Paper Reviewed
Clark, T.D., Raby, G.D., Roche, D.G., Binning, S.A., Speers-Roesch, B., Jutfelt, F. and Sundin, J. 2020. Ocean acidification does not impair the behavior of coral reef fishes. Nature 577: 370-375.

In an incredibly important and revealing paper published in the journal Nature, Clark et al. (2020) write that "establishing a robust and independently replicated database of the effects of ocean acidification on fishes is essential to gain reliable understanding of the consequences of climate change on marine ecosystems." Such a database, they add, is critical "before drawing broad conclusions and implementing management measures."

Unfortunately, too many have been far too eager to jump to conclusions when it comes to estimating the impacts of ocean acidification. And in this regard, Clark et al. note that "a number of highly publicized studies have reported detrimental effects of elevated CO2 levels on the sensory systems and behaviors of fishes, with coral reef fishes appearing to be the most sensitive despite experiencing large daily and seasonal fluctuations in nature (for example, 100-1,300 µatm)." Such projected detrimental effects include "alterations in olfaction, hearing, vision, learning, behavioral lateralization, activity levels, boldness, anxiety and susceptibility to predation," which have led to "dire predictions for fish populations and marine ecosystems."

But how solid is this body of research?

Clark et al. note there are two important red flags that call the pessimistic ocean acidification projections of fish into question. First, fish are well-known for having robust acid-base regulatory systems that help them maintain tissue pH, even under extreme partial pressure levels of CO2 (pCO2) that exceed end-of-century pCO2 forecasts by 15 times (i.e., 15,000 µatm). Second, they note that there are "substantial disparities [in published ocean acidification impacts] among studies and species, even when methodological approaches are similar." And so, to address these concerns, the team of seven scientists "commenced a three-year research program in 2014 to quantify the effects of end-of-century ocean acidification on the sensory and behavioral ecology of coral reef fishes." In doing so, they replicated and built upon "some of the most prominent studies in this field to understand the diversity in behavioral responses within and across species." Furthermore, they raised the bar and enhanced the transparency of their work by fully documenting their methods and providing raw data to the public so that their work could be easily replicated by others.

And what did their work reveal?

Their study focused on three main research of ocean acidification research on fish: (1) chemical cues from predators, (2) activity levels and (3) behavioral lateralization. With respect to chemical cues, Clark et al. "quantified the effects of elevated CO2 on predator cue avoidance across 3 consecutive years in 560 individuals from 6 species of pomacentrid coral reef fishes." Results of this segment of their analysis revealed that "none of the coral reef fishes that we examined exhibited attraction to predator cues when acclimated to high CO2 levels, in contrast to previous reports on the same and other species." Furthermore, they used statistical procedures to compare their data with prior datasets and found that "the [negative] results reported previously for coral reef fishes are highly improbable (probability of 0 out of 10,000)...show[ing] no evidence of CO2 effects on chemical cue avoidance."

With respect to activity levels, Clark et al. note that prior studies indicate there is up to a 90-fold increase in activity in coral reef fishes exposed to end-of-century CO2 levels. However, they report "most activity measurements (for example, distances moved) from coral reef fishes have not used video footage but have been made using direct manual observations" that are subjective in nature. For their analysis, Clark et al. "filmed 582 individuals from 6 species across 3 years and quantified swimming activity in behavioral arenas using automated tracking software." The end result of this second focus was the observation that "fish exposed to high CO2 did not exhibit consistently elevated activity levels compared with conspecifics under control conditions." In contrast, they found that "activity levels were highly variable among individuals, increasing the risk of type-1 errors in experiments using small sample sizes, and possibly in large-sample experiments that rely on human observation rather than automated video analysis."

Finally, with respect to behavioral lateralization, the researchers investigated this trait using 175 fishes across four species. Results indicated that there was no CO2 effect on population-level behavioral lateralization.

In commenting on their findings, Clark et al. state the obvious, that "in contrast to previous studies on the same and closely related species, we found no consistent detrimental effects of end-of-century CO2 levels on the avoidance of predator chemical cues, activity levels or behavioral lateralization." Consequently, they conclude that "on the basis of our findings on more than 900 wild and captive-reared individuals of 6 species across 3 years, we conclude that acclimation to end-of-century levels of CO2 does not meaningfully alter important behaviors of coral reef fishes." Therefore, they say "the catastrophic projections for fish sustainability based on CO2-induced behavioral impairments must be reassessed in light of our findings."