Responses of pink salmon to CO2-induced aquatic acidification

The persistence of most coastal marine species depends on larvae finding suitable adult habitat at the end of an offshore dispersive stage that can last weeks or months. We tested the effects that ocean acidification from elevated levels of atmospheric carbon dioxide (CO(2)) could have on the ability of larvae to detect olfactory cues from adult habitats. Larval clownfish reared in control seawater (pH 8.15) discriminated between a range of cues that could help them locate reef habitat and suitable settlement sites. This discriminatory ability was disrupted when larvae were reared in conditions simulating CO(2)-induced ocean acidification. Larvae became strongly attracted to olfactory stimuli they normally avoided when reared at levels of ocean pH that could occur ca. 2100 (pH 7.8) and they no longer responded to any olfactory cues when reared at pH levels (pH 7.6) that might be attained later next century on a business-as-usual carbon-dioxide emissions trajectory. If acidification continues unabated, the impairment of sensory ability will reduce population sustainability of many marine species, with potentially profound consequences for marine diversity.

While ocean acidification is predicted to threaten marine biodiversity, the processes that directly impact species persistence are not well understood. For marine species, early life history stages are inherently vulnerable to predators and an innate ability to detect predators can be critical for survival. However, whether or not acidification inhibits predator detection is unknown. Here, we show that newly hatched larvae of the marine fish Amphiprion percula innately detect predators using olfactory cues and this ability is retained through to settlement. Aquarium-reared larvae, not previously exposed to predators, were able to distinguish between the olfactory cues of predatory and non-predatory species. However, when eggs and larvae were exposed to seawater simulating ocean acidification (pH 7.8 and 1000 p.p.m. CO2) settlement-stage larvae became strongly attracted to the smell of predators and the ability to discriminate between predators and non-predators was lost. Newly hatched larvae were unaffected by CO2 exposure and were still able to distinguish between predatory and non-predatory fish. If this impairment of olfactory preferences in settlement-stage larvae translates to higher mortality as a result of increased predation risk, there could be direct consequences for the replenishment and the sustainability of marine populations.

There is increasing concern that ocean acidification, caused by the uptake of additional CO(2) at the ocean surface, could affect the functioning of marine ecosystems; however, the mechanisms by which population declines will occur have not been identified, especially for noncalcifying species such as fishes. Here, we use a combination of laboratory and field-based experiments to show that levels of dissolved CO(2) predicted to occur in the ocean this century alter the behavior of larval fish and dramatically decrease their survival during recruitment to adult populations. Altered behavior of larvae was detected at 700 ppm CO(2), with many individuals becoming attracted to the smell of predators. At 850 ppm CO(2), the ability to sense predators was completely impaired. Larvae exposed to elevated CO(2) were more active and exhibited riskier behavior in natural coral-reef habitat. As a result, they had 5-9 times higher mortality from predation than current-day controls, with mortality increasing with CO(2) concentration. Our results show that additional CO(2) absorbed into the ocean will reduce recruitment success and have far-reaching consequences for the sustainability of fish populations.