Transgenerational acclimation and adaptation of reef fishes to ocean acidification

Ocean acidification, caused by the uptake of additional CO₂ from the atmosphere, will have far-reaching impacts on marine ecosystems. Many experiments have demonstrated negative effects of projected future CO₂ levels and reduced seawater pH on a diverse range of marine species. However, most of these studies have been of short duration and may not accurately predict the longer-term effects of ocean acidification on marine populations. In particular, few studies have considered the potential for marine organisms to acclimate or adapt to ocean acidification. Recent experiments show that short-term exposure to elevated CO₂ can affect a range of life history and behavioural traits in marine fishes, yet few studies have tested if these effects are maintained across multiple generations, or if fish populations might adapt to projected future CO₂ levels. A multigenerational perspective will enable us to better predict how ocean acidification will affect marine populations. This study therefore examines the potential effects of transgenerational exposure to ocean acidification in coral reef fishes. Reproduction is critical for individual and population success, and is where transgenerational effects will originate. However, reproduction is energetically expensive and could be adversely affected by rising CO₂ levels in the ocean. Therefore, Chapter 2 investigates 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) levels for a 9-month period that included the summer breeding season. 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. These results demonstrate different effects of high CO₂ on fish reproduction, even among species within the same family. Previous studies have shown that the behaviour and sensory performance of juvenile coral reef fishes are impaired at CO₂ levels projected to occur in the ocean in the next 50–100 years. However, it is unknown whether parental exposure to elevated CO₂ can allow for behavioural acclimation. Chapter 3 tests the potential for transgenerational acclimation of reef fish olfactory preferences and behavioural lateralization at moderate (656 μatm) and high (912 μatm) end-of-century CO₂ projections. Juvenile spiny damselfish, Ac. polyacanthus, from control parents (446 μatm) exhibited an innate avoidance to chemical alarm cue (CAC); however, juveniles lost this innate response and even became attracted to CAC when reared at elevated CO₂ levels. Juveniles from parents maintained at mid-CO₂ and high-CO₂ levels also lost their innate avoidance of CAC when reared in elevated CO₂, demonstrating no capacity for transgenerational acclimation of olfactory responses. Behavioural lateralization was also disrupted for juveniles reared under elevated CO₂, regardless of parental conditioning. These results demonstrate minimal potential for transgenerational acclimation in this fish, suggesting that genetic adaptation will be necessary to overcome the effects of ocean acidification on behaviour. Changes to the morphology of fish otoliths (aragonitic ear bones) have been observed under higher levels of CO₂, with potential implications for hearing, balance and orientation in a future high CO₂ environment. However, no studies have tested for possible transgenerational effects of high CO₂ on otolith morphology. Chapter 4 assesses transgenerational effects of high CO₂ on otolith area, perimeter, maximum length and circularity in juvenile Ac. polyacanthus. Offspring from parents maintained at control (446 μatm), moderate CO₂ (652 μatm) and high CO₂ (912 μatm) were reared for 6 weeks in the three treatments, in a fully crossed design. Otolith development in juveniles was affected by moderate CO₂ exposure, but these effects were absent when parents also experienced moderate CO₂. However, transgenerational exposure to high CO₂ resulted in increased otolith area and perimeter. These results show that transgenerational acclimation can mitigate the effects of moderate CO₂ on otolith development in Ac. polyacanthus, but higher CO₂ levels lead to marked effects on otolith development across generations. The lack of transgenerational acclimation in behaviours to high CO₂ (Chapter 3) indicates that genetic adaptation will be required to maintain behavioural performance in the future. Adaptation depends on the presence of heritable phenotypic variation in the trait, which may differ between populations and environments. Previous studies have shown that some individuals exhibit greater behavioural tolerance to high CO₂ than others, but whether this behavioural tolerance is heritable is unknown. In Chapter 5, I used father-midoffspring regressions to estimate the heritability of behavioural tolerance to high CO₂ (754 μatm) in both field and laboratory-reared populations of Ac. polyacanthus. The field population of Ac. polyacanthus exhibited high heritability of olfactory behaviour phenotype (h² = 0.56) when offspring were acutely exposed to high CO₂ for 4-5 days. The laboratory population exhibited similarly high heritability of olfactory behaviour phenotype (h² = 0.65) when offspring were acutely exposed to high CO₂. However, this heritability was completely lost when juveniles where chronically exposed to high CO₂ for 6 weeks. Parental exposure to high CO₂ did not alter this relationship between acute and chronic CO₂ treatments: heritability of behavioural phenotype was high when offspring were acutely exposed to high CO₂, but lost when offspring when chronically exposed to high CO₂, regardless of parent treatment. The loss of heritability occurred because juveniles that were relatively tolerant to high CO₂ in the acute treatment lost this tolerance in the chronic CO₂ treatment. This indicates that genetic variation in behavioural tolerance to high CO₂ is obscured by non-adaptive plasticity when offspring are chronically exposed to high CO₂. These results demonstrate that behavioural tolerance to high CO₂ is heritable, but adaptive potential may be severely limited by non-adaptive plasticity when a high CO₂ environment is experienced across several generations, as will occur due to rising CO₂ levels in the ocean. This research is among the first to use a multigenerational approach to test the effects of ocean acidification on reef fishes and estimate their adaptive potential. The results demonstrate how CO₂ levels predicted for the end of the century affect the behaviour and life history traits of reef fish in various ways. Critically, I found no evidence for transgenerational acclimation of impaired behaviours to CO₂, and that heritable variation in behavioural tolerance to high CO₂ was obscured by non-adaptive plasticity when offspring were reared from hatching in a high CO₂ environment. These results are concerning because they indicate little scope for acclimation or adaptation of impaired behavioural responses to high CO₂, at least in Ac. polyacanthus. Further research should examine potential trade-offs of behavioural and physiological processes in elevated CO₂ environments to better predict overall survival and success of marine populations. This research demonstrates the important of incorporating a long-term, multigenerational perspective when assessing the likely impacts of ocean acidification on marine ecosystems.