Rapid embryonic development supports the early onset of gill functions in two coral reef damselfishes.

The gill is one of the most important organs for growth and survival of fishes. Early life stages in coral reef fishes often exhibit extreme physiological and demographic characteristics that are linked to well-established respiratory and ionoregulatory processes. However, gill development and function in coral reef fishes is not well understood. Therefore, we investigated gill morphology, oxygen uptake and ionoregulatory systems throughout embryogenesis in two coral reef damselfishes, Acanthochromis polyacanthus and Amphiprion melanopus (Pomacentridae). In both species, we found key gill structures to develop rapidly early in the embryonic phase. Ionoregulatory cells appear on gill filaments 3-4 days post-fertilization and increase in density, whilst disappearing or shrinking in cutaneous locations. Primary respiratory tissue (lamellae) appears 5-7 days post-fertilization, coinciding with a peak in oxygen uptake rates of the developing embryos. Oxygen uptake was unaffected by phenylhydrazine across all ages (pre-hatching), indicating that haemoglobin is not yet required for oxygen uptake. This suggests that gills have limited contribution to respiratory functions during embryonic development, at least until hatching. Rapid gill development in damselfishes, when compared with that in most previously investigated fishes, may reflect preparations for a high-performance, challenging lifestyle on tropical reefs, but may also make reef fishes more vulnerable to anthropogenic stressors.

Contrasting effects of constant and fluctuating pCO2 conditions on the exercise physiology of coral reef fishes.

Ocean acidification (OA) is predicted to affect the physiology of some fishes. To date, most studies have investigated this issue using stable pCO2 levels based on open ocean projections. Yet, most shallow, nearshore systems experience temporal and spatial pCO2 fluctuations. For example, pCO2 on coral reefs is highest at night and lowest during the day, but as OA progresses, both the average pCO2 and magnitude of fluctuations are expected to increase. We exposed four coral reef fishes - Lutjanus fulviflamma, Caesio cuning, Abudefduf whitleyi, and Cheilodipterus quinquelineatus - to ambient, stable elevated, or fluctuating elevated pCO2 conditions for 9-11 days. Then, we measured swimming performance, oxygen uptake rates, and haematological parameters during the day and at night. When compared to ambient pCO2 conditions, L. fulviflamma, C. cuning, and A. whitleyi exposed to fluctuating elevated pCO2 increased swimming performance, maximum oxygen uptake rates, and aerobic scope, regardless of time of day; whereas, the only nocturnal species studied, C. quinquelineatus, decreased maximum oxygen uptake rates and aerobic scope. Our findings suggest that exposure to fluctuating or stable elevated pCO2 can physiologically benefit some coral reef fishes; however, other species, such as the cardinalfish examined here, may be more sensitive to future OA conditions.

Elevated temperature and CO2 have positive effects on the growth and survival of larval Australasian snapper.

Rising water temperature and increased uptake of CO2 by the ocean are predicted to have widespread impacts on marine species. However, the effects are likely to vary, depending on a species' sensitivity and the geographical location of the population. Here, we investigated the potential effects of elevated temperature and pCO2 on larval growth and survival in a New Zealand population of the Australasian snapper, Chrysophyrs auratus. Eggs and larvae were reared in a fully cross-factored experiment (18 °C and 22 °C/pCO2 440 and 1040 µatm) to 16 days post hatch (dph). Morphologies at 1 dph and 16 dph were significantly affected by temperature, but not CO2. At 1dph, larvae at 22 °C were longer (7%) and had larger muscle depth at vent (14%), but had reduced yolk (65%) and oil globule size (16%). Reduced yolk reserves in recently hatched larvae suggests higher metabolic demands in warmer water. At 16 dph, larvae at elevated temperature were longer (12%) and muscle depth at vent was larger (64%). Conversely, survival was primarily affected by CO2 rather than temperature. Survivorship at 1 dph and 16 dph was 24% and 54% higher, respectively, under elevated CO2 compared with ambient conditions. Elevated temperature increased survival (24%) at 1 dph, but not at 16 dph. These results suggest that projected climate change scenarios may have an overall positive effect on early life history growth and survival in this population of C. auratus. This could benefit recruitment success, but needs to be weighed against negative effects of elevated CO2 on metabolic rates and swimming performance observed in other studies on the same population.

An uncertain future: Effects of ocean acidification and elevated temperature on a New Zealand snapper (Chrysophrys auratus) population.

Anthropogenic CO2 emissions are warming and acidifying Earth's oceans, which is likely to lead to a variety of effects on marine ecosystems. Fish populations will be vulnerable to this change, and there is now substantial evidence of the direct and indirect effects of climate change on fish. There is also a growing effort to conceptualise the effects of climate change on fish within population models. In the present study knowledge about the response of New Zealand snapper to warming and acidification was incorporated within a stock assessment model. Specifically, a previous tank experiment on larval snapper suggested both positive and negative effects, and otolith increment analysis on wild snapper indicated that growth may initially increase, followed by a potential decline as temperatures continue to warm. As a result of this uncertainty, sensitivity analysis was performed by varying average virgin recruitment (R0) by ±30%, adult growth by ±6%, but adjusting mean size at recruitment by +48% as we had better evidence for this increase. Overall adjustments to R0 had the biggest impact on the future yield (at a management target of 40% of an unfished population) of the Hauraki Gulf snapper fishery. The most negative scenario suggested a 29% decrease in fishery yield, while the most optimistic scenario suggested a 44% increase. While largely uncertain, these results provide some scope for predicting future impacts on the snapper fishery. Given that snapper is a species where the response to climate change has been specifically investigated, increasing uncertainty in a future where climate change and other stressors interact in complex and unpredictable ways is likely to be an important consideration for the management of nearly all fish populations.

Elevated CO2 affects anxiety but not a range of other behaviours in juvenile yellowtail kingfish.

Elevated seawater CO2 can cause a range of behavioural impairments in marine fishes. However, most studies to date have been conducted on small benthic species and very little is known about how higher oceanic CO2 levels could affect the behaviour of large pelagic species. Here, we tested the effects of elevated CO2, and where possible the interacting effects of high temperature, on a range of ecologically important behaviours (anxiety, routine activity, behavioural lateralization and visual acuity) in juvenile yellowtail kingfish, Seriola lalandi. Kingfish were reared from the egg stage to 25 days post-hatch in a full factorial design of ambient and elevated CO2 (~500 and ~1000 µatm pCO2) and temperature (21 °C and 25 °C). The effects of elevated CO2 were trait-specific with anxiety the only behaviour significantly affected. Juvenile S. lalandi reared at elevated CO2 spent more time in the dark zone during a standard black-white test, which is indicative of increased anxiety. Exposure to high temperature had no significant effect on any of the behaviours tested. Overall, our results suggest that juvenile S. lalandi are largely behaviourally tolerant to future ocean acidification and warming. Given the ecological and economic importance of large pelagic fish species more studies investigating the effect of future climate change are urgently needed.

Elevated CO2 and food ration affect growth but not the size-based hierarchy of a reef fish.

Under projected levels of ocean acidification, shifts in energetic demands and food availability could interact to effect the growth and development of marine organisms. Changes to individual growth rates could then flow on to influence emergent properties of social groups, particularly in species that form size-based hierarchies. To test the potential interactive effects of (1) food availability, (2) elevated CO2 during juvenile development, and (3) parental experience of elevated CO2 on the growth, condition and size-based hierarchy of juvenile fish, we reared orange clownfish (Amphiprion percula) for 50 days post-hatching in a fully orthogonal design. Development in elevated CO2 reduced standard length and weight of juveniles, by 9% and 11% respectively, compared to ambient. Development under low food availability reduced length and weight of juveniles by 7% and 15% respectively, compared to high food. Parental exposure to elevated CO2 restored the length of juveniles to that of controls, but it did not restore weight, resulting in juveniles from elevated CO2 parents exhibiting 33% lower body condition when reared in elevated CO2. The body size ratios (relative size of a fish from the rank above) within juvenile groups were not affected by any treatment, suggesting relative robustness of group-level structure despite alterations in individual size and condition. This study demonstrates that both food availability and elevated CO2 can influence the physical attributes of juvenile reef fish, but these changes may not disrupt the emergent group structure of this social species, at least amongst juveniles.

Effects of elevated CO2 on predator avoidance behaviour by reef fishes is not altered by experimental test water.

Pioneering studies into the effects of elevated CO2 on the behaviour of reef fishes often tested high-CO2 reared fish using control water in the test arena. While subsequent studies using rearing treatment water (control or high CO2) in the test arena have confirmed the effects of high CO2 on a range of reef fish behaviours, a further investigation into the use of different test water in the experimental arena is warranted. Here, we used a fully factorial design to test the effect of rearing treatment water (control or high CO2) and experimental test water (control or high CO2) on antipredator responses of larval reef fishes. We tested antipredator behaviour in larval clownfish Amphiprion percula and ambon damselfish Pomacentrus amboinensis, two species that have been used in previous high CO2 experiments. Specifically, we tested if: (1) using control or high CO2 water in a two channel flume influenced the response of larval clownfish to predator odour; and (2) using control or high CO2 water in the test arena influenced the escape response of larval damselfish to a startle stimulus. Finally, (3) because the effects of high CO2 on fish behaviour appear to be caused by altered function of the GABA-A neurotransmitter we tested if antipredator behaviours were restored in clownfish treated with a GABA antagonist (gabazine) in high CO2 water. Larval clownfish reared from hatching in control water (496 µatm) strongly avoided predator cue whereas larval clownfish reared from hatching in high CO2 (1,022 µatm) were attracted to the predator cue, as has been reported in previous studies. There was no effect on fish responses of using either control or high CO2 water in the flume. Larval damselfish reared for four days in high CO2 (1,051 µatm) exhibited a slower response to a startle stimulus and slower escape speed compared with fish reared in control conditions (464 µatm). There was no effect of test water on escape responses. Treatment of high-CO2 reared clownfish with 4 mg l-1 gabazine in high CO2 seawater restored the normal response to predator odour, as has been previously reported with fish tested in control water. Our results show that using control water in the experimental trials did not influence the results of previous studies on antipredator behaviour of reef fishes and also supports the results of novel experiments conducted in natural reef habitat at ambient CO2 levels.