocean's carbon cycle under accelerating anthropogenic influences.     

A triple trophic boost: How carbon emissions indirectly change a marine food chain

The pervasive enrichment of CO₂ in our oceans is a well‐documented stressor to marine life. Yet, there is little understanding about how CO₂ affects species indirectly in naturally complex communities. Using natural CO₂ vents, we investigated the indirect effects of CO₂ enrichment through a marine food chain. We show how CO₂ boosted the biomass of three trophic levels: from the primary producers (algae), through to their grazers (gastropods), and finally through to their predators (fish). We also found that consumption by both grazers and predators intensified under CO₂ enrichment, but, ultimately, this top‐down control failed to compensate for the boosted biomass of both primary producers and herbivores (bottom‐up control). Our study suggests that indirect effects can buffer the ubiquitous and direct, negative effects of CO₂ enrichment by allowing the upward propagation of resources through the food chain. Maintaining the natural complexity of food webs in our ocean communities could, therefore, help minimize the future impacts of CO₂ enrichment.     

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 (pCO₂) and decreasing pH might affect reproduction in adult fishes. We investigated the effects of near‐future levels of pCO₂ on the reproductive performance of the cinnamon anemonefish, Amphiprion melanopus, from the Great Barrier Reef, Australia. Breeding pairs were held under three CO₂ 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 CO₂ 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%) CO₂ treatment. Pairs in the High CO₂ 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 CO₂ 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 pCO₂. However, any long‐term consequences of increased reproductive effort on individuals or populations remain to be determined.     

The other ocean acidification problem: CO2 as a resource among competitors for ecosystem dominance

Predictions concerning the consequences of the oceanic uptake of increasing atmospheric carbon dioxide (CO₂) have been primarily occupied with the effects of ocean acidification on calcifying organisms, particularly those critical to the formation of habitats (e.g. coral reefs) or their maintenance (e.g. grazing echinoderms). This focus overlooks direct and indirect effects of CO₂ on non-calcareous taxa that play critical roles in ecosystem shifts (e.g. competitors). We present the model that future atmospheric [CO₂] may act as a resource for mat-forming algae, a diverse and widespread group known to reduce the resilience of kelp forests and coral reefs. We test this hypothesis by combining laboratory and field CO₂ experiments and data from ‘natural’ volcanic CO₂ vents. We show that mats have enhanced productivity in experiments and more expansive covers in situ under projected near-future CO₂ conditions both in temperate and tropical conditions. The benefits of CO₂ are likely to vary among species of producers, potentially leading to shifts in species dominance in a high CO₂ world. We explore how ocean acidification combines with other environmental changes across a number of scales, and raise awareness of CO₂ as a resource whose change in availability could have wide-ranging community consequences beyond its direct effects.     

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.     

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.     

Lessons from two high CO2 worlds – future oceans and intensive aquaculture

Exponentially rising CO₂ (currently ~400 μatm) is driving climate change and causing acidification of both marine and freshwater environments. Physiologists have long known that CO₂ directly affects acid–base and ion regulation, respiratory function and aerobic performance in aquatic animals. More recently, many studies have demonstrated that elevated CO₂ projected for end of this century (e.g. 800–1000 μatm) can also impact physiology, and have substantial effects on behaviours linked to sensory stimuli (smell, hearing and vision) both having negative implications for fitness and survival. In contrast, the aquaculture industry was farming aquatic animals at CO₂ levels that far exceed end‐of‐century climate change projections (sometimes >10 000 μatm) long before the term ‘ocean acidification’ was coined, with limited detrimental effects reported. It is therefore vital to understand the reasons behind this apparent discrepancy. Potential explanations include 1) the use of ‘control’ CO₂ levels in aquaculture studies that go beyond 2100 projections in an ocean acidification context; 2) the relatively benign environment in aquaculture (abundant food, disease protection, absence of predators) compared to the wild; 3) aquaculture species having been chosen due to their natural tolerance to the intensive conditions, including CO₂ levels; or 4) the breeding of species within intensive aquaculture having further selected traits that confer tolerance to elevated CO₂. We highlight this issue and outline the insights that climate change and aquaculture science can offer for both marine and freshwater settings. Integrating these two fields will stimulate discussion on the direction of future cross‐disciplinary research. In doing so, this article aimed to optimize future research efforts and elucidate effective mitigation strategies for managing the negative impacts of elevated CO₂ on future aquatic ecosystems and the sustainability of fish and shellfish aquaculture.     

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.     

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.     

Silent oceans: ocean acidification impoverishes natural soundscapes by altering sound production of the world's noisiest marine invertebrate

Soundscapes are multidimensional spaces that carry meaningful information for many species about the location and quality of nearby and distant resources. Because soundscapes are the sum of the acoustic signals produced by individual organisms and their interactions, they can be used as a proxy for the condition of whole ecosystems and their occupants. Ocean acidification resulting from anthropogenic CO₂ emissions is known to have profound effects on marine life. However, despite the increasingly recognized ecological importance of soundscapes, there is no empirical test of whether ocean acidification can affect biological sound production. Using field recordings obtained from three geographically separated natural CO₂ vents, we show that forecasted end-of-century ocean acidification conditions can profoundly reduce the biological sound level and frequency of snapping shrimp snaps. Snapping shrimp were among the noisiest marine organisms and the suppression of their sound production at vents was responsible for the vast majority of the soundscape alteration observed. To assess mechanisms that could account for these observations, we tested whether long-term exposure (two to three months) to elevated CO₂ induced a similar reduction in the snapping behaviour (loudness and frequency) of snapping shrimp. The results indicated that the soniferous behaviour of these animals was substantially reduced in both frequency (snaps per minute) and sound level of snaps produced. As coastal marine soundscapes are dominated by biological sounds produced by snapping shrimp, the observed suppression of this component of soundscapes could have important and possibly pervasive ecological consequences for organisms that use soundscapes as a source of information. This trend towards silence could be of particular importance for those species whose larval stages use sound for orientation towards settlement habitats.     

FUNCTIONAL GENETIC DIVERGENCE IN HIGH CO2 ADAPTED EMILIANIA HUXLEYI POPULATIONS

Predicting the impacts of environmental change on marine organisms, food webs, and biogeochemical cycles presently relies almost exclusively on short‐term physiological studies, while the possibility of adaptive evolution is often ignored. Here, we assess adaptive evolution in the coccolithophore Emiliania huxleyi, a well‐established model species in biological oceanography, in response to ocean acidification. We previously demonstrated that this globally important marine phytoplankton species adapts within 500 generations to elevated CO₂. After 750 and 1000 generations, no further fitness increase occurred, and we observed phenotypic convergence between replicate populations. We then exposed adapted populations to two novel environments to investigate whether or not the underlying basis for high CO₂‐adaptation involves functional genetic divergence, assuming that different novel mutations become apparent via divergent pleiotropic effects. The novel environment “high light” did not reveal such genetic divergence whereas growth in a low‐salinity environment revealed strong pleiotropic effects in high CO₂ adapted populations, indicating divergent genetic bases for adaptation to high CO₂. This suggests that pleiotropy plays an important role in adaptation of natural E. huxleyi populations to ocean acidification. Our study highlights the potential mutual benefits for oceanography and evolutionary biology of using ecologically important marine phytoplankton for microbial evolution experiments.     

Echinometra sea urchins acclimatized to elevated pCO2 at volcanic vents outperform those under present‐day pCO2 conditions

Rising atmospheric CO₂ concentrations will significantly reduce ocean pH during the 21st century (ocean acidification, OA). This may hamper calcification in marine organisms such as corals and echinoderms, as shown in many laboratory‐based experiments. Sea urchins are considered highly vulnerable to OA. We studied an Echinometra species on natural volcanic CO₂ vents in Papua New Guinea, where they are CO₂‐acclimatized and also subjected to secondary ecological changes from elevated CO₂. Near the vent site, the urchins experienced large daily variations in pH (>1 unit) and pCO₂ (>2000 ppm) and average pH values (pH_T 7.73) much below those expected under the most pessimistic future emission scenarios. Growth was measured over a 17‐month period using tetracycline tagging of the calcareous feeding lanterns. Average‐sized urchins grew more than twice as fast at the vent compared with those at an adjacent control site and assumed larger sizes at the vent compared to the control site and two other sites at another reef near‐by. A small reduction in gonad weight was detected at the vents, but no differences in mortality, respiration, or degree of test calcification were detected between urchins from vent and control populations. Thus, urchins did not only persist but actually ‘thrived’ under extreme CO₂ conditions. We suggest an ecological basis for this response: Increased algal productivity under increased pCO₂ provided more food at the vent, resulting in higher growth rates. The wider implication of our observation is that laboratory studies on non‐acclimatized specimens, which typically do not consider ecological changes, can lead to erroneous conclusions on responses to global change.     

Ocean Acidification Affects the Phyto-Zoo Plankton Trophic Transfer Efficiency

The critical role played by copepods in ocean ecology and biogeochemistry warrants an understanding of how these animals may respond to ocean acidification (OA). Whilst an appreciation of the potential direct effects of OA, due to elevated pCO₂, on copepods is improving, little is known about the indirect impacts acting via bottom-up (food quality) effects. We assessed, for the first time, the chronic effects of direct and/or indirect exposures to elevated pCO₂ on the behaviour, vital rates, chemical and biochemical stoichiometry of the calanoid copepod Acartia tonsa. Bottom-up effects of elevated pCO₂ caused species-specific biochemical changes to the phytoplanktonic feed, which adversely affected copepod population structure and decreased recruitment by 30%. The direct impact of elevated pCO₂ caused gender-specific respiratory responses in A.tonsa adults, stimulating an enhanced respiration rate in males (> 2-fold), and a suppressed respiratory response in females when coupled with indirect elevated pCO₂ exposures. Under the combined indirect+direct exposure, carbon trophic transfer efficiency from phytoplankton-to-zooplankton declined to < 50% of control populations, with a commensurate decrease in recruitment. For the first time an explicit role was demonstrated for biochemical stoichiometry in shaping copepod trophic dynamics. The altered biochemical composition of the CO₂-exposed prey affected the biochemical stoichiometry of the copepods, which could have ramifications for production of higher tropic levels, notably fisheries. Our work indicates that the control of phytoplankton and the support of higher trophic levels involving copepods have clear potential to be adversely affected under future OA scenarios.