Near-future CO2 levels impair the olfactory system of a marine fish

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.

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.

Many marine fish and invertebrates show a dual life history where settled adults produce dispersing larvae. The planktonic nature of the early larval stages suggests a passive dispersal model where ocean currents would quickly cause panmixis over large spatial scales and prevent isolation of populations, a prerequisite for speciation. However, high biodiversity and species abundance in coral reefs contradict this panmixis hypothesis. Although ocean currents are a major force in larval dispersal, recent studies show far greater retention than predicted by advection models. We investigated the role of animal behavior in retention and homing of coral reef fish larvae resulting in two important discoveries: (i) Settling larvae are capable of olfactory discrimination and prefer the odor of their home reef, thereby demonstrating to us that nearby reefs smell different. (ii) Whereas one species showed panmixis as predicted from our advection model, another species showed significant genetic population substructure suggestive of strong homing. Thus, the smell of reefs could allow larvae to choose currents that return them to reefs in general and natal reefs in particular. As a consequence, reef populations can develop genetic differences that might lead to reproductive isolation.