Hypoxia-driven mortality events are increasingly recognized as an important component of the effect of climate change on coral reef ecosystems, yet such events are underreported because they are not targeted in standard monitoring programs. Here, we report mass die-offs of reef-associated fauna in 2014 and 2015 on Dongsha Atoll, a remote coral reef ecosystem in the South China Sea. Dongsha Atoll is a ring-shaped barrier reef encircling a lagoon that is flushed by tidal- and wind-driven currents. During May‑June of 2014 and 2015, calm conditions stalled water exchange with the surrounding sea, affecting the animals living in the reef system.

The objective of our report is to describe the mortality of coral reef fauna that occurred in the Dongsha Atoll lagoon in 2014 and 2015.

During May–June of 2014 and 2015, we observed mass mortality of thousands of fish in the families Apogonidae, Balistidae, Muraenidae, Pomacentridae, and Scorpaenidae in addition to cephalopods, gastropods, and crustaceans. The dead organisms were found in green turbid waters that were trapped inside the lagoon (Fig. 1). In the dead patch observed offshore, the decaying organisms were found only in a warm surface layer that was approximately 2 m thick, which we interpret as originating in the lagoon and then drifting off the reef.

The onset of mortality tended to coincide with neap tides and/or calm weather. Neap tides occurred on May 22, 2014, and June 10, 2015, each preceding a die-off event by 1–2 days (Fig. 1B). Although the mortality events observed on June 1, 2014, and June 16, 2015 did not occur during neap tides, current speeds on the adjacent reef flat at both of these times were relatively slow (<5 cm s-1) due to weak winds and small waves. Temperatures reached 30.2°C on May 23, 2014, 30.5°C on June 1, 2014, and 33.9°C on June 11, 2015 (data downloaded from http://www.bco-dmo.org/dataset/560618). Coral bleaching occurred on the eastern part of the reef flat during both 2014 and 2015 as a result of unusually calm weather and warm waters compared to the preceding several years. Bleaching on the reef flat in May–June 2014 was transient with little or no coral mortality, whereas bleaching in the later half of June through July 2015 caused 40% coral mortality. The coral bleaching events were separated from the die-offs that we report here by 1–2 km, and in 2015 the coral mortality occurred 1–2 months after our observations. Thus, while the coral bleaching and the die-offs that we observed seem to be distinct events, they both correspond to relatively calm weather and high water temperatures.

We suspect that the die-offs were caused by hypoxia because suffocating fish from Apogonidae and Pomacentridae families were swimming to the surface to gulp air. Oxygen saturation on the adjacent reef flat is typically <10% around dawn, even reaching anoxia for 30–60 min on some days, due to high rates of community metabolism. This depletion of oxygen might be exacerbated in the lagoon during calm conditions. Stagnant lagoon waters, combined with weak winds and high temperatures, could limit the input and solubility of oxygen in seawater. The reef fauna and flora- including any plankton blooms may rapidly consume the available oxygen, and its low concentration could be reinforced by the decomposition of decaying organisms. This situation may be viewed as a “fish-bowl” effect in which organisms are trapped in an isolated volume of water that becomes warm and possibly oxygen-starved.

If these die-off events were indeed caused by hypoxia, then to our knowledge this is the first report of such events on a submerged coral atoll without land separating lagoon and offshore waters. Dongsha Atoll is a marine protected area far from river discharges or human pollution, the common drivers of marine hypoxia. Rather, these die-offs occurred under the strong 2014–15 El Niño, which brought anomalously high temperatures and calm weather to the South China Sea. Hypoxia events on Dongsha Atoll, and potentially other reefs, could become more common as the oceans warm and weather patterns change.

We observed these die-off events while conducting separate studies. As such, we did not design a specific experiment to quantify the numbers of dead individuals nor did we measure oxygen levels directly within the dead zones.

Factors other than hypoxia may have contributed to the mass mortality events. Destructive fishing practices, including the use of explosives and cyanide, have reportedly been employed at Dongsha Atoll. However, we saw no evidence that these fishing methods were in use at the time of our observations, and we doubt that such fishing would cause mortality over as large an area as we observed. High water temperatures and/or acidification also cannot be ruled out entirely.

Die-off events like those we report are difficult to characterize because they are sporadic. Predicting these events will be important in forecasting coral reef futures, but doing so requires an understanding of the causes of dead zones. Our observations contribute to a relatively small but growing database of dead zones potentially related to hypoxia. Future studies characterizing the physical and chemical drivers of specific events, and meta-analyses of the common drivers of these events globally will be important for advancing our knowledge of coral reef responses to rapidly changing ocean habitats.

Mortality events were observed visually, and the dates and locations were recorded (Fig. 1A–B). The approximate sizes of some of the dead zones were estimated by traversing them with a motor boat. However, these sizes are considered crude estimates as they are approximated on the basis of one or two GPS points marked when crossing the dead zones once or twice. All observations were made during daylight hours, typically between 10:00 and 14:00 local time. Water depths varied from approximately 10 m at the edge of the lagoon to 2 m on the reef flat. Both expeditions (in 2014 and 2015) were 4 weeks in duration, and the reef was accessed by boat daily except for 5 days in each year when inclement weather prevented any observations.

Fonds De La Recherche Scientifique: FNRS (24880335) (Gajdzik).

Academie royale des Sciences, des Lettres et des Beaux-Arts de Belgique (Fonds Agathon De Potter) (Gajdzik).

We thank Keryea Soong, the Dongsha Atoll Research Station and Marine National Park, Professor Eric Parmentier and Dr. Bruno Frédérich (University of Liège), and Dr. Anne Cohen and Pat Lohmann (WHOI).

Not Applicable.