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Brief Report
Revised

Rapid coral mortality following unusually calm and hot conditions on Iriomote, Japan

[version 2; peer review: 2 approved]
Previously titled: Rapid coral mortality following doldrums-like conditions on Iriomote, Japan
PUBLISHED 12 Mar 2018
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OPEN PEER REVIEW
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This article is included in the Ecology and Global Change gateway.

Abstract

Coral bleaching can be induced by many different stressors, however, the most common cause of mass bleaching in the field is higher than average sea surface temperatures (SST). Here, we describe an unusual bleaching event that followed very calm sea conditions combined with higher than average SST. Patterns of mortality differed from typical bleaching in four ways: 1) mortality was very rapid; 2) a different suite of species were most affected; 3) tissue mortality in Acropora spp. was often restricted to the center of the colony; 4) the event occurred early in summer. The two weeks prior to the event included 8 days where the average wind speed was less than 3 ms-1. In addition, SSTs in the weeks preceding and during the event were 1.0-1.5°C higher than the mean for the last 30 years. We hypothesize that this unusual bleaching event was caused by anoxia resulting from a lack of water movement induced by low wind speeds combined with high SST.

Keywords

climate change, coral bleaching, coral reefs, disturbance

Revised Amendments from Version 1

In response to the comments of Robert van Woesik we have removed all reference to the doldrums, the table has been rearranged so the species are ranked from most to least impacted, we have specified the aspect of the site and addressed all the grammatical and typological errors identified. In response to the comments of Misha Matz we now included sea surface temperatures and wind speeds for the year preceding the bleaching event. These data suggest it was both hotter and calmer in the week prior to the bleaching than at the same time of year in 2015. However, as Misha points out, it is not possible to prove that this bleaching was a result of hypoxia driven by calm or hot conditions. To do this we would need to have placed oxygen electrodes in the centre of colonies during the event. We have, however, added comments to the effect that wind speeds less than 3 m/s are generally regarded as the cut-off below which calm weather bleaching can occur and cited the NOAA website in support of this statement. Absolute values of wind speed are the correct metric to present – this is what affects wave and water movement. Unfortunately, we can find no literature in support of the statement that “Tissue mortality beginning in the center of the colony typically indicates anoxia..”. Therefore, we have reworded the sentence to make it clear that this statement is based on personal observation alone. We have kept the BMI index in Table 1 because this is now used to rank the taxa as requested by Robert van Woesik.

To read any peer review reports and author responses for this article, follow the "read" links in the Open Peer Review table.

Introduction

Coral bleaching is a generalized response that can be induced by many different stressors13. Whilst the most common cause of large scale bleaching on coral reefs is unusually high sea surface temperatures (SSTs)4,5, prolonged periods of calm weather have also been associated with mass bleaching events in the Caribbean6,7 and the Indo-Pacific810. Experimental work has also confirmed that low water flow can exacerbate thermal bleaching11,12.

The ecology of thermal coral bleaching in response to high SSTs is reasonably well documented. For example, colonies affected by high temperatures typically take between two to six weeks to bleach and bleached tissue can take another two to twenty weeks to die13. In addition, species vary in their susceptibility to thermal bleaching14,15, resulting in a predicable hierarchy of response16,17. Temporal patterns are also apparent with most high temperature induced mass bleaching events generally occurring towards the end of the summer months18,19. Any change in this predictable bleaching ecology suggests an alternative cause (i.e., not thermal stress) for a given bleaching event.

Here, we describe an atypical bleaching event that we hypothesize was caused by an interaction of temperature with very calm sea conditions caused by an extended period of low winds. We identify a number of characteristic features of this calm weather bleaching that allow it to be distinguished from thermal bleaching in the field. Establishing the cause of specific bleaching events is vital in order to correctly attribute damage caused by climate change and other potential stressors.

Methods

The study site was on the reef crest (1 m depth) at Nata Reef, Iriomote, Japan (24.4282°N, 123.7955°E). Initial observations at the site were made between 26 and 29 May, 2016 at which point in time no bleached corals were noted. Surveys to quantify bleaching and mortality were conducted on 12 June, 2016. Twenty replicate 1m2 quadrats were placed haphazardly on the reef crest, and the condition and species identity of all hard coral colonies with a maximum diameter greater than 5cm were recorded. Species were identified in the field following20 and the names updated to the currently accepted names following21 Colonies were placed in one of six bleaching categories following22: (1) unbleached, (2) the entire colony pale, (3) 1–50% of the colony white, (4) 51–99% of the colony white, (5) 100% of colony white or fluorescent, or (6) recently dead. The data from the quadrats was pooled as the data was collected. The bleaching mortality index was calculated following16. Data on environmental conditions leading up to the bleaching episode and for a similar time frame in 2015 were obtained from the Japan Meteorological Agency, which allows for these data to be used as long as due credit is given.

Results

Bleaching and mortality was rapid. No colonies were bleached at the time of the first surveys (26 May, 2016) yet two weeks later (12 June, 2016), 5% of colonies were dead and a further 31% were bleached (Table 1).

Table 1. Bleaching categories of hard corals at Nata Reef on 12 June 2016.

BMI = Bleaching Mortality Index.

taxaunbleachedmoderateseveredeadBMIn
Acropora selago0001001001
Montipora aequituberculata0001001003
Montipora efflorescens02727457311
Goniastrea pectinata050500502
Milleporidae1733500446
Dipsastraea rotumana010000331
Montipora turgescens010000331
Platygyra ryukyuensis2550250334
Platygyra verweyi670033333
Dipsastrea pallida30502003010
Montipora crassituberculata46321842628
Montipora digitata710290197
Acropora nasuta505000172
Pocillopora damicornis6722110159
Pavona venosa574300147
Porites annae604000135
Acropora hyacinthus712900107
Platygyra pini75250084
Porites cylindrica772300813
Acropora digitifera811900632
Galaxea fascicularis821800611
Favites halicora86140057
Goniastrea retiformis861400514
Acropora aspera10000001
Acropora gemmifera10000001
Astrea annuligera10000001
Cyphastrea serailia10000003
Favites abdita10000003
Favites magnistellata10000002
Montipora monasteriata10000004
Pavona decussata10000002
Porites lichen10000003
Porites lutea10000001
Porites rus10000006
Psammocora contigua10000001
total64238521618

Mortality was highest in Montipora aequituberculata and M. efflorescens (Figure 1A), and in an additional three species of the family Merulinidae, that were also badly affected (Table 1). Bleaching and tissue mortality were generally restricted to the center of colonies in the locally abundant species Acropora digitifera and A. hyacinthus (Figure 1B, C, D).

284344b7-d009-486f-9b8f-4f45857d2ac7_figure1.gif

Figure 1.

(a) Dead and dying Montipora aequituberculata colonies (b) Acropora hyacinthus colony with bleached and dying tissue in the middle of the colony (c) a second A. hyacinthus colony (d) close up of the colony in (c). Images were captured using a Canon S100 digital camera in waterproof housing.

The bleaching event occurred early in June, the first month of the northern summer, following a period of low wind and higher than average sea surface temperature (SST). Eight days in the previous two weeks had average wind speeds of under 3 ms-1 (Table 2). Winds were also mostly from the south, which is offshore at the study site and therefore likely to further reduce wave size and water motion (Table 2). Mean daily SSTs in the month preceding the second survey were 0.0–1.5°C higher than the mean for the previous 30 years (Table 3). Wind speeds were higher and SST lower during the same time interval in 2015 (Table 2 & Table 3).

Table 2. Mean daily wind speeds in the 12 days prior to the first observations of bleaching on 12 June 2016 and for the same dates in 2015.

Data from Japan Meteorological Agency.

Date2015 wind
speed
(m/s)
2015 wind
direction
2016 wind
speed
(m/s)
2016 wind
direction
30 May2.2SSE2.1ENE
31 May3.1ENE1.8SE
1 June2.6NE3.4W
2 June4.8SSW3NE
3 June4.6SSW2.1SW
4 June2.3S2.1ENE
5 June5.5SSW3.2NE
6 June3.8S2.5NE
7 June4.2SSW1.6SE
8 June3.3SW1.9ESE
9 June3SSW2ENE
10 June4.2SSW3SSW
11 June5.3S6.4SSW
12 June4S8.2SSW

Table 3. Sea surface temperature anomalies in the weeks preceding the bleaching event on Nata Reef and a similar time interval in 2015.

Values are the degrees in centigrade above the 30 year average for this site in each time interval. Data from the Japan Meteorological Agency.

10 day period
ending
2015 SST
anomaly °C
2016 SST
anomaly °C
10 April00
20 April-0.51
30 April01.5
10 May0.51.5
20 May0.51
30 May0.51
10 June0.51

Discussion

This bleaching event was different to typical thermal bleaching in a number of important ways. In particular, rapid tissue mortality, an atypical hierarchy of susceptibility, and the occurrence of the event in early summer, all distinguish this event from typical thermal bleaching. We hypothesize that unusually high SST combined with a lack of water flow due to low winds speeds resulted in anoxic stress to these colonies. This hypothesis is supported by very low wind speeds (Table 2) combined with higher than average mean daily SST (Table 3) in the weeks prior to the event.

In contrast to the typical thermal response, bleaching and mortality were very rapid, with a high proportion of colonies bleached and some dying within the two week period between the surveys (Table 1). Bleaching and, in particular, mortality typically take between 4–6 weeks to present in corals following thermal stress13. In addition, the hierarchy of susceptibility was very different to that following thermal bleaching. Here, the worst affected species included two Montipora spp. and a number of merulinids (Table 1), when typically Acropora spp. and Pocillopora spp. are the most severely affected following thermal bleaching5,15,22.

The pattern of tissue bleaching and mortality was also unusual. In Acropora colonies the typical pattern following thermal stress is for the whole colony to bleach13. In contrast, mortality was restricted to the center of most Acropora colonies in this event (Figure 1a, b, c). Tissue mortality beginning in the center of the colony is suggestive of anoxia, which often occurs in aquaria with inadequate flow or oxygenation (pers obs). This pattern of mortality is also superficially similar to feeding scars caused by Acanthaster planci or Drupella spp.23 and a naïve observer might well have attributed this mortality to either of these corallivores24. A thorough search of the site, including underneath these and adjacent colonies, indicated that neither of these corallivores were present.

The timing of the bleaching event in early summer is also unusual. Thermal bleaching typically occurs much later in the summer. For example, recurrent seasonal bleaching on Magnetic Island, Australia, occurs in the last month of the austral summer i.e., February18. Similarly, the 1998 mass bleaching event in Japan was first noticed in the latter part of the summer i.e., late July25. In contrast, this calm weather event occurred early in June, the first month of the northern summer.

Doldrums-like conditions (defined by NOAA as days with average wind speeds of less than 3 ms-1) have previously been linked to mass bleaching events69. However, the capacity of calm weather to cause more localized damage outside of the typical thermal bleaching window in late summer has not previously been recognized. In addition, the potential link to anoxia, while tested in the laboratory26, has not been made in the field. This observation is especially important in the context of the continuing increase in the scale and frequency of mass bleaching events27 because it would generally be assumed that this small-scale phenomenon might presage a larger mass bleaching event. Determining the cause of specific bleaching events is vital in order to accurately distinguish the effects of climate change versus other causes of degradation on coral reefs.

Data availability

The pooled raw bleaching data is provided in Table 1.

Source data for Table 2 are available from the Japan Meteorological Agency, at:

http://www.data.jma.go.jp/obd/stats/etrn/view/daily_s1.php?prec_no=91&block_no=47917&year=2015&month=05&day=30&view=a3

http://www.data.jma.go.jp/obd/stats/etrn/view/daily_s1.php?prec_no=91&block_no=47917&year=2015&month=06&day=30&view=a3

http://www.data.jma.go.jp/obd/stats/etrn/view/daily_s1.php?prec_no=91&block_no=47917&year=2016&month=05&day=30&view=a3

http://www.data.jma.go.jp/obd/stats/etrn/view/daily_s1.php?prec_no=91&block_no=47917&year=2016&month=06&day=30&view=a3

Source data to generate the values in Table 3 are available from the Japan Meteorological Agency, at: http://bit.ly/2y8qlBw.

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VERSION 2 PUBLISHED 22 Sep 2017
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Baird AH, Keith SA, Woolsey E et al. Rapid coral mortality following unusually calm and hot conditions on Iriomote, Japan [version 2; peer review: 2 approved]. F1000Research 2018, 6:1728 (https://doi.org/10.12688/f1000research.12660.2)
NOTE: If applicable, it is important to ensure the information in square brackets after the title is included in all citations of this article.
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Key to Reviewer Statuses VIEW
ApprovedThe paper is scientifically sound in its current form and only minor, if any, improvements are suggested
Approved with reservations A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit.
Not approvedFundamental flaws in the paper seriously undermine the findings and conclusions
Version 2
VERSION 2
PUBLISHED 12 Mar 2018
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Reviewer Report 05 Apr 2018
Mikhail V. Matz, Department of Integrative Biology, University of Texas at Austin, Austin, TX, USA 
Approved
VIEWS 11
I’m generally satisfied with the authors' response, although I really hoped to see more previous-years data than just one year before the event - in my opinion the case for the “doldrums effect” becomes progressively more convincing the better you can ... Continue reading
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Matz MV. Reviewer Report For: Rapid coral mortality following unusually calm and hot conditions on Iriomote, Japan [version 2; peer review: 2 approved]. F1000Research 2018, 6:1728 (https://doi.org/10.5256/f1000research.15488.r31834)
NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article.
Version 1
VERSION 1
PUBLISHED 22 Sep 2017
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Reviewer Report 04 Dec 2017
Robert van Woesik, Department of Biological Sciences, Florida Institute of Technology, Melbourne, FL, USA 
Approved
VIEWS 24
The manuscript by Baird and colleagues is a useful contribution to the literature. There are however a few minor edits that are necessary to make this short contribution publishable.

Firstly, the title is inaccurate, or at least ... Continue reading
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van Woesik R. Reviewer Report For: Rapid coral mortality following unusually calm and hot conditions on Iriomote, Japan [version 2; peer review: 2 approved]. F1000Research 2018, 6:1728 (https://doi.org/10.5256/f1000research.13707.r26305)
NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article.
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30
Cite
Reviewer Report 05 Oct 2017
Mikhail V. Matz, Department of Integrative Biology, University of Texas at Austin, Austin, TX, USA 
Approved with Reservations
VIEWS 30
This is a compact report of an unusual bleaching episode, presenting an interesting hypothesis that it could have been caused by anoxia during atypical doldrums conditions. Both are valuable for improving our understanding of factors affecting coral survival in times ... Continue reading
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HOW TO CITE THIS REPORT
Matz MV. Reviewer Report For: Rapid coral mortality following unusually calm and hot conditions on Iriomote, Japan [version 2; peer review: 2 approved]. F1000Research 2018, 6:1728 (https://doi.org/10.5256/f1000research.13707.r26307)
NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article.

Comments on this article Comments (0)

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VERSION 2 PUBLISHED 22 Sep 2017
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Alongside their report, reviewers assign a status to the article:
Approved - the paper is scientifically sound in its current form and only minor, if any, improvements are suggested
Approved with reservations - A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit.
Not approved - fundamental flaws in the paper seriously undermine the findings and conclusions
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