The global impacts of climate change on fish

Climate change is a global issue and the effects on fish populations remain largely unknown. It is thought that climate change could affect fish at all levels of biological organisation, from cellular,
individual, population and community. This thesis has taken a holistic approach to examine the ways in which climate change could affect fish from both tropical, marine ecosystems (Great Barrier Reef,
Australia) and temperate, freshwater ecosystems (non-tidal River Thames, Britain). Aerobic scope of coral reef fish tested on the Great Barrier Reef was significantly reduced by just a 2°C rise in water temperature (31, 32 and 33°C, compared to the current summer mean of 29°C) due to increased resting oxygen consumption and an inability to increase the maximal oxygen uptake. A 0.3 unit decline in pH, representative of ocean acidification, caused the same percentage loss in aerobic scope as did a 3°C warming. Interfamilial differences in ability to cope aerobically with warming waters will likely lead to changes in the community structure on coral reefs with damselfish replacing cardinalfish.

Concerning Britain, there is evidence of gradual warming and increased rainfall in winter months over a 150 year period, suggesting that British fish are already experiencing climate change. It was evident from an analysis of a 15 year dataset on fish populations in the River Thames, that cyprinid species displayed a different pattern in biomass and density to all the non-cyprinid fish population, suggesting that there will be interfamilial differences in responses to climate change.

Using a Biological Indicator Approach on the three-spined stickleback, Gasterosteus aculeatus, a 2°C rise in water temperature resulted in a stress response at the cellular and whole organism level. A 6°C rise in temperature resulted in a stress response at the biochemical level (higher cortisol and glucose concentrations), cellular level (higher neutrophil: lymphocyte ratio) and whole organism level (higher ventilation rate and lowered condition factor, hepatosomatic index and growth). G. aculeatus is considered to be temperature tolerant; therefore these results indicate that climate change may prove to be stressful for more temperature-sensitive species. This study has demonstrated that climate change will have direct effects on fish populations, whether they are in temperate regions such as Britain or in tropical coral reefs,but with strong interfamilial differences in those responses.

Effects of ocean acidification on the larval growth of olive flounder (Paralichthys olivaceus)

Little is known about how marine fishes respond to the reduced pH condition caused by the increased CO₂ in the atmosphere. We investigated the effects of CO₂ concentration on the growth of olive flounder (Paralichthys olivaceus) larvae. Newly hatched larvae were reared in three different concentrations of CO₂ (574, 988 and 1297 μatm CO₂) in temperature-controlled water tanks until metamorphosis (4 weeks). Body lengths, weights, and the concentration of some chemical elements in larval tissue were measured at the completion of each experiment, and experiment was repeated three times in May, June, and July 2011. Results indicated that body length and weight of flounder larvae were significantly increased with increasing CO₂ concentration (P < 0.05). Daily growth rates of flounder larvae were higher (0.391 mm) from the high CO₂ concentration (1297 μatm) than those (0.361 mm and 0.360 mm) from the lower ones (988 and 574 μatm).The measurement on some chemical elements (Ca, Fe, Cu, Zn and Sr) in fish tissue also revealed the increasing tendency of element concentration with increasing CO₂ in seawater, although statistical significance cannot be tested due to the single measurement. It suggests that there are enrichment processes of these cations in larval tissue in the low pH condition.

Effects of sub-lethal CO2(aq) concentrations on the performance of intensively reared gilthead seabream (Sparus aurata) in brackish water: flow-through experiments and full-scale RAS results

The effects sub-lethal CO_2(aq) concentrations were tested for the first time on gilthead seabream (Sparus aurata) juveniles (4 to 25 g; 64 growth days) and adult (∼300-400 g; 71 days) fish, both in fully controlled pilot tests and the latter also as part of full-scale RAS (recirculating aquaculture system) operation. In the pilot experiments (concentration range 5.2 to 56.3 mgCO₂/L) the specific growth rate, mortality rate, and physical fish disorders were monitored. In the full scale experiment, two groups of fish, originally from the same batch, were exposed for 197 days to controlled (by NaOH dosage) and uncontrolled pH conditions, resulting in exposure of the fish to significantly different CO_2(aq) concentrations. The pilot results showed, as expected, that the seabream fish grew faster at the lower CO₂ concentrations and that the growth rate of both juveniles and adult fish was only minimally inhibited up to roughly 20 mg CO₂/L (compared to a previously published curve). Mortality rate was considerable only at the highest CO₂ concentration (∼56 mgCO₂/L). Physical irregularities were not observed, apart from abnormally-high absence of swim bladder at the highest CO_2(aq) treatment. The (statistically significant) results from the full-scale RAS operation showed that growing gilthead seabream for 197 days at roughly constant and relatively low (∼16 mg/L) CO_2(aq) concentration resulted in fish with ∼10% larger mean weight relative to the fish grown in ponds in which CO_2(aq) was not controlled and its concentration fluctuated daily between 19 and 37 mg/L.

Ocean acidification alters the otoliths of a pantropical fish species with implications for sensory function

Ocean acidification affects a wide diversity of marine organisms and is of particular concern for vulnerable larval stages critical to population replenishment and connectivity. Whereas it is well known that ocean acidification will negatively affect a range of calcareous taxa, the study of fishes is more limited in both depth of understanding and diversity of study species. We used new 3D microcomputed tomography to conduct in situ analysis of the impact of ocean acidification on otolith (ear stone) size and density of larval cobia (Rachycentron canadum), a large, economically important, pantropical fish species that shares many life history traits with a diversity of high-value, tropical pelagic fishes. We show that 2,100 μatm partial pressure of carbon dioxide (pCO₂) significantly increased not only otolith size (up to 49% greater volume and 58% greater relative mass) but also otolith density (6% higher). Estimated relative mass in 800 μatm pCO₂ treatments was 14% greater, and there was a similar but nonsignificant trend for otolith size. Using a modeling approach, we demonstrate that these changes could affect auditory sensitivity including a ∼50% increase in hearing range at 2,100 μatm pCO₂, which may alter the perception of auditory information by larval cobia in a high-CO₂ ocean. Our results indicate that ocean acidification has a graded effect on cobia otoliths, with the potential to substantially influence the dispersal, survival, and recruitment of a pelagic fish species. These results have important implications for population maintenance/replenishment, connectivity, and conservation efforts for other valuable fish stocks that are already being deleteriously impacted by overfishing.

Sex in murky waters : anthropogenic disturbance of sexual selection in pipefish

Animals experience variation in their environment because of natural changes. However, due to anthropogenic disturbance, the speed and severity of these changes have recently increased. This thesis investigates how reproductive behaviours may be affected by human induced environmental change. In specific, I investigate how visual and chemical changes in the aquatic environment, caused by eutrophication, affect mating systems and sexual selection in fish. Broad-nosed- and straight-nosed pipefish, which both have been studied in detail for a long period, were used as model organisms. These two species are particularly suitable model organisms since they perform complex courtship behaviours, including the advertisement of ornaments and a nuptial dance. Further, two distinct populations were studied, one on the Swedish west coast and one in the Baltic Sea, as these two locations vary in the degree and extent of environmental disturbance, in particular turbidity. I found that changes in the visual environment had no impact on the development of female sexual ornaments in these sex-role reversed pipefishes, but it hampered adaptive mate choice. Turbidity also had a negative effect on reproductive success in the Baltic Sea population. Changes in the chemical environment in the form of increased pH reduced the probability to mate, while hypoxia did not alter mating propensity. However, hypoxic water delayed the onset of both courting and mating. Hence, human induced change in aquatic environments may alter the processes of sexual selection and population dynamics.

The response of abyssal organisms to low pH conditions during a series of CO2-release experiments simulating deep-sea carbon sequestration

The effects of low-pH, high-pCO₂ conditions on deep-sea organisms were examined during four deep-sea CO₂ release experiments simulating deep-ocean C sequestration by the direct injection of CO₂ into the deep sea. We examined the survival of common deep-sea, benthic organisms (microbes; macrofauna, dominated by Polychaeta, Nematoda, Crustacea, Mollusca; megafauna, Echinodermata, Mollusca, Pisces) exposed to low-pH waters emanating as a dissolution plume from pools of liquid carbon dioxide released on the seabed during four abyssal CO₂-release experiments. Microbial abundance in deep-sea sediments was unchanged in one experiment, but increased under environmental hypercapnia during another, where the microbial assemblage may have benefited indirectly from the negative impact of low-pH conditions on other taxa. Lower abyssal metazoans exhibited low survival rates near CO₂ pools. No urchins or holothurians survived during 30–42 days of exposure to episodic, but severe environmental hypercapnia during one experiment (E1; pH reduced by as much as ca. 1.4 units). These large pH reductions also caused 75% mortality for the deep-sea amphipod, Haploops lodo, near CO₂ pools. Survival under smaller pH reductions (ΔpH<0.4 units) in other experiments (E2, E3, E5) was higher for all taxa, including echinoderms. Cephalopods, gastropods, and fish were more tolerant than most other taxa. The gastropod Mohnia vernalis and octopus Benthoctopus sp. survived exposure to pH reductions that episodically reached −0.3 pH units. Ninety percent of abyssal zoarcids (Pachycara bulbiceps) survived exposure to pH changes reaching ca. −0.3 pH units during 30–42 day-long experiments.

Meta-analysis reveals complex marine biological responses to the interactive effects of ocean acidification and warming

Ocean acidification and warming are considered two of the greatest threats to marine biodiversity, yet the combined effect of these stressors on marine organisms remains largely unclear. Using a meta-analytical approach, we assessed the biological responses of marine organisms to the effects of ocean acidification and warming in isolation and combination. As expected biological responses varied across taxonomic groups, life-history stages, and trophic levels, but importantly, combining stressors generally exhibited a stronger biological (either positive or negative) effect. Using a subset of orthogonal studies, we show that four of five of the biological responses measured (calcification, photosynthesis, reproduction, and survival, but not growth) interacted synergistically when warming and acidification were combined. The observed synergisms between interacting stressors suggest that care must be made in making inferences from single-stressor studies. Our findings clearly have implications for the development of adaptive management strategies particularly given that the frequency of stressors interacting in marine systems will be likely to intensify in the future. There is now an urgent need to move toward more robust, holistic, and ecologically realistic climate change experiments that incorporate interactions. Without them accurate predictions about the likely deleterious impacts to marine biodiversity and ecosystem functioning over the next century will not be possible.

Elevated CO2 affects predator-prey interactions through altered performance

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

Metabolic shifts in the Antarctic fish Notothenia rossii in response to rising temperature and PCO2

Introduction

Ongoing ocean warming and acidification increasingly affect marine ecosystems, in particular around the Antarctic Peninsula. Yet little is known about the capability of Antarctic notothenioid fish to cope with rising temperature in acidifying seawater. While the whole animal level is expected to be more sensitive towards hypercapnia and temperature, the basis of thermal tolerance is set at the cellular level, with a putative key role for mitochondria. This study therefore investigates the physiological responses of the Antarctic Notothenia rossii after long-term acclimation to increased temperatures (7°C) and elevated PCO₂ (0.2 kPa CO₂) at different levels of physiological organisation.

Results

For an integrated picture, we analysed the acclimation capacities of N. rossii by measuring routine metabolic rate (RMR), mitochondrial capacities (state III respiration) as well as intra- and extracellular acid–base status during acute thermal challenges and after long-term acclimation to changing temperature and hypercapnia. RMR was partially compensated during warm- acclimation (decreased below the rate observed after acute warming), while elevated PCO₂ had no effect on cold or warm acclimated RMR. Mitochondrial state III respiration was unaffected by temperature acclimation but depressed in cold and warm hypercapnia-acclimated fish. In both cold- and warm-exposed N. rossii, hypercapnia acclimation resulted in a shift of extracellular pH (pH_e) towards more alkaline values. A similar overcompensation was visible in muscle intracellular pH (pH_i). pH_i in liver displayed a slight acidosis after warm normo- or hypercapnia acclimation, nevertheless, long-term exposure to higher PCO₂ was compensated for by intracellular bicarbonate accumulation.

Conclusion

The partial warm compensation in whole animal metabolic rate indicates beginning limitations in tissue oxygen supply after warm-acclimation of N. rossii. Compensatory mechanisms of the reduced mitochondrial capacities under chronic hypercapnia may include a new metabolic equilibrium to meet the elevated energy demand for acid–base regulation. New set points of acid–base regulation under hypercapnia, visible at the systemic and intracellular level, indicate that N. rossii can at least in part acclimate to ocean warming and acidification. It remains open whether the reduced capacities of mitochondrial energy metabolism are adaptive or would impair population fitness over longer timescales under chronically elevated temperature and PCO₂.

CO2-driven seawater acidification differentially affects development and molecular plasticity along life history of fish (Oryzias latipes)

Fish early life stages have been shown to react sensitive to simulated ocean acidification. In particular, acid–base disturbances elicited by altered seawater carbonate chemistry have been shown to induce pathologies in larval fish. However, the mechanisms underlying these disturbances are largely unknown. We used gene expression profiling of genes involved in acid–base regulation and metabolism to investigate the effects of seawater hypercapnia on developing Japanese ricefish (medaka; Oryzias latipes). Our results demonstrate that embryos respond with delayed development during the time window of 2–5 dpf when exposed to a seawater pCO₂ of 0.12 and 0.42 kPa. This developmental delay is associated with strong down-regulation of genes from major metabolic pathways including glycolysis (G6PDH), Krebs cycle (CS) and the electron transport chain (CytC). In a second step we identified acid–base relevant genes in different ontogenetic stages (embryos, hatchlings and adults) and tissues (gill and intestine) that are up regulated in response to hypercapnia, including NHE3, NBCa, NBCb, AE1a, AE1b, ATP1a1a.1, ATP1a1b, ATP1b1a, Rhag, Rhbg and Rhcg. Interestingly, NHE3 and Rhcg expressions were increased in response to environmental hypercapnia in all ontogenetic stages and tissues tested, indicating the central role of these proteins in acid–base regulation. Furthermore, the increased expression of genes from amino acid metabolism pathways (ALT1, ALT2, AST1a, AST1b, AST2 and GLUD) suggests that energetic demands of hatchlings are fueled by the breakdown of amino acids. The present study provides a first detailed gene expression analysis throughout the ontogeny of a euryhaline teleost in response to seawater hypercapnia, indicating highest sensitivity in early embryonic stages, when functional ion regulatory epithelia are not yet developed.