Intergenerational effects of climate change on a coral reef fish, Amphiprion melanopus

The marine environment is facing the dual threats of rising temperature and ocean acidification. Coral reef ecosystems are thought to be especially sensitive to these threats due to evolving in a relatively stable thermal environment and the susceptibility of reef building corals to ocean acidification. For populations of marine organisms to persist under climate change conditions, they must be able to reproduce and produce offspring that will survive in the environment. This study examined the effects of ocean acidification and increasing temperature on reproduction in a coral reef fish, the cinnamon anemonefish (Amphiprion melanopus) and tested how parental effects influence the susceptibility of the offspring to these dual stressors. Ocean acidification is predicted to negatively affect reproduction of marine organisms, but few studies have tested this prediction in marine fishes. In Chapter 2, I determined the effect of ocean acidification on reproduction of A. melanopus by exposing adult breeding pairs to near-future CO₂ levels for a period of 9-months. A current-day control (~400μatm) and two CO₂ treatments (moderate (~600μatm) and high (~1000μatm)) were used based on CO₂ projections for the year 2100. Contrary to expectations, high CO₂ conditions stimulated reproduction. Pairs exposed to high CO₂ produced twice as many clutches, 60% more eggs and had 80% higher reproductive output compared with controls. Despite the increase in fecundity there were no changes in egg or hatchling size. This suggests, that for some species, increased CO₂ may not be as stressful as previously thought. Further, it suggests that a relatively small increase in CO₂ could potentially have stimulatory effects (a hormetic response) in reef fish. While no negative effects of increased reproductive effort were detected for either the adults or the offspring, it is possible that there could be effects in the longer-term that were not possible to investigate in this study. Increasing CO₂ is the main driver of rising temperature and ocean acidification; consequently these stressors will affect the marine environment simultaneously. In Chapter 3 I examined the interactive effects of increased temperature and ocean acidification on reproduction in fish using a current-day control (~400μatm) and two CO₂ treatments (moderate (~600μatm) and high (~1100μatm)) fully crossed with a current-day temperature control (+0.0°C (+28.5°C)), and 2 elevated temperature treatments (+1.5°C (30.0°C) and +3.0°C (31.5°C)). Reproductive activity was recorded throughout the breeding season and adult body condition was determined at the end of the breeding season. Elevated CO₂, by itself, only affected some hatchling traits, significantly reducing hatchling length at high CO₂ and reducing yolk area in both CO₂ treatments. Increased temperature, in contrast, had a more detrimental effect on reproductive performance. Notably there was a decline in reproduction with increasing temperature across all CO₂ treatments, with no reproduction occurring at +3.0°C. There was no effect of increasing CO₂ or temperature on adult body condition (Fulton's K) or hepatosomatic index, suggesting that the decline in reproduction was not due to increased energy expenditure at higher temperatures. Instead the decline in reproduction may be due to changes in hormone concentrations or efficacy. Plasma 17β-estradiol concentrations were highest in the treatment groups with the highest reproduction and were significantly lower with +3.0°C increase. However, whether this was a treatment effect or due to a correlation between hormone production and the stage of oocyte development is unknown. These results suggest that increasing temperature is a greater threat than ocean acidification to reproduction in reef fishes. The impact of ocean acidification on marine organisms may depend on the strength and direction of intergenerational effects. In Chapter 4, I examined the potential intergenerational effects of increased CO₂ by comparing the performance of offspring reared at the same CO₂ as their parents (control, moderate and high), with the performance of offspring from control parents that were reared at high CO₂ from hatching. This design allowed me to examine the acute (within generation) effects of elevated CO₂ on juvenile growth and survival and to determine if parental effects altered this response. Offspring in each CO₂ treatment were also reared at 3 different temperatures to examine the interactive effects of ocean acidification and global warming. Juvenile survival, weight, length and routine metabolic rate were measured at 31-days post hatching. Juveniles from control parents that were reared under high CO₂ had significantly lower performance compared with juveniles reared in control conditions. However, offspring from elevated CO₂ parents performed as well, if not better under high CO₂ conditions than control offspring. A decline in performance was detected with increasing temperature irrespective of CO₂ treatment. These results show that there is scope for transgenerational acclimation to ocean acidification, with the parental effects appearing to prime the offspring for the environment they will experience, thereby improving performance in a high CO₂ environment. Studies that neglect parental or transgenerational effects may not provide a true representation of the effects of ocean acidification. Recent studies have shown that increased CO₂ can increase otolith size in fish, however parental effects have not yet been investigated. In Chapter 5 I examined size and shape morphometrics of otoliths from juvenile A. melanopus using the same experimental design as Chapter 4. This allowed me to determine both the acute and parental effects of increased CO₂ on this important sense organ. I detected no significant differences in otolith size shape or asymmetry associated with acute or parental exposure to elevated CO₂ or increased temperature. These findings are consistent with earlier studies on coral reef fish otoliths and, combined, suggest that not all fish will be sensitive to elevated CO₂. I suggested reasons for differences in sensitive and provide caveats for interpretation and extrapolation of the literature on otolith calcification under elevated CO₂, and provide suggestions for future research. This research is the first to examine the interactive effects of high CO₂ and elevated temperature on fish reproduction and to test the potential for acclimation to ocean acidification in coral reef fish. My research shows that life history traits of reef fish may be relatively resilient to ocean acidification as a result of the capacity for transgenerational acclimation. However, reef fish reproduction is very sensitive to increasing temperature. Future studies should examine interactions between multiple climate change stressors, include the potential for transgenerational acclimation, and investigate how reproduction may change over multiple generations of exposure to rising temperature and ocean acidification.