The effects of climate change on predator-prey interactions in coral reef fish

Climate change is one of the greatest threats facing marine ecosystems. Despite a rapid increase in scientific research in this field, predicting the response and acclimatory capacity of marine animals remains difficult. Moreover, predicting the responses of interacting species is further challenging owing to different sensitivities to elevated carbon dioxide (CO₂) and increasing temperatures among species. Recent studies demonstrate that end of century predicted increases in CO₂ and temperature can affect the physiological performance and behaviour of marine fishes; however, little is known of the effect of these stressors on ecological processes, such as predator-prey interactions. To explore this, Chapter 2 aimed to determine whether predators and prey respond differently to modest increases in temperature (ambient 27°C and elevated temperature 30°C), and whether these responses change the outcome of predator-prey interactions by affecting the kinematics of the encounter. Exposure to elevated temperatures significantly affected the predator-prey interactions of a pair of common reef fish, the planktivorous damselfish (Pomacentrus wardi) and the piscivorous dottyback (Pseudochromis fuscus). When predators exposed to elevated temperatures interacted with prey exposed in a similar manner, maximal attack speeds increased. This effect coupled with decreasing prey escape speeds and escape distances led to increased predation rates. Prey exposed to elevated temperatures also had decreased reaction distances and increased apparent looming threshold, suggesting that their sensory performance was affected. This occurred despite the increase in maximal attack speeds, which in other species has been shown to increase reaction distances. These results suggest that the escape performance of prey is sensitive to short-term increases in ambient temperature. Predators may become more successful, leading to strong selection for the maintenance of maximal escape performance in prey. In addition to increasing sea surface temperatures, ocean acidification is posing a problem for many marine organisms. Recent research has shown that exposure to elevated 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 it is due to prey increasing activity levels. Chapter 3 examined the potential cause of increased mortality of prey fish, asking the specific question: Does exposure to elevated CO₂ change the outcome of predator-prey encounters by altering the kinematics of the predator-prey interaction? To test this question, prey (Pomacentrus amboinensis) were exposed to elevated CO₂ (~880 μatm) or to a present-day control (~440 μatm) and allowed to interact with similarly exposed predators (Pseudochromis fuscus) in a cross-factored design. This enabled me to tease apart the independent effects on the predator and prey as well as the interacting effects when both were exposed to elevated CO₂. These results show that exposure to elevated CO₂ significantly affected the interactions between P. amboinensis and P. fuscus. Specifically, 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. While there has been extensive research on the effects of elevated CO₂ and rising temperatures on marine organisms, most studies have tested the effects of these drivers in isolation. However, given that these stressors are unlikely to occur independently, there is a need to gain a more ecologically realistic understanding of how the combined effects of temperature and acidification will affect marine organisms. Chapter 4 tested the independent and interactive effects of short-term elevated CO₂ and temperature exposure on the interactions between P. wardi and its predator, P. fuscus. Predators and prey were split into 4 different treatment groups in a 2 CO₂ (405 and 930 μatm) x 2 temperature (27 and 30°C) design. Results showed that predator success increased following predator and prey exposure to elevated CO₂ and temperature. Specifically, exposure to high temperatures resulted in the greatest capture success followed by the combined exposure to elevated CO₂ and temperature. There was a strong influence of temperature on prey escape behaviour. We observed significant changes in prey reaction distances, apparent looming thresholds and directionality, as well as declining escape speeds and distances. Contrary to expectations, there was little influence of temperature or CO₂ on the behaviour of the predator, suggesting that the attack behaviour of P. fuscus was robust to these environmental changes. Overall, high temperature had an overwhelming negative effect on the escape behaviour of the prey compared to the independent effect of CO₂ or the combined exposure to elevated CO₂ and temperature. These results, combining escape performance, attack behaviour and mortality rates, suggest that increasing CO₂ and warming may lead to complex changes in the predator-prey relationships of coral reef communities. Though recent studies have shown that elevated CO₂ can increase the mortality rate of prey when exposed to predators (for example Chapter 3), the extent to which fish larvae can acclimate their escape responses across generations exposed to elevated CO₂ is unknown. Chapter 5 tested the acute effects of elevated CO₂ exposure on the escape responses of juvenile fish and whether such effects are altered by exposure of parents to elevated CO₂ (transgenerational acclimation). To test the hypothesis that transgenerational acclimation may reduce the impact of elevated CO₂ on escape performance, adults and juveniles were reared under current-day CO₂ levels (~400 μatm) or CO₂ levels projected to occur by the end of the century (~1087 μatm). Comparisons between treatments enabled the determination of the acute (within-generation) effects of increased CO₂ on juvenile escape performance and whether such effects were mediated by exposure of parents to increased CO₂. Elevated CO₂ negatively affected the reactivity and locomotor performance of juvenile fish, but parental exposure to high CO₂ reduced the effects in some traits, indicating the potential for acclimation of behavioural impairment across generations. However, acclimation was not complete in some traits, and absent in others, suggesting that transgenerational acclimation does not completely compensate the effects of high CO₂ on escape responses. This research demonstrated that there is a potential for rapid acclimation for variables that influence escape performance, if the parents have been exposed to the same environmental history. However, parental effects did not fully restore performance in most traits. Thus, negative effects of higher CO₂ levels on behaviour remain, although at reduced levels. Whether behaviours could be fully acclimated in future generations and the potential costs of such acclimation to other processes is unknown. This highlights the need to exercise caution when making statements about whole organism acclimation. Examining interactions between species in response to environmental stressors can be complex due to behaviourial subtleties that may not be captured. However, only focusing on the responses of individual species is likely to provide an insufficient basis from which an understanding of long term responses to climate change can be inferred. This is particularly true in complex ecological environments, such as coral reefs. In the present era of rapid climate change, understanding how changes to individual performance influences the relationships between predators and their prey will be increasingly important in predicting the effects of climate change within ecosystems. These are the first studies to address how the kinematics at the basis of predator-prey interactions may change in response to independent and concurrent exposure to elevated CO₂ and temperature, and whether there is any potential for acclimation to occur. Understanding how organisms and ecosystems respond to key environmental drivers remains a priority for science, management and conservation.