Rapid onsets of warming events trigger mass mortality of coral reef fish Amatzia Genina,b,1,2, Liraz Levya,c, Galit Sharond, Dionysios E. Raitsose, and Arik Diamantf aThe Interuniversity Institute of Marine Sciences in Eilat, 88103 Eilat, Israel; bDepartment of Ecology, Evolution and Behavior, Silberman Life Science Institute, The Hebrew University of Jerusalem, 91904 Jerusalem, Israel; cNature and Parks Authority, 88000 Eilat, Israel; dNational Center of Mariculture, Israel Oceanographic and Limnological Research Institute, 88112 Eilat, Israel; eDepartment of Biology, National and Kapodistrian University of Athens, 15784 Athens, Greece; and fMorris Kahn Marine Research Station, Leon H. Charney School of Marine Science, University of Haifa, 3780400 Sdot Yam, Israel Edited by Nancy Knowlton, Smithsonian Institution, Washington, DC, and approved August 17, 2020 (received for review May 17, 2020) Our study reveals a hitherto overlooked ecological threat of warming has been bacterial infection (12, 13, 19, 20). Evidently, crowding climate change. Studies of warming events in the ocean have and enclosure facilitate pathogen transmission while preventing escape. In typically focused on the events’ maximum temperature and dura- accordance with this dichotomy between farmed and wild fish, the com- tion as the cause of devastating disturbances in coral reefs, kelp mon understanding is that the effect of global warming on the latter will be forests, and rocky shores. In this study, however, we found that gradual, emerging through long-term physiological changes, alterations in the rate of onset (Ronset), rather than the peak, was the likely trig- habitat structures, and modified productivity and trophic pathways (7, ger of mass mortality of coral reef fishes in the Red Sea. Following 21–25). A review of 727 events of mass mortalities of wild animals during a steep rise in water temperature (4.2 °C in 2.5 d), thermally the past ∼75 y (26) found that over half of the documented cases of mass stressed fish belonging to dozens of species became fatally in- mortality events in wild fish followed incidents of cooling whereas events fected by Streptococcus iniae. Piscivores and benthivores were dis- related to hot thermal stress in fish started to appear only in the 1980s. proportionately impacted whereas zooplanktivores were spared. Along that line, a recent compilation of opinions, in which 33 experts listed Mortality rates peaked 2 wk later, coinciding with a second warm- crucial knowledge gaps in our understanding of the impacts of climate ∼ ing event with extreme Ronset. The epizootic lasted 2 mo, extend- change on coral reef fishes (27), did not even consider mass mortalities as a ing beyond the warming events through the consumption of consequence of warming. Here, we challenge those views, showing how pathogen-laden carcasses by uninfected fish. The warming was warming events with high Ronset threaten the survival and sustainable widespread, with an evident decline in wind speed, barometric functioning of fish communities in coral reefs. ENVIRONMENTAL SCIENCES pressure, and latent heat flux. A reassessment of past reports sug- gests that steep Ronset was also the probable trigger of mass mor- Results and Discussion talities of wild fish elsewhere. If the ongoing increase in the A warming event with an unprecedented Ronset (4.2 °C rise of sea frequency and intensity of marine heat waves is associated with surface temperature [SST] in 2.5 d) (Fig. 1A) occurred over the a corresponding increase in the frequency of extreme Ronset, ca- coral reefs of Eilat, northern Red Sea, in early July 2017. This lamities inflicted on coral reefs by the warming oceans may extend outstanding Ronset was the steepest recorded since daily mea- far beyond coral bleaching. surements started 32 y ago (Fig. 1 C and D). A second event of ECOLOGY warming with extreme Ronset occurred 2 wk later (14 to 16 July) epizootic | warming rate | Streptococcus | heat flux | Red Sea Significance arine heat waves (MHWs) and heat spikes—a prolonged — Mdiscrete event with anomalously warm water (1) have Our study reveals a hitherto overlooked effect of warming on become more frequent as the global ocean warms (2, 3). Some of coral reefs. Traditionally, ecological studies of warming events those events have triggered profound changes in marine com- focused on maximum temperatures and duration, rather than munities, among them a catastrophic, world-wide degradation of the rate of warming at the onset. Here, we show that onsets coral reefs due to bleaching (4, 5), a tropicalization of benthic can trigger widespread mortality of reef fish. Hundreds of communities along the coast of Western Australia (6, 7), and a thermally stressed fish, belonging to dozens of species, became devastation of the gorgonian-dominated community along the fatally infected with a common pathogen in the Red Sea. Dif- northeast coast of the Mediterranean Sea (8, 9). In most cases, ferential susceptibility led to selective mortality, with dispro- widespread mortalities that preceded those changes affected portional death among predators and benthic feeders. A nonmotile organisms, such as stony corals, gorgonians, seaweeds, reassessment of past reports suggests that extreme onset mollusks, and sponges (4, 5, 7–9). Unlike motile animals that can might have been an overlooked trigger of fish kills elsewhere. escape warming events by descending to deeper water (10, 11), Warming tropical and subtropical reefs may face an increasing sedentary organisms lack the ability to move away. In the few frequency of extreme onsets, eliciting calamities far beyond cases where the mortality of wild fish was attributed to MHWs, coral bleaching. either the warming conditions were not substantiated with measurements (12–14), the trigger of mortality remained unclear Author contributions: A.G., L.L., G.S., and A.D. designed research; A.G., L.L., G.S., D.E.R., and A.D. performed research; G.S. and A.D. contributed new reagents/analytic tools; A.G., (6, 15), or other factors, such as toxic algal bloom (13, 14) or L.L., D.E.R., and A.D. analyzed data; A.G., L.L., G.S., D.E.R., and A.D. wrote the paper; and hypoxia (16), turned out to be the cause of death. As shown below, an D.E.R. performed the remote-sensing analyses. anomalous rate of onset (Ronset), defined as the rate of warming at the start The authors declare no competing interest. of a warming event (1), can be a trigger for widespread mortality of reef This article is a PNAS Direct Submission. fish. Note that our definition of Ronset refers to the maximum rate of Published under the PNAS license. warming observed during the course of warming, not necessarily the one 1Present address: Ocean and Coasts Program, Global Change Institute, University of ending with the event’s maximum temperature, as defined by Hobday et al. Queensland, St. Lucia, QLD 4072, Australia. (1). Mass mortalities of cultured fish following an abrupt rise in temper- 2To whom correspondence may be addressed. Email: [email protected]. ature are common among farmed fish as they are enclosed in cages or This article contains supporting information online at https://www.pnas.org/lookup/suppl/ ponds from which they cannot escape (12, 13, 17, 18). Aside from cases of doi:10.1073/pnas.2009748117/-/DCSupplemental. hypoxia, a ubiquitous cause of death of farmed fish following abrupt www.pnas.org/cgi/doi/10.1073/pnas.2009748117 PNAS Latest Articles | 1of8 Downloaded by guest on September 29, 2021 event occurred in early summer, the maximum temperature (28.6 °C) reached was by no means exceptional for that season (Fig. 1B). Indications of an unusual occurrence of fish death emerged 2 d after the start of the first warming event, with the more ex- treme Ronset, when carcasses of two parrotfish and two groupers were observed lying on the seabed on 4 July (Fig. 2). Nine ad- ditional carcasses were found 2 d later, and 10 more on the following day (Fig. 3A). Normally, findings of fish carcasses were rare in the coral reefs of Eilat (SI Appendix, Fig. S1). Following the realization that this unusual finding of many carcasses might indicate a start of widespread mortality, a citizen-science cam- paign was initiated, through which divers and swimmers were asked to search for carcasses, record their findings, and remove the carcasses from the sea. Mortality rates peaked during the campaign’s third week, following the second extreme Ronset (Fig. 1A), when 104 carcasses were found (Fig. 3A). The epizo- otic lasted 10 wk, with declining carcass sightings during the second week of August (6 wk after the warming event), and a return to normal levels in early September (Fig. 3A). In total, 427 fish carcasses belonging to 28 families (at least 42 species) were collected during the event. Carcasses were found along the entire coast of Eilat (11.4 km), extending from the sandy beaches near the northern end of the Gulf (sites 1 to 4 in Fig. 3B) through the coral reefs in the south (site 21 in Fig. 3B). The highest number was recorded within the protected reef of the nature reserve (site 14 in Fig. 3B). Our records undoubtedly underestimated the true extent of the mortality since some carcasses had been missed by observers, and others might have been devoured by predators and scaven- gers (Movie S1). Many carcasses (41%) were found floating, about one-third lying on the bottom, and the remainders washed ashore. The maximum depth at which carcasses were found on the seabed was 25 m. While searches were most intensive in the shallows, a handful of technical and scientific divers recurrently examined the deep reefs, down to 60 m, at sites 9, 10, and 15 to 17 (Fig. 3B), but found no carcasses at those depths.