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Supplementary Information for

Title: Rapid onsets of warming events trigger mass mortality of coral reef fish

By: Amatzia Genin, Liraz Levy, Galit Sharon, Dionysios E. Raitsos, Arik Diamant

Corresponding author: Amatzia Genin Email: [email protected]

This PDF file includes:

Figures S1 to S8 Tables S1

Legends for Movies S1 to S3 SI References

Other supplementary materials for this manuscript include the following:

Movies S1 to S3

www.pnas.org/cgi/doi/10.1073/pnas.2009748117

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Fig. S1. Annual counts of fish carcasses in the coral reef of Eilat prior to 2017. Fish carcasses were recorded during 2004-2016 through daily visual surveys in a 1.5 km transect along the coral reef of Eilat. Values are indicated above the bars. The routine survey was interrupted during the 2017 die-off event, as the person in charge joined the extensive public search for carcasses. Note the general decline in carcass findings following the removal of the fish farms from the Gulf in 2008, with no findings occurring during the 5.5 years preceding the July 2017 event. A total of 19 fish carcasses were found in the 13 years of this survey (a long-term average of a carcass every ~8 months), compared with 57 carcasses (out of the total of 427) collected along the same section of the reef during the two months of the 2017 die off.

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Fig. S2. Oxygen dynamics in the northern Gulf of Aqaba. (A) Vertical profiles in the month of July in the two years preceding the event (2015, 2016), a few days after the first warming event (July 10th, 2017) and a year later (2018). (B) Monthly profiles of dissolved oxygen concentration in the water column in the northern Gulf of Aqaba during summer 2017, starting before the warming event (late June) through the end of the epizootic (September). (C) Monthly measurements of dissolved oxygen concentrations since 2003 in the surface waters at Station OS, ~2 km offshore of the coral reef of Eilat. No exceptional decline in oxygen concentrations is apparent during the 2017 warming events, as sometime occurs when a confined waterbody warms up (1, 2).

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Fig. S3. Phytoplankton and benthic algae in the coral reef of Eilat during the summers of 2008-2018.

(A) Sea-surface chlorophyll a at the coral reef of Eilat in June-September of 2008-2016 and 2018 (green lines) and 2017 (black line). (B) Monthly averages [±SD] of Chlorophyll a extracted from benthic algae growing on grazing-free (caged) plates at 5 and 20 m depth in the Coral Reef Nature Reserve and at 7-10 m depth at the reef off IUI during the summer (June-September) in the years 2008-2018. Neither phytoplankton nor benthic algae bloomed during summer 2017.

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Fig. S4: Air temperature at the coral reef of Eilat. Mean daily temperatures at the IUI pier from June

to September in 2007- 2016 and 2018 (brown lines) and in 2017 (black line). Red and green rectangles indicate the onsets of the first and second warming events, respectively.

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Fig. S5. Changes in the numerical barometric pressure (geopotential height) in early summer 2017.

The maps show the anomalies in the geopotential height (m, gridded at the 1000 hPa) over the region extending from Europe to the Indian Ocean during the warming event in summer 2017 in Eilat,

starting prior to the onset of the first event (A), during its onset (B), during two typical days between the first and second events (C, D), during the onset of the second event (E), and 2 days after it ended (F). Red arrow in A indicates the location of Eilat at the northern end of the Gulf of Aqaba (Red Sea).

Note the Thermal Low that developed over the Sahara desert during each onset. The daily maps were obtained from NOAA National Center for Environmental Prediction (NCEP), Department of Energy (https://psl.noaa.gov/data/composites/day/) (3). Thermal Lows are most intense during the summer over subtropical continental areas such as the Sahara desert, where they are typically associated with weak winds in their periphery (4). The NCEP/NCAR’s wind model (https://www.ucar.edu/) indicated that during the Thermal Lows shown in this figure the winds were substantially weaker over the entire Gulf of Aqaba, in agreement with our direct measurements in Eilat (Fig. 5).

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Fig. S6. Time series of SST at the coral reef of Eilat. Measurements were carried out daily, in the morning, over the reef slope in the Coral Reef Nature Reserve of Eilat since 1988. Red rectangle indicates 2017.

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Fig. S7. Time series of remotely-sensed SST during warming events with mass mortalities of wild fish in Kuwait and Western Australia. A - Kuwait Bay (29.43° N, 47.98° E) in July - August 2001; B- Dongara, Western Australia (29.28° S, 114.89° E) in February - March 2011. SST data sources were determined by their availability for the corresponding time period, with Group for High Resolution Sea Surface Temperature (GHRSST) SST products of OSTIA used for Kuwait Bay, and MUR, for Western Australia ( https://podaac.jpl.nasa.gov/; accessed: 2020-04-01). Horizontal black bars indicate the reported periods of the fish die off based on references 5 and 6, for A and B, respectively.

A B

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Fig. S8. Ground truth of the satellite-derived measurements of SST. (A) – Daily measurements of SST at the IUI Pier (blue line) and remote sensing values (black line) from 15 June to 20 July 2017, both showing the onsets of the first and second warming events (red and green rectangles, respectively).

The satellite data (GHRSST) were obtained from the closest pixel to the coral reef of Eilat Nature Reserve. (B) – Regression line (blue) between the satellite and pier measurements taken during the years 2016-2018 (r2 = 0.96, p<0.00001, N=1080).

B A

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Table S1: Cause of death in the necropsied fishes. Date of collection, species, weight and total length of the fish and an indication whether or not Streptococcus iniae was molecularly identified as the cause of depth (+ or -, respectively). The P. miles lacking S. iniae was heavily infected by Vibrio sp.

Additional 7 necropsied fish yielded inconclusive results due to post-mortem carcass decomposition.

Streptococcus iniae Total

Length (mm) Weight

(g) Fish species

Date

+ 400

1443 V. louti

9.7.2017

+ 340

923 V. louti

10.7.2017

+ 207

151 Stephanolepis sp

+ 560

1666 V. louti

11.7.2017

+ Parupeneus cyclostomus

12.7.2017

+ P. cyclostomus

+ Scarus sp.

+ 210

218 Cheilodipterus sp.

13.7.2017

+ 245

287 Arothron hispdus

14.7.2017

+ 475

1121 V. louti

+ Ecsenius lineatus

24.7.2017

Plotosus japonicus + 25.7.2017

P. japonicus + 26.7.2017

- 320

Pterois miles 342 29.7.2017

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Movie S1 (separate file). Fish feeding on a moribund striped eel catfish. (Recorded by A. Diamant on July 25th, 2017.)

Movie S2 (separate file). Moribund parrotfish on the bottom at the coral reef. (Recorded by O. Legum on July 16th, 2017.)

Movie S3 (separate file). Moribund lionfish swirling in the water above the coral reef. (Recorded by A.

Diamant on July 15th, 2017.)

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SI References

1. R. F. Keeling, A. Körtzinger, N. Gruber, Ocean deoxygenation in a warming world. Ann. Rev. Mar.

Sci. 2, 199–229 (2010).

2. J.-P. A. Hobbs, C. A. McDonald, Increased seawater temperature and decreased dissolved oxygen triggers fish kill at the Cocos (Keeling) Islands, Indian Ocean. J. Fish Biol. 77, 1219–1229 (2010).

3. E. Kalnay et al., The NCEP/NCAR 40‐year re‐analysis project, Bull. Am. Meteorol. Soc., 77, 437–471 (1996).

4. R. H. Johnson, Thermal low. Encyclopedia of Atm. Sci., Acad. Press, 2269-2273 (2003).

5. P. M. Glibert, et al., A fish kill of massive proportion in Kuwait Bay, Arabian Gulf, 2001: the roles of bacterial disease, harmful algae, and eutrophication. Harmful Algae 1, 215–231 (2002).

6. A. F. Pearce, M. Feng, The rise and fall of the “marine heat wave” off Western Australia during the summer of 2010/2011. Journal of Marine Systems 111–112, 139–156 (2013).

References

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