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Rapid Onsets of Warming Events Trigger Mass Mortality of Coral Reef Fish

Rapid Onsets of Warming Events Trigger Mass Mortality of Coral Reef Fish

Rapid onsets of warming events trigger mass mortality of reef

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, ; 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 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 in the Red . Following 21–25). A review of 727 events of mass mortalities of wild 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 . 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 , in early July 2017. This lamities inflicted on coral reefs by the warming may extend outstanding Ronset was the steepest recorded since daily mea- far beyond . 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 , 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 (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 (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/ 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 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. The three dominant families among the carcasses were par- rotfish (Scaridae), groupers (Serranidae), and (Balistidae) (Fig. 4A). An analysis using Chesson’s Index of Se- lectivity α (28), comparing the proportions of different functional groups among the carcasses to those found in the local reefs prior to the die-off event, indicated that piscivores (mostly groupers) and benthic grazers (mostly parrotfish) were dispro- Fig. 1. Water temperature at the coral reef of Eilat. (A) Time series of portionately affected whereas zooplanktivores (damselfish, reef temperature recorded every 10 min at 2 m depth from 1 May to 13 Sep- — tember 2017. Rectangles indicate the extreme R of the two successive anthias) the most abundant guild of fish on local coral reefs onsets — warming events. The first Ronset (red rectangle) was steeper, with the water (29) were rarely affected (Fig. 4). Were zooplanktivores truly warming up by 4.2 °C in 2.5 d (24.4 to 28.6 °C between predawn 2 July and spared, or were their carcasses relatively hard to find? While

late afternoon on 4 July). During the second Ronset (14 to 16 July; green most fish belonging to this guild were small (<10 cm in length), it rectangle), the water warmed by 3.4 °C in 2.5 d (25.1 to 28.5 °C). (B) Time was unlikely that their paucity among the collected carcasses was series of daily means of water temperature during the period June to Sep- due to their obscurity. Dozens of research divers regularly op- tember in the years 2007 to 2016 and 2018 (blue lines) and 2017 (black line). erated in the Interuniversity Institute (IUI) coral reef (site 17 in ’ The red and green rectangles are as in A. Note that, despite the event s Fig. 3B) during the die-off period but found no carcasses of those extreme R , the peak temperatures in July and August 2017 remained onsets planktivorous fish. Moreover, in an unrelated study, in which 10 well within the normal range for summers in Eilat. (C) Mean daily increase in = SST over three consecutive days since 1988 at the coral reef of Eilat (32 y). groups of coral-inhabiting damselfish (Dascyllus marginatus; n Only positive (warming) values are plotted. Note that the maximum 46) were individually tagged in situ, none disappeared during the warming rate in July 2017 shown in C was lower than that shown in A be- epizootic. cause the daily measurements, recorded every morning between 8–9 AM, Most of the dead fish were large adults (>30 cm in length). missed the coldest (predawn) and warmest (late afternoon) hours of the day. Many had bright red gills, indicating that they died shortly before (D) Frequency distribution of the daily increase in SST in the 32-y-long time sighting. In some cases, moribund fish exhibited disoriented series shown in C. The red and green arrows indicate the first and second movements or were lying on the seabed, still ventilating (Movies Ronset, respectively. S2 and S3). Moribund and freshly dead specimens were imme- diately taken to the pathology laboratory for examination. Nec- ropsies were performed on 14 fish belonging to eight different when the water warmed by 3.4 °C in 2.5 d (25.1 to 28.5 °C) species (SI Appendix, Table S1). Clear evidence of severe in- (Fig. 1A). Temperatures remained high (>28 °C) for 2 or 3 d fection by Streptococcus iniae was found in 13 cases. The infec- after the first and second onsets, respectively. As the warming tions were found in the blood, spleen, liver, kidney, and brain. In

2of8 | www.pnas.org/cgi/doi/10.1073/pnas.2009748117 Genin et al. Downloaded by guest on September 29, 2021 Fig. 2. Fish carcasses photographed during the summer 2017 die-off event in Eilat. Photographs are numbered as follows: 1, assasi (Arabian picassofish); 2 and 5, Variola louti (grouper); 3, Arothron hispidus (white-spotted puffer); 4, Siganus rivulatus (marbled spinefoot); 6, Cheilinus lunulatus (broomtail ); 7, fuscopurpureus (purple brown parrotfish); 8, partly eaten Scarus gibbus (heavybeak parrotfish); 9, Tetrosomus gibbosus (humpback turretfish); and 10, Chaetodon fasciatus (diagonal butterflyfish). (Yellow scale bars: ∼5cm.)

all 13 individuals, S. iniae was the only pathogenic bacterium support the hypothesis that the warming event was the outcome isolated. The single fish lacking S. iniae was heavily infected by of a broader atmospheric mechanism. Vibrio sp. Of the two occurrences of extreme Ronset, the first (2 to 4 July; S. iniae is a ubiquitous pathogen of fish, found throughout the +4.2 °C in 2.5 d) (Fig. 1A) appeared to be the trigger of the ENVIRONMENTAL SCIENCES world’s warm waters (19), including the northern Red Sea (30). epizootic as it corresponded with the start of fish die-off (4 July). While nonsymptomatic fish may be covert carriers of this bac- The later, less extreme Ronset (14 to 16 July; +3.4 °C in 2.5 d) terium (20), a healthy immune system normally prevents debili- probably exacerbated the fish death, leading to the correspond- tating infections from developing. Our visual, microscopic, and ing peak in the number of recorded carcasses (Fig. 3A). molecular examination of the carcasses did not reveal unusual The virulence of Streptococcus infection in fish depends on occurrences of parasites or infections by other pathogens. The both the state of the individual’s immune system and the dose identification of S. iniae was based on cultures isolated from introduced (17, 20). Therefore, a consumption of -laden ECOLOGY infected organs, followed by molecular analysis. Fish infected by carcasses (photograph 8 in Fig. 2 and Movie S1) likely contrib- S. iniae typically show acute signs of bacteremia, meningo- uted to the spread of the infection (33). Correspondingly, all but encephalitis, and panophthalmitis (14, 19). Indeed, behavioral one of the 13 most-affected families (Fig. 4A) were benthic observations of some moribund fish (Movie S3) exhibited signs feeders, potentially consuming carcasses or their remains found compatible with infection of the central nervous system. S. iniae on the seabed. Infections via feeding and fecal–oral routes (20) appeared to be the direct cause of death of most fish that died appeared to be the likely reason for the prolonged epizootic, during the epizootic. lasting several weeks after the end of the warming event. Overall, Measurements of dissolved oxygen at the coastal and deep the decline in the populations of the eight hard-hit taxa (Scaridae monitoring stations during the epizootic indicated surface con- to Scorpaenidae excluding Pomacentridae in Fig. 4A) was 4.8%, centrations around 208 μM, well within the range of 189 to indicating that the decline of the epizootic 2 mo after it began 211 μM typical for that season (SI Appendix, Fig. S2). Similarly, was unlikely an outcome of a sharp decline in population size. no , a known cause of (13, 14), Note that our removal of carcasses from the sea might have coincided with the event as the of phytoplankton in the lowered the spread of the bacterial infection. water and the benthic on the reef were well within their Why did the motile fish not escape the warming waters (3, 10, normal ranges (SI Appendix, Fig. S3). Nor was air temperature 11)? Unlike sessile or sedentary animals (4, 5, 7–9), fish could unusual for that period (SI Appendix, Fig. S4). have sought a nearby refuge in deep waters. For example, in the The onset of the two warming events coincided with a de- coral reef off the IUI, fish residing at 10 m depth could find clining barometric pressure, weakening winds, a moderate in- ∼3 °C cooler waters at 50 m depth, a short distance (∼250 m) crease in relative humidity, and, consequently, a remarkable away. Yet they remained in the warming zone. A likely reason decrease in latent (evaporative) heat loss and corresponding for this behavior is that most of the fish that died during the increase of the net heat flux to the sea surface (Fig. 5). Latent event (Fig. 4A), were species that maintain limited home ranges heat flux is the major cooling mechanism of the sea surface in the (34, 35), with some being strictly territorial (36). Gulf of Aqaba (31, 32). Satellite records of SST indicated that An extensive study on the upper temperature threshold of the warming event happened simultaneously along most of the tropical fishes (37) concluded that global warming should not yet Gulf of Aqaba (∼180 km), showing the occurrence of the steep affect coral reef fishes directly because the upper thermal tol- Ronset over its entire northern section (Fig. 6). The decline in erance of many species greatly exceeds the range to which they wind speed appeared to be the outcome of a thermal low over are currently exposed. Challenging this conclusion, our study the Sahara Desert, as evident from the large-scale mapping of shows that the critical parameter at stake is not necessarily the geopotential height (SI Appendix, Fig. S5) and the corresponding peak temperature, but the rate of warming. The maximum decline of in situ barometric pressure during each of the two temperature during the event in Eilat (28.6 °C) was not excep- occurrences of extreme Ronset (Fig. 5D). These observations tional as higher temperatures with no noticeable mortality of fish

Genin et al. PNAS Latest Articles | 3of8 Downloaded by guest on September 29, 2021 occurred in August 2001 in Kuwait Bay (12, 13), allegedly due to an extreme MHW. However, a later compilation of monthly SST in Kuwait Bay (41) indicated that water temperature in August 2001 was not unusual as warmer summers with no reports on local fish mortalities occurred in preceding years (figure 5 in ref. 41). Our analysis of satellite-derived daily SST changes in Kuwait Bay during that period indicated the occurrence of a steep Ronset several days prior to the start of the fish die-off (SI Appendix, Fig. S7A). Similar to the warming event in Eilat, the high Ronset in Kuwait Bay coincided with weak winds and calm , and the cause of death was infection by Streptococcus agalactiae (13). The second reexamined event was the mass mortality of fish observed during the 2011 MHW along the coast of Western Australia (6). There, as well, our remote-sensing analysis showed that the fish die-off started a few days after a sharp Ronset (SI Appendix, Fig. S7B). The occurrence of a steep onset and its relationship to the mortality event was briefly stated, describing it as a warming spike with a 2 to 3 °C rise in water temperature over a few days (6, 42). As in Eilat and Kuwait Bay, the rise in temperature coincided with weak winds and calm seas (6). No identification of pathogens was possible because the carcasses were collected after being washed up on beaches (6) and therefore already decomposing. Our assessment of these two warming events suggest that an extreme Ronset could have been an overlooked trigger of past mortalities of wild fish elsewhere prior to the 2017 event in Eilat. A selective loss of predators and benthic feeders (Fig. 4B)is expected to change the diversity and functioning of fish

Fig. 3. Spatiotemporal characteristics of the fish epizootic in summer 2017 in Eilat. (A) Total number of fish carcasses recorded per week along the coast of Eilat. Dates on the horizontal axis indicate the first day of the corre- sponding week. (B) Total number of fish carcasses recorded at 21 sites along the entire coast of Eilat during the epizootic. Symbols on the map indicate the total number of carcasses found at each site as indicated in the legends shown in the upper left corner. Sites 1 to 7 had sandy bottom with scattered reef boulders; sites 12 to 18 are continuous coral reefs; all other sites are a mixture of sandy bottom and patch reefs. The red star indicates the location of the IUI.

occurred in over half of the 32 summers on record (SI Appendix, Fig. S6). A rapid change in temperature is a well-documented stressor of fish, suppressing immune response and increasing suscepti- bility to pathogens (19, 38, 39). An experimental study on Fig. 4. Taxonomic composition of the carcasses and live fish in the coral reef sockeye during its prespawning migration in the Fraser of Eilat. (A) Frequency of occurrence of different fish taxa (genus or family) among the carcasses (black bars; n = 392 identified fish), before the die-off River in Canada (40) coincidentally simulated a similar warming event (blue bars; summer 2016; n = 2,351) and in fall 2017 after the epi- rate to the one we measured in Eilat. There, the fish were im- zooticended(redbars;n = 2,128). (B) Chesson α index of selectivity (28) mersed in water that was gradually warmed at a rate of 3 °C in comparing the relative occurrence among the carcasses to that in the liv- 2 d (to 18 °C) and acoustically monitored after their release back ing community prior to the die-off event, calculated for five different to the river (15 °C). That warming treatment increased the functional groups, based on their feeding mode. The expected value under mortality of the exposed fish by ∼50%, as compared with the random mortality is α = 0.2 (dashed line). Pisc, piscivores, consisting mostly mortality of control individuals immersed in ambient tempera- (76%) of Serranidae (groupers); Graze, benthic herbivores, consisting ∼ ture. The reported reason for the lower survival in the warm- mostly (90%) of Scaridae (parrotfish) and some ( 5% each) Siganidae treatment fish was a rise in parasite infection (40). (rabbitfish) and Acanthuridae (surgeonfish); Invert, benthic invertebrate feeders, consisting mostly (24%) of Balistidae (triggerfish), Chaetodonti- Our reexamination of two documented events of mass mor- dae (butterflyfish, 17%), and Plotosiidae (eel-tail catfish, 17%); Omni, tality of wild fish that had been attributed to extreme tempera- omnivores, consisting mostly (15%) of Ostraciidae (boxfish, 15%); Plank, ture anomalies (6, 12, 13) indicated that also in those cases an planktivores, consisting mostly (80%) of Pomacentridae (damselfish) and extreme Ronset might have been the trigger. The first event the scalefin anthias, P. squamipinnis.

4of8 | www.pnas.org/cgi/doi/10.1073/pnas.2009748117 Genin et al. Downloaded by guest on September 29, 2021 communities in affected reefs, especially if recurring. Will the frequency of extreme Ronsets increase alongside the predicted increase in frequency and magnitude of MHWs in the 21st century (43, 44)? To the best of our knowledge, the relationships between occurrences of extreme Ronsets and MHWs or thermal lows have not yet been explored. However, rationally, if extreme Ronsets occur at a certain percent of such warming events, re- gardless of how small that percent is (e.g., Fig. 1D), the outcome of more frequent warming events may be a proportional increase in the frequency of extreme Ronset. Calamities inflicted on coral reefs by the warming oceans may extend far beyond bleaching and its consequences (45). Materials and Methods Environmental Conditions: The National Monitoring Program. As detailed be- low, much of the background information presented here uses data recorded by Israel’s National Monitoring Program (NMP) in the Gulf of Eilat (46). NMP started to operate in 2003 and is active to date. Some activities were added in later years. The access to the NMP database is publicly open at https://iui- eilat.huji.ac.il/Research/NMPMeteoData.aspx. Following are succinct de- scriptions of the NMP methods related to the parameters used in this study. Detailed descriptions are found at https://iui-eilat.huji.ac.il/Research/ NMPMethodsEng.aspx. Continuous measurements. Water temperatures, air temperature, wind speed and direction, barometric pressure, solar radiation, and relative humidity (used in Figs. 1 A and B and 5) were measured at the pier of the Interuni- versity Institute for Marine Sciences of Eilat (“IUI Pier”; 29.5033° N; 34.9178° E), located 30 m offshore, over the upper reef slope, where the bottom depth is ∼4 m. These measurements were recorded at 10-min intervals and

later used to calculate hourly and daily means. A real-time display of the ENVIRONMENTAL SCIENCES data is available at www.meteo-tech.co.il/eilat-yam/eilat_en.asp. Measure- ments started in September 2006 and continue to date. Water temperature was measured with a thermistor attached to a piling at ∼2 m below the surface (at low tide). All other parameters were measured at 6 to 10 m above sea surface. Daily measurements of SST and Chlorophyll a. These daily measurements were made in the morning (0800 to 0900) since 1988, at a fixed point, ∼10 m seaward of the reef flat on the pier of the Coral World Underwater Ob- servatory, located at the Coral Reef Nature Reserve, ∼350 m northeast of the ECOLOGY IUI pier. Being measured once a day in the morning, these measurements missed the coolest (predawn) and warmest (late afternoon) times of the day. Therefore, these measurements (used in Fig. 1 C and D and SI Appendix, Fig. S6) differed from the aforementioned daily means used in Fig. 1B that were calculated based on the continuous measurements. Surface concentrations of extracted chlorophyll a were measured daily as described in ref. 47. Briefly, two samples (330 mL each) of surface water were collected concurrently with the SST measurements at the same lo- cation, prefiltered using a 100-μm plankton net (to remove zooplankton), and transferred to the laboratory where phytoplankton was retained by filtering the water through GF/F filters. The chlorophyll was extracted in buffered 90% acetone solution for 24 h under dark and cold (4 °C) con- ditions, followed by measurements using a calibrated fluorometer (TD700; Turner Design). Measurements of dissolved oxygen. Vertical profiles of dissolved oxygen (and other parameters) from the surface to 700 m depth have been carried out as part of NMP at the permanent “Station A” (29.5° N; 34.95° E) once a month since 2003. Station A is located in the open waters, ∼3 km southeast of the Nature Reserve Coral Reef of Eilat. In addition, we used NMP’s monthly measurements of dissolved oxygen concentration at 1 m below surface at another station (“OS”), located ∼2 km offshore, directly in front of the coral

dashed lines (gray) in all panels indicate the first and second Ronsets (1 and 14 July, respectively). Note that the extreme Ronset during each of the two Fig. 5. Time series of key environmental conditions related to the onset of successive warming events coincided with a declining barometric pressure, the warming event in summer 2017 in Eilat. Shown are (A) water temper- subsiding winds, reduced latent cooling, and intensified negative net heat ature, (B) wind speed, (C) barometric pressure, (D) air temperature, (E)rel- flux (i.e., sea surface warming), as well as a marginal increase in relative ative humidity, and (F) net and latent (evaporative) heat fluxes. In all panels humidity (E). A coincidence with increasing air temperature was more obvi- except F, colored lines are hourly means, and black lines are daily means. ous during the second event (D). The declines in barometric pressure and Lines in F indicate daily means of net heat flux (red) and latent heat flux wind speed at the onset of the two warming events coincided with two (blue), with positive values indicating upward fluxes (sea surface cooling). separate occurrences of a thermal low over the Sahara Desert (SI Appendix, Note the reversed direction of the axis of the net flux. The two vertical Fig. S5).

Genin et al. PNAS Latest Articles | 5of8 Downloaded by guest on September 29, 2021 surveys have continued to date, long after the fish farms were removed from sea in 2008. Unfortunately, the routine transects were interrupted during the fish die-off period (July to September 2017) as the person in charge of that activity joined the extensive, public search for carcasses, re- suming the routine surveys only in late 2017, after the die-off event was over. Therefore, annual totals presented in SI Appendix, Fig. S1 do not include 2017.

Calculations of Heat Fluxes. The latent and sensible heat fluxes were calcu- lated with the Coupled Ocean–Atmosphere Response Experiment (COARE) V. 3 algorithm (53), covering low wind conditions. The long-wave (infrared) cooling was calculated based on the algorithms of Bignami et al. (54). Cal- culations were based on the aforementioned measurements of solar radia- tion, wind speed, relative humidity, water and air temperatures, and barometric pressure at the IUI pier.

Satellite Remote Sensing Observations. The Group for High Resolution (GHRSST) (version 1.0) product was acquired from the Fig. 6. Remote sensing SST depicting daily changes over the Gulf of Aqaba NASA Earth Observing System Data and Information System (EOSDIS) Physical

from 25 June through 10 July 2017, showing the extreme Ronset of the first Oceanography Distributed Active Archive Center (PO.DAAC) at the Jet Pro- warming event (1 to 4 July). The satellite-derived SST values agreed re- pulsion Laboratory (Pasadena, CA) (https://podaac.jpl.nasa.gov/). The data- markably well with the daily means of direct measurements of water tem- sets have been produced on an operational basis at the Naval Oceanographic perature at the IUI pier (SI Appendix, Fig. S8A). The small red star at the top Office (NAVOCEANO) on a global 0.1° grid since April 2008. The K10 L4 SST of the Upper Left panel indicates the location of the IUI. Note that the product consists of merged observations from the Advanced Very High- maximum temperature shown here for 4 July (∼27.5 °C) is lower than the Resolution Radiometer (AVHRR), the Advanced Microwave Scanning Radi- maximum seen in Fig. 1A (28.6 °C) because the latter was obtained from ometer for EOS (AMSR-E), and the Geostationary Operational Environmental measurements taken every 10 min, thereby recording the true maximum of Satellite (GOES) Imager. The daily, level 4 SST data (tuned to represent SST at the day, usually occurring in late afternoon. The spatial characteristics of the 1-m depth) were processed over the Gulf of Aqaba and analyzed to depict the onset of the second warming event (14 to 16 July) were similar (SI Appendix, spatiotemporal distribution of SST. The final choice of the GHRSST K10 L4 SST, Fig. S8A). among the few remote-sensing products available, followed our finding of an excellent agreement between the satellite-derived SST product (average over the pixel nearest to IUI) and the in situ measurements of water temperature at reef. The dominant southward winds in the Gulf generate Ekman transport 2mdepthattheIUIpier(SI Appendix,Fig.S8). A 3-y-long cross-correlation that drives surface waters westward, from the offshore region toward the analysis between the two daily time series indicated an extremely high, highly reef (48). Therefore, the concentrations of dissolved commodities in the significant correlation coefficient (Pearson r = 0.98, P < 0.0001; n = 1,080) (SI open waters, around Stations A and OS, were similar to those near the Appendix,Fig.S8B). reef (49). Quantification of benthic algae. Our aim in analyzing the aforementioned – chlorophyll concentrations and the abundance of benthic algae was to assess Recording Carcasses Citizen Science. Following the realization in early July the possibility that the fish die-off was due to a harmful algal bloom (50, 2017 that the abnormal occurrence of dying fish on the coral reef might 51). Since 2008, NMP has monitored the “potential” growth rate of mac- indicate a beginning of widespread mortality, we issued a call to the public roalgae in the coral reef of Eilat on caged polyvinyl chloride (PVC) plates through media and local dive centers. Divers and swimmers were asked to (10 × 10 cm in size) at three sites, three replicates per site: the reef off IUI search for carcasses, record the date, time, location, and depth of finding, (7 to 10 m depth), and the shallow (5 m) and deep (20 m) reefs at the Coral remove the carcasses from the sea, and, if possible, take a photograph of Reef Nature Reserve. The meshed cages (52) (1-cm mesh size) effectively the carcass to assist with taxonomic identification and size estimates. The exclude grazers, including herbivorous fish and sea urchins. The concen- recording of carcasses by nonexpert citizens sometimes necessitated the tration of chlorophyll a per area was used as proxy for the algal biomass. pooling of different taxa in groups (genus, family), each consisting of New plates were deployed once a month and retrieved 2 mo afterward. several species that could not be reliably differentiated. Therefore, our Retrieved plates were transferred to the laboratory where the algae report of the total number of species that died during the event under- grown on each plate was scraped off, excess water was removed by fil- estimated the actual number. The objective of removing the dead fish tering the material through GF/A filters, then the scraped algae was im- from the sea was twofold: to help reduce the spread of the epizootic through the consumption of infected fish and to prevent repetitive counts mersed in acetone–methanol solution (1:1 ratio) for 24 h of cold (4 °C) dark of the same carcasses. The collected carcasses were taken to the local extraction, followed with spectrophotometric reading of the extracted headquarters of the Nature and Parks Authority for incineration. Mori- chlorophyll a. bund or freshly dead fish (those with red gills) were rushed to the National Census of coral reef fishes. Annual surveys of coral reef fishes have been carried Center of Mariculture in Eilat for necropsy and further analysis. The in- out as part of NMP since 2015. Fish were counted by divers along 25 to formation received on the carcasses was compiled by one of the authors (L. 30 cubic-shaped transects, with a 1 × 7-m rectangular base, extending from L.). As the number of swimmers and divers was relatively higher during the the seabed (5 to 8 m depth) through the , up to the sea sur- weekends, the search effort was nonuniform during the week. Therefore, face. Counted fish were identified to the species or family levels. The data the temporal dynamics of the fish mortality in Fig. 3A is presented using were sorted based on the fish diets to one of the following five functional weekly intervals. groups: 1) piscivores (mostly groupers); 2) grazers (mostly parrotfish, sur- geonfish, and rabbitfish); 3) feeders on benthic invertebrates (mostly trig- gerfish, butterflyfish, and marine catfish); 4) omnivores (mostly boxfish); and Necropsy. Primary bacterial cultures were isolated in a laminar flow hood 5) planktivores (damselfish and the serranid Pseudanthias squamipinnis). from spleen, liver, head kidney, blood, and brain of moribund and freshly Here, we used the results of the census carried out in summer 2016, a year dead fish. Inoculations were made on tryptic soy agar (TSA) (Difco) prepared before the fish die-off, and the one carried out in September 2017, after the with 25% sterile . Incubation was at 24 ± 1 °C. Following subculture, end of the epizootic. DNA was extracted from a pure bacterial colony. Briefly, DNA was extracted Long-term monitoring of fish carcasses. Occasional findings of floating fish from a needle-touched bacterial colony (in three replicates), using grinding carcasses in 1990 to 2003, when fish farms operated near the northern end of buffer (100 mM Tris·HCl, pH 9, 100 mM ethylenediaminetetraacetic acid the Gulf of Eilat (∼1 km east of site no. 1 in Fig. 3B), prompted NMP in 2004 [EDTA], and 1% sodium dodecyl sulfate [SDS]). The homogenate was incu- to start daily transects to record fish carcasses on the coral reef. The transect bated for 30 min at 70 °C. Forty-two microliters of 8 M potassium acetate was visually surveyed every morning by a snorkeler, swimming at the surface were then added, and the mixture was placed on ice for 30 min, after which along a ∼1.5-km transect over the upper reef slope (5 to 15 m bottom depth) it was centrifuged at 12,000 × g for 15 min at 4 °C. To eliminate pellet traces, of the Coral Reef Nature Reserve (between sites 14 and 17 in Fig. 3B). The the supernatant was transferred to a fresh tube and centrifuged again for

6of8 | www.pnas.org/cgi/doi/10.1073/pnas.2009748117 Genin et al. Downloaded by guest on September 29, 2021 5 min. DNA was precipitated with 1 volume of isopropanol and left for ACKNOWLEDGMENTS. We thank the Israel NMP in the Gulf of Eilat for 15 min at room temperature. Pelleted DNA was washed twice in 70% eth- providing the invaluable environmental data. We thank members of the anol, and the air-dried pellet was dissolved in 50 μL of double-distilled H O. NMP, IUI, and Nature and Park Authority in Eilat; and Orie Legum and the 2 many divers, snorkelers, and residents of Eilat for their contribution to the DNA quantity and quality (260:280 ratios) were measured in a Nanodrop campaign of recording and collecting carcasses. We thank local dive centers, One (Thermo Scientific). PCR analysis of the 16S gene using 27f (5′-AGAGTT editors of local and national newspapers, and social media administrators TGATCCTGGCTCAG-3′) and 1492R (5′ TACGGCTACCTTGTTACGACTT-3′) pri- for their contribution to the call for this citizen-science campaign. We thank mers was performed. PCR products were purified using QIAquick PCR Puri- Roberto Ehrlich for his help with the necropsy and its analysis. We thank the “ ” fication Kit 250 (QIAGEN, Hilden, Germany). DNA quantity and quality Israel Meteorological Service for wind data from their station Elat and the GHRSST from the NASA EOSDIS PO.DAAC at the Jet Propulsion Laboratory (260:280 ratios) were estimated for the second time in a microplate spec- (Pasadena, CA) for the satellite-derived SST products. Parts of the study were trophotometer (PowerWave XS; BioTek). Purified PCR products from tem- supported by grants from the Israel Science Foundation (1211/14) and Israel plate DNA were sequenced at Hy Laboratories Ltd. (Hylabs, Rehovot, Israel). Ministry of Science and Technology (3-16729) (to A.G.). The NMP is funded by the Israel Ministry of Environmental Protection. We thank Sophie Dove, Ove Hoegh-Guldberg, Margarita Zarubin, and Daniela Genin for insightful Statistical Analysis. Pearson correlation and regression analyses were carried discussions on the ecology of the warming event, and L. G. C. Genevier and out using SYSTAT (V. 13). G. Krokos for helping with the analysis of remote sensing and atmospheric circulation. We thank Prof. Steve Brenner (Bar Ilan University) for the calcu- lations and interpretation of the heat flux dynamics. Comments and sugges- Data Availability. All study data are included in the article and SI Appendix. tions made by two anonymous reviewers greatly improved the manuscript.

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