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Effects of global change on the social behaviour of marine organisms

Periodic Reporting for period 1 - GlobChangeBehav (Effects of global change on the social behaviour of marine organisms)

Reporting period: 2018-04-01 to 2020-03-31

Marine global change stressors such as ocean acidification (OA) and warming (OW) are expected to impact marine organisms and ecosystems in various ways. One of the ways in which marine global change might inflict ecosystem-level changes is through altering animal behaviour. Thus, understanding how OA and OW affect the behaviour of animals that are important for ecosystem processes is crucial for predicting ecosystem effects of marine global change. Given that humans have a strong association and reliance on marine ecosystems as a source of food and recreation, understanding how these systems may function in the future is very important from a societal perspective.

The initial objectives of this project were to understand the impacts of OA and OW on social behaviours in marine animals, using invertebrates and fish as model organisms. We proposed to conduct experiments on three main areas of interest: 1) shoaling behaviour in fish and invertebrates; 2) aggregative behaviours in echinoderms; and 3) a transgenerational assessment of global change effects on fish behaviour and physiology.

Unfortunately, the questions posed initially for this project (in 2016) had been largely studied when the project started in 2018, and we decided to slightly alter the questions of interest that we would tackle in our experiments to be more impactful from a scientific perspective and to have a strong socioeconomic component. We decided to focus our attention on OA and OW effects on animal behaviour in the context of behavioural repeatability. To test behavioural repeatability in the context of marine global change, we chose two organisms and two different behaviours : 1) valve closure responses to tactile predator cues in bivalves; and 2) self-righting responses in sea stars (rather than aggregative behaviours). In addition to these experiments, the relevant literature review for the project gave light to a meta-analysis regarding the effects of OA on marine fish behaviour.
The project started in late August, 2018, which resulted in a delay in starting empirical experiments. During this time, we conducted a systematic literature search and meta-analysis to determine factors driving behavioural responses of fish to ocean acidification. We found that the reported effects of OA on fish behaviour were not explained biologically, but were predominantly associated with study sample size (large effects were restricted to studies with small samples sizes) and publication bias (large effects published in high-impact, prestigious journals). A manuscript for this aspect of the project is written and we recently approached the journal 'Nature' regarding publication.

Two long-term experiments were conducted at the Kristineberg Marine Research Centre in Sweden. The first experiment tested effects of long-term exposure to OA and OW on responses to predators in blue mussels and the repeatability of such responses. Mussels were exposed to OA and OW conditions for 3 months and individual responses to predators were assessed over 4 repeated trials at the end of the exposure. We found that OW, but not OA, affected mussels' response to predators by causing them to remain closed for a longer period of time after being attacked. We also found that smaller mussels took longer to open than larger mussels, that this behaviour was highly repeatable, and that mussels generally reduced the time spent closed as trials progressed. A manuscript for this experiment has been drafted and will soon be submitted for primary publication in a peer-reviewed journal (likely 'Proceedings of the Royal Society B').

The second experiment tested for the effects of ocean acidification and warming on self-righting in sea stars and its repeatability. Sea stars were exposed to OA and OW conditions just as the mussels were and at the end of the exposure, repeated self-righting trials were conducted over a 7-day period. This experiment was repeated twice. Functionally, the design of this experiment allowed us to test hypotheses regarding the role of repeated measurements at multiple scales in global change-behaviour experiments. Interestingly, we found that OW, but not OA, increased self-righting times in sea stars, but this effect was only apparent on the first day of repeatability trials in the first experiment. For the rest of the trials, we observed no effect of OA or OW and a global analysis including all experiments and trials revealed no significant effect of OA or OW on self-righting. Additional data analysis for this project is still being conducted and a manuscript will be prepared for peer-reviewed publication within the next 4-6 months (likely a submission to the journal 'Global Change Biology').
Our experiment regarding mussel valve closures has implications for the roles of mussels as ecosystem engineers. When closed, mussels cease feeding and thus are not filtering water. This can affect mussel growth and filtering activity. Given that mussels under high temperatures remained closed longer, their condition and filtering capacity may be affected. Indeed our results corroborate previous studies suggesting that mussels are sensitive to high temperatures. Given the ecological and economic roles of bivalve globally, our results have societal implications for the sustainability of bivalve fisheries and aquaculture and the role of bivalves in water filtration.

Secondly, we found no effect of OA on animal behaviour in both of our empirical experiments, and found that reports of OA effects on fish behaviour may be compounded by poor methodology (low sample size) and publication bias. These results corroborate well with a study recently conducted by F. Jutfelt and colleagues in which the strong effects of OA on coral reef fishes reported in previous studies could not be empirically replicated. Collectively, these results suggest that OA may not have as severe of an effect on animal behaviour as has been thought for the past decade. This has societal implications for management and conservation strategies for fish populations in the face of ocean acidification. For example, management strategies using previous reports of OA on fish behaviour may be unnecessarily altering management practices. Ultimately, the results of this project cast doubt on OA effects on animal behaviour.

At a broad scale, the project's results have major implications for how science regarding environmental stress and animal behaviour is conducted. The meta-analysis found that severe effects of oA were restricted to studies with low samples sizes - specifically studies that employed a sample size of less than 30 fish per experimental treatment. Furthermore, the sea star experiment suggested that, when sample sizes are low, spurious effects can be detected that may not actually exist if experiments are not repeated. These findings have important implications for how experiments regarding climate change and animal behaviour are conducted, suggesting that to have confidence in experimental results, such studies should, when possible, employ a baseline sample size of 30 individuals and should repeat behavioural assays. Furthermore, the results provide two easy-to-assess aspects of global change-behaviour studies for scientists and non-scientists to determine the reliability of results from global change-behaviour studies.
Water with and without mussels 1 hour after adding concentrated algae
Sea stars in bucket
Single mussel open and filtering water