Sulfide exposure accelerates hypoxia-driven mortality

The effect of the presence of sulfide on the survival of benthic organisms under hypoxia was tested using a meta-analysis of published experimental results evaluating the effects of the presence of hydrogen sulfide on the median survival time of benthic macrofauna under hypoxia. The meta-analysis confirmed that survival times under hypoxia are reduced by an average of 30% in marine benthic communities exposed to hydrogen sulfide. The effect of sulfide on survival was higher for egg forms than for juvenile or adult stages. The aggravation of the negative effects of spreading hypoxia in the presence of sulfide suggests that the threats derived from hypoxia to marine biodiversity are greater than anticipated on the basis of the direct effects of low oxygen concentration alone. Dissolved oxygen is a property that has changed drastically in a short period of time in the marine environment (Diaz and Rosenberg 1995; Diaz 2001). Oxygen deficiencies have increased in frequency, duration, and severity in the world’s coastal areas during recent decades (Diaz and Rosenberg 2008), and as a consequence hypoxia is emerging as a major threat to marine biodiversity (Vaquer-Sunyer and Duarte 2008). Hypoxia reduces the abundance and diversity of the benthic macrofauna (Josefson and Widbom 1988; Rosenberg et al. 1991; Gray et al. 2002) and affects the structure and function of marine ecosystems (Wu 2002). Changes in the benthic macrofauna community observed after episodes of severe oxygen deficiency indicate differential tolerance to oxygen concentrations (Diaz and Rosenberg 1995), with mollusks and polychaetes being typically more tolerant to oxygen deficiency than echinoderms, fishes, and crustaceans (Theede et al. 1969; Taylor and Spicer 1987; Levitt and Arp 1991). These differences in tolerance are reflected also in the length of time organisms survive under hypoxia (VaquerSunyer and Duarte 2008). However, the onset of hypoxia is followed by a number of changes in the ecosystem that significantly affect the conditions for further organismal survival (Conley et al. 2009). In particular, as hypoxia progresses, benthic microbial communities shift to sulfate reduction, and sulfide concentrations increase in the environment (Conley et al. 2009). When oxygen is not available to oxidize organic matter, prokaryotes utilize alternative electron acceptors such as sulfate, nitrate, nitrite, or metal oxides. Sulfate is normally the most abundant, and its reduction has sulfide as an end product (Berner 1984). Sulfide is always present in the anoxic layer of marine sediments (Fenchel and Jorgensen 1977) and its diffusion into bottom water is controlled by the oxic sediment depth, dictated by the rate of oxygen diffusion and the oxygen consumption in the sediment (Vistisen and Vismann 1997). During hypoxic events, the anoxic layer of the sediments migrates upwards and can reach the water column, with sulfide intrusion into the bottom water. Sulfide is very toxic to most aerobic organisms because of its inhibition of cytochrome c oxidase activity at micromolar (mmol L21) concentrations (Nicholls 1975b; Petersen 1977; Nicholls and Kim 1982). Sulfide binds with high affinity to the ferric iron in the heme site of cytochrome aa3 (Nicholls 1975a). The interaction of sulfide with blood proteins such as hemoglobin, binding to the hemoglobin porphyrin ring (Berzofsky et al. 1971), reduces oxygen delivery to mitochondria in some species (Evans 1967). As sulfide increases during hypoxia, the macrofauna is also exposed to sulfide, so that benthic mass mortalities during hypoxic events may be a consequence of both sulfide toxicity and hypoxia rather than low oxygen concentration alone (Vistisen and Vismann 1997). Environmental stressors can have additive effects in shortening survival time of marine organisms under hypoxia, such as increasing temperature, increased pCO2 levels in the ambient waters (Portner and Farrell 2008), and the presence of hydrogen sulfide and contaminants, among others. Here we test whether the presence of sulfide affects survival of benthic animals under hypoxia. More specifically, we use a meta-analysis of published experimental results examining the survival of benthic organisms under both hypoxia and the presence of sulfide to evaluate the effects of the presence of hydrogen sulfide on the median survival time of benthic macrofauna under hypoxia.