Reduced early life growth and survival in a fish in direct response to increased carbon dioxide

Absorption of anthropogenic carbon dioxide by the world’s oceans is causing mankind’s ‘other CO2 problem’, ocean acidification1. Although this process will challenge marine organisms that synthesize calcareous exoskeletons or shells2–6, it is unclear how it will affect internally calcifying organisms, such as marine fish7. Adult fish tolerate short-term exposures toCO2 levels that exceed those predicted for the next 300years (∼2,000ppm; ref. 8), but potential effects of increased CO2 on growth and survival during the early life stages of fish remain poorly understood7. Here we show that the exposure of early life stages of a common estuarine fish (Menidia beryllina) to CO2 concentrations expected in the world’s oceans later this century caused severely reduced survival and growth rates. When compared with present-day CO2 levels (∼400ppm), exposure of M. beryllina embryos to ∼1,000ppm until one week post-hatch reduced average survival and length by 74% and 18%, respectively. The egg stage was significantly more vulnerable to high CO2-induced mortality than the posthatch larval stage. These findings challenge the belief that ocean acidification will not affect fish populations, because even small changes in early life survival can generate large fluctuations in adult-fish abundance9,10. Since the industrial revolution, average atmospheric and oceanic CO2 concentrations have risen by 40% to 393 ppm (ref. 11; in 2011); levels that now far exceed those of the past one million years (180–280 ppm; ref. 12). Current emission scenarios predict that CO2 concentrations will increase further and reach ∼800 ppm during this century and potentially 2,000 ppm by the year 2300 (ref. 8). Apart from accelerating global climate change, another major concern is the absorption of CO2 by the world’s oceans and the resulting decrease in ocean pH, carbonate ion concentration (CO3) and calcium carbonate (CaCO3) saturation state (!; refs 1,2,4). Collectively known as ocean acidification, these shifts in marine chemistry will probably alter the phenotypes and hence the fitness of many marine organisms, particularly those with exoskeletons and shells made from calcium carbonate (CaCO3; ref. 3). Experimentally increased CO2 conditions have been shown to adversely affectmany species of foraminifers13, coccolithophores14, corals3, pteropodes2, bivalves5,6, crustaceans15 and echinoderms16. In contrast, direct effects of ocean acidification on fish, the world’s most important marine resource, are at present assumed to be negligible4,7,17. Fish calcify internal (bones, otoliths) rather than external skeletal elements, and as highly mobile vertebrates have evolved effective acid–base and osmoregulatory mechanisms to overcome high metabolic CO2 levels4. The high CO2 tolerance of juvenile and adult fish has been extensively documented for decades, suggesting no measureable growth or survival effects even at exposures of up to 16,000 ppm CO2 (ref. 7; eight times the relevant level for future climate change scenarios). However, the