In:
Proceedings of the National Academy of Sciences, Proceedings of the National Academy of Sciences, Vol. 109, No. 24 ( 2012-06-12)
Abstract:
The information presented here is important for society and coastal managers, because we confirm that sediments washed off the land may be damaging to coral reefs and that nutrient enrichment of as little as 1% in sediments washed off the land is potentially detrimental for coral reefs. The sustainable use of the coastal vegetative zones and upland development is essential to minimize the runoff of organic matter and sediment, because at present local and regional prevention of reef degradation from terrestrial runoff is the only way to slow the decline in coral reefs at a time of mounting reef damage from global warming and ocean acidification. We then tested which factor initially might have caused the death of the coral by conducting tank experiments without the use of sediment. In these experiments we used different combinations of oxygen and sulfide concentrations and pH in water. Corals survived in conditions without oxygen at pH 8.2 for the tested 4 d. In addition, air-saturated oxic water with pH 7 did not harm corals for 4 d. In contrast, the combination of anoxia and pH 7 was fatal within 1 d. The role of hydrogen sulfide as an accelerator of coral damage was demonstrated in an experiment in which we first exposed corals to oxygen-free water and pH 7 for 12 h and then added hydrogen sulfide in moderate concentrations. Under these conditions the corals were killed after another 3 h. We therefore demonstrated that the combined effect of adverse conditions (anoxia and pH 7) within a thin layer of sediment enriched with nutrients kills coral within 24 h. We propose that coral is damaged irreversibly by a combination of acidification and anoxia, which is a consequence of microbial activity in the sediment layer, and that this process is accelerated by hydrogen sulfide produced from the degradation of coral tissue once the first coral tissue has died. We designed several experiments following the analysis of natural sediment from sediment traps and measuring the conditions in naturally accumulated sediment on corals in the Great Barrier Reef of Australia. First, we mixed sediments with homogenized plankton to produce sediment with four different concentrations of organic matter. Mesocosm experiments were used in which the sediments were suspended and allowed to settle to form a layer about 2.5 mm thick on pieces of the broad, flat (foliose) coral Montipora peltiformis . After each treatment, the sediment was washed off, and the coral pieces were inspected visually. Additionally, the photosynthetic yield (specifically, the first quantum yield in what is termed “photosystem II”) of zooxanthellae, the single-celled algal symbionts in the coral’s tissue, was measured as a proxy for the fitness of the living coral–algae organism (also termed a “holobiont”). Microelectrodes were used to measure profiles of oxygen, hydrogen sulfide, and pH in the sediments over a 6-d period. At the same time, radiolabeling techniques were used to determine rates of sulfate reduction in the sediment deposited on the coral. These datasets ( Fig. P1 ) showed that after 24 h of exposure to enriched sediment, the first spots of dead coral tissue were visible, even though hydrogen sulfide concentrations in the sediment were low. After 48 h, when hydrogen sulfide concentrations were high, large areas of tissue of the sediment-covered coral were dead or degraded. We then applied a mathematical model to show that the hydrogen sulfide concentrations measured after 24 h were 10 times higher and after 48 h were 370 times higher than could be explained by sulfate reduction in the sediment only. The model also showed that hydrogen sulfide did not originate from the sediment but primarily was produced below the sediment layer, i.e., from degrading coral tissue. Thus, the coral died before sulfide concentrations were high, and the death occurred because of other factors. In coastal areas, the combination of sediments and nutrients causes mineral and organic particles to aggregate, sink to the bottom, and eventually cover corals ( 2 ). Previous studies ( 3 ) have shown that thin layers of sediments with certain properties might kill corals within 24 h. The major microbial process in anoxic marine sediments is sulfate reduction by bacteria, which leads to the production of hydrogen sulfide ( 4 ). Hydrogen sulfide is a potent toxin to most organisms. Initially, we hypothesized that organic enrichment in sediment enhances sulfate reduction, resulting in the production of toxic hydrogen sulfide, which then kills the coral. Worldwide, coral reefs are at risk from sediments and nutrients that are brought to the sea by run-off from land as a function of massive coastal deforestation and development, which leads to the destabilization of upland and intertidal sediments ( 1 ). Here, we investigated the mechanisms leading to the rapid death of corals when exposed to run-off and sedimentation, hypothesizing the involvement of microbes. We conducted a series of microcosm experiments of natural and organic-rich sediment, taking oxygen concentrations, pH, and hydrogen sulfide concentrations into account. We found that adverse conditions (anoxia and pH 7) within a thin layer of enriched sediment cause the death of coral and propose that this process is accelerated by hydrogen sulfide produced from the microbial degradation of coral tissue. We show that it is important to understand the underlying mechanisms of this detrimental process to improve coastal management practices in efforts to protect coral reefs against this major threat and to promote the sustainable use of tropical coastal habitats.
Type of Medium:
Online Resource
ISSN:
0027-8424
,
1091-6490
DOI:
10.1073/pnas.1100715109
Language:
English
Publisher:
Proceedings of the National Academy of Sciences
Publication Date:
2012
detail.hit.zdb_id:
209104-5
detail.hit.zdb_id:
1461794-8
SSG:
11
SSG:
12
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