The industrial activity of the 21st century has driven rapid change in the marine environment; the ocean is simultaneously acidifying, warming and getting noisier, and is predicted to continue to do so (Gattuso et al., 2015). Recent studies have shown these three stressors to modify fundamental ecological interactions with deleterious consequences for prey survival, and have suggested such changes could reap potential consequences for future community structure and function (Munday et al., 2014; Simpson et al., 2016; Allan et al., 2017).
The complex mechanics of the predator-prey relationship generally occur as the result of an ‘evolutionary arms race’ between the two, in which one selects an advantageous functional trait against the other, driven by mutual interactions (Schmitz, 2017). The predation of coral reef recruits is instrumental in structuring assemblages (Roberts, 1996), and following settlement, reef fish use a variety of evolved functional traits to detect, avoid and discriminate between predators. Anthropogenic stressors may thereby disadvantage juvenile fish in affecting these physiological and behavioural adaptations.
Such has rung true for reef fish exposed to an increased oceanic partial pressure of CO2, whereby a loss of receptiveness to predator odors was observed. Munday et al. (2014) studied the impact of ocean acidification on juvenile damselfish species (Dascyllus aruanus and Pomacentrus moluccensis) and cardinalfishes (Apogon cyanosoma and Cheilodipterus quinquelineatus).
The olfactory preferences of individuals of each species from either CO2 seeps and control reefs were tested using a binary choice channel. As expected, all fish from control reefs strongly avoided channels containing predator odor. Contrarily, the fish from CO2 seeps showed an attraction to predator olfactory cues, spending 90% of their time in the channel containing predator odor.
To assess boldness, the maximum distance moved from habitat, total distance moved and amount of time spent in shelter was measured. The time of re-emergence was also recorded, following a simulated ‘chase’. Fish from CO2 seeps also showed elevated activity and boldness when compared to those from control reefs; travelling further from shelter and emerging six times faster following the ‘chase’.
Published in Nature Climate Change, rated impact factor of 18, this study is of crucial importance. The idea of ocean acidification affecting predator-prey interactions is not a novel finding; previous laboratory-based work has demonstrated a reduction in olfactory discrimination (Ferrari et al., 2015; Dixson, et al., 2010) and increased boldness resulting in a higher likelihood of mortality by predation (Munday et al., 2009). However, the findings of Munday et al. (2014) are of particular interest, as they support previous conclusions in a natural setting by utilising a ‘realistic’ experimental design in that they able to emulate long-term, predicted conditions for the future.
Ocean warming has also been shown to negatively influence inter-specific interactions (Allan et al., 2017). Using laboratory assays to employ a multi-stressor approach, Allan et al. (2017) investigated the independent and combined effects of elevated CO2 and warming on the predator-prey relationship between the dusky dottyback (Pseudochromis fuscus) and its prey, recruited common damselfish (Pomacentrus wardi).
Experimental fish were split into four treatment groups; control temperature – control CO2, high temperature – control CO2, elevated CO2 – control temperature and high temperature – elevated CO2. During trials, one individual of Ps. fuscus and one of Po. wardi that had been subjected to the same treatment were released into a tank and the proceeding interaction was filmed. Subsequent footage was then analysed to measure the following variables: capture success, attack rate, predation rate, predator attack distance and speed, prey reaction distance, directionality, prey escape distance and mean prey escape speed.
Allan et al. (2017) found predator success to be higher when individuals were exposed to either high temperature and elevated CO2 independently. Exposure to higher temperatures was found to increase attack and predation rates, with prey species displaying a decrease in reactivity and impaired directionality. Exposure to the combined stressors significantly affected prey escape speed, however contrary to previous study (Ferrari et al., 2015), Allan et al. (2017) did not observe an increase in predation rate.
Although published in Biology Letters, a journal with a substantially lower impact factor, this study remains of great importance primarily because it identifies the need for multiple anthropogenic stressors to be studied in coalition. Secondly, this study builds upon the work of Ferrari et al. (2015) which was the first to study the combined effects of the two stressors. However, whereas previous work could not ‘partition the role played by predator from prey’, Allan et al. (2017) use a novel technique to elucidate the impacts on separate trophic roles, whereby they show the functional traits of the predator species to be affected as well as the prey.
The changing ocean soundscape has also been shown to disadvantage functional traits in post-settled juvenile fish. Simpson et al. (2016) combined laboratory and field experiments to study the impact of anthropogenic noise on predator-prey dynamics using Dusky dottyback (Pseudochromis fuscus) and Ambon damselfish (Pomacentrus amboinensis), respectively.
Anti-predator behaviour was measured by simulating and filming ambush-predator strikes. Video analysis revealed that exposure to motorboat noise reduced the frequency and speed of response to simulated prey strikes; P. amboinensis were less likely to startle to predator attacks by six times and of the startled fish, the response to the stimulus was 22% slower.
Predator performance was also tested by measuring strike-success rate. In experiments with boat noise, P. fuscus capture of first P. amboinensis was facilitated by 74% fewer strikes, and 82% fewer strikes per P. amboinensis overall. A key finding was that boat noise playback in tanks increased mortality due to predation by 2.9 times, with similar results found in field experiments.
Published in Nature, an extremely well-reputed journal with an impact factor of 30, this study indicates that repeated exposure to anthropogenic noise has the potential to detrimentally impact fish demography. Previous work on anthropogenic noise has highlighted an effect on predator-prey dynamics but critically, Simpson et al. (2016) quantify the deleterious impacts on prey survival for the first time.
By interfering with key ecological interactions at a crucial life stage, there is the potential for chemical, heat-related and acoustic marine stressors to destabilize coral reef fish populations. Thus, it is of great importance that this area continues to be a priority for research. In order to influence policy and mitigation strategies for the future, a direction for future research can be identified; as anthropogenic stressors rarely occur alone, future studies may have increased predictive power if they are able to assess the combined impacts of multiple stressors and can evaluate any resulting antagonistic or synergistic effects.