# Coral responses to a repeat bleaching event in Mayotte in 2010

David Obura, Lionel Bigot, Francesca Benzoni

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## To cite this version:

David Obura, Lionel Bigot, Francesca Benzoni. Coral responses to a repeat bleaching event in Mayotte in 2010. PeerJ, 2018, 6, pp.e5305. 10.7717/peerj.5305. hal-01906866

HAL Id: hal-01906866

https://hal.univ-reunion.fr/hal-01906866

Submitted on 27 Oct 2018

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Distributed under a Creative Commons Attribution 4.0 International License
# Coral responses to a repeat bleaching event in Mayotte in 2010

David O. Obura<fnref n="1" />, Lionel Bigot<fnref n="2" /> and Francesca Benzoni<fnref n="3" />

## ABSTRACT

**Background.** High sea surface temperatures resulted in widespread coral bleaching and mortality in Mayotte Island (northern Mozambique channel, Indian Ocean: 12.1°S, 45.1°E) in April–June 2010.

**Methods.** Twenty three representative coral genera were sampled quantitatively for size class distributions during the peak of the bleaching event to measure its impact.

**Results.** Fifty two percent of coral area was impacted, comprising 19.3% pale, 10.7% bleached, 4.8% partially dead and 17.5% recently dead. *Acropora*, the dominant genus, was the second most susceptible to bleaching (22%, pale and bleached) and mortality (32%, partially dead and dead), only exceeded by *Pocillopora* (32% and 47%, respectively). The majority of genera showed intermediate responses, and the least response was shown by *Acanthastrea* and *Leptastrea* (6% pale and bleached). A linear increase in bleaching susceptibility was found from small colonies (<2.5 cm, 83% unaffected) to large ones (>80 cm, 33% unaffected), across all genera surveyed. Maximum mortality in 2010 was estimated at 32% of coral area or biomass, compared to half that (16%), by colony abundance.

**Discussion.** Mayotte reefs have displayed a high level of resilience to bleaching events in 1983, 1998 and the 2010 event reported here, and experienced a further bleaching event in 2016. However, prospects for continued resilience are uncertain as multiple threats are increasing: the rate of warming experienced (0.1 °C per decade) is some two to three times less than projected warming in coming decades, the interval between severe bleaching events has declined from 16 to 6 years, and evidence of chronic mortality from local human impacts is increasing. The study produced four recommendations for reducing bias when monitoring and assessing coral bleaching: coral colony size should be measured, unaffected colonies should be included in counts, quadrats or belt transects should be used and weighting coefficients in the calculation of indices should be used with caution.

**Subjects** Ecology, Marine Biology, Climate Change Biology

**Keywords** Coral bleaching, Western Indian Ocean, Acropora, Recovery, Northern Mozambique Channel, Coral reef, Eastern Africa, Climate change, Resilience

## INTRODUCTION

Coral bleaching is an increasingly common phenomenon on tropical coral reefs as background warming occurs and inter-annual modes of climate variability intensify (*McPhaden, Zebiak & Glantz, 2004; Hoegh-Guldberg et al., 2007*). Repeated major coral

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<footnote n="1">¹ CORDIO East Africa, Mombasa, Kenya</footnote>

<footnote n="2">² UMR Entropie, Laboratoire d'écologie marine, Université de la Reunion, Saint Denis, Reunion</footnote>

<footnote n="3">³ Department of Biotechnology and Biosciences, University of Milano—Bicocca, Milan, Italy</footnote>
bleaching events are now standard occurrence in most world regions (Donner, Rickbeil & Heron, 2017; Hughes et al., 2018), including the Caribbean (Eakin et al., 2010; Jackson et al., 2014), the Pacific (Chin et al., 2011), and the western Indian Ocean (McClanahan et al., 2014; Obura et al., 2017), and recently in concurrent years on the Great Barrier Reef (Hughes et al., 2017b). The Western Indian Ocean (WIO) has suffered repeated bleaching events, with the most extreme being in 1998 (Wilkinson et al., 1999; Goreau et al., 2000), but with smaller events before, most notably in 1983 (Faure et al., 1984) and since, in 2005 (McClanahan et al., 2005), 2007 (D Obura, 2007, unpublished data), 2010 (Eriksson, Wickel & Jamon, 2012) and 2016 (Nicet et al., 2016; Obura et al., 2017). The increasing frequency of major bleaching events (Hughes et al., 2018) is calling into question the long term survival of coral reef ecosystems, with most world regions predicted to experience severe bleaching conditions on an annual basis within the next 40–80 years (Van Hooidonk et al., 2016).

How well coral reefs will cope with these conditions is a major question in current research (Hughes et al., 2017a). The WIO was among the worst affected regions during the 1998 bleaching event. In that year three phenomena coincided—1998 was an unusually hot year globally, and strong positive phases of the El Niño Southern Oscillation (ENSO) and Indian Ocean Dipole (IOC) occurred in phase (Saji et al., 1999; McPhaden, Zebiak & Glantz, 2004). As a consequence, coral mortality at different reef sites varied between 50–80%, and accounted for a loss of 16% of healthy reefs (reviewed in Wilkinson, 2000). The Northern Mozambique Channel, one of the least known regions of the WIO, had variable levels of coral bleaching reported in the 1998 event (Souter, Obura & Linden, 2000; Wilkinson, 2000; Obura et al., 2018). While it is a center of diversity and accumulation for coral species (Obura, 2012; Obura, 2016), it may show some characteristics of being a climate refuge because of its low rate of temperature rise (McClanahan et al., 2007a; McClanahan et al., 2007b; McClanahan et al., 2014). However, larger scale studies present it as among the earliest parts of the WIO to face severe thermal stress conditions (Sheppard, 2003; Van Hooidonk et al., 2016).

Mayotte (12.1°S, 45.1°E) is the oldest island in the Comoro archipelago, located in the center of the Northern Mozambique Channel. It has somewhat lower coral diversity than surrounding mainland and Madagascar coasts on account of the island area effect (Obura, 2012). However, it has among the highest geomorphological diversity of reef habitats in the western Indian Ocean. It is highly eroded with high sedimentation and turbidity in the lagoon (Thomassin, 2001). Sea surface temperatures (SSTs) around Mayotte are warm and bimodal (Ateweberhan & McClanahan, 2010) determined by the monsoons and interactions of the South Equatorial Current with Madagascar, varying between 25.5 and 29 °C. Coral bleaching on Mayotte has been well documented in 1983 and 1998 (Faure et al., 1984; Quod et al., 2002), as well as in 2010 (Eriksson, Wickel & Jamon, 2012) (Nicet et al., 2016, L Bigot & D Obura, 2010, unpublished data).

This study is based on surveys in early June 2010 following the peak months of high sea surface temperatures from February to April (Fig. 1). Bleaching and mortality of corals were observed throughout the island's reefs. This paper focuses on comparisons among coral genera and coral colony size classes in bleaching and mortality patterns, and estimation
<figure><img src="image_4.png" /><figcaption>**Figure 1** Sea Surface Temperature (SST) in the Western Indian Ocean, by month, from January to July 2010. Mean monthly level 3 data at 4 km resolution, source: Moderate Resolution Imaging Spectro-radiometer (MODIS), https://oceancolor.gsfc.nasa.gov/cgi/l3.</figcaption></figure>

Full-size

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DOI: 10.7717/peerj.5305/fig-1

of the full impact of the bleaching event on the corals of Mayotte, in the context of repeat bleaching events.

## METHODS

Coral reef structures on Mayotte Island are diverse, including outer reef banks and slopes, inner slopes of the barrier, a second inner barrier reef at the southwest of the island and fringing reefs around the main island and smaller islets (Fig. 2). The island is densely populated, with high pressure on the lagoon from fishing, and sedimentation from runoff and land-use change (Thomassin, 2001; Bigot et al., 2018).

Sampling for coral bleaching was conducted on the Tara Oceans Expedition from 30 May–17 June 2010, following peak bleaching months. Twenty seven of the 34 sites (Table 1, Fig. 2) were sampled between a depth of 8 and 12 m, corresponding to the zone of maximum reef development, though on two fringing and one inner barrier sites the reef profile forced sampling to be done at 4–7 m, and on two outer barrier and the two bank reefs, sampling was done at 16–20 m. This paper reports on two survey methods collected as part of a more comprehensive dataset (Obura & Grimsdith, 2009). Coral size class structure was sampled with 1 m wide belt transects, including bleaching and mortality observations by colony,
<figure><img src="image_6.png" /><figcaption>**Figure 2** Map of Mayotte, showing the reef and lagoon structure, and sampling sites coded by reef zone (UNEP-WCMC, 2010).</figcaption></figure>

Full-size

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DOI: 10.7717/peerj.5305/fig-2
<table><caption>**Table 1** Sampling details of Tara Oceans Expedition to Mayotte, 2010. The table shows the depth characteristics of each site, the area of small coral quadrats and large coral transects samples, actual number of coral colonies counted, and standardized number and area of colonies (to 100 m²).</caption><thead><tr><th rowspan="2">SITE</th><th rowspan="2">Zone</th><th rowspan="2">Depth</th><th colspan="2">Area sampled (m²)</th><th rowspan="2"># colonies counted</th><th colspan="2">Standardized to 100 m²</th></tr><tr><th>&lt;10 cm</th><th>&gt;10 cm</th><th># colonies</th><th>area (m²)</th></tr></thead><tbody><tr><td>MA05</td><td>bank</td><td>20</td><td>3</td><td>12</td><td>132</td><td>1,625</td><td>68.5</td></tr><tr><td>MA24</td><td>bank</td><td>20</td><td>6</td><td>25</td><td>97</td><td>527</td><td>89.0</td></tr><tr><td>MA03</td><td>outer barrier</td><td>10</td><td>3</td><td>13</td><td>299</td><td>5,691</td><td>59.8</td></tr><tr><td>MA14</td><td>outer barrier</td><td>10</td><td>3</td><td>10</td><td>242</td><td>3,983</td><td>48.4</td></tr><tr><td>MA15</td><td>outer barrier</td><td>9</td><td>5</td><td>20</td><td>347</td><td>2,980</td><td>30.8</td></tr><tr><td>MA16</td><td>outer barrier</td><td>10</td><td>5</td><td>22</td><td>303</td><td>2,366</td><td>75.2</td></tr><tr><td>MA18</td><td>outer barrier</td><td>10</td><td>3</td><td>12</td><td>338</td><td>5,467</td><td>70.5</td></tr><tr><td>MA22</td><td>outer barrier</td><td>11</td><td>6</td><td>25</td><td>208</td><td>1,529</td><td>42.8</td></tr><tr><td>MA27</td><td>outer barrier</td><td>16</td><td>6</td><td>25</td><td>217</td><td>1,349</td><td>30.7</td></tr><tr><td>MA28</td><td>outer barrier</td><td>16</td><td>6</td><td>25</td><td>328</td><td>2,832</td><td>19.6</td></tr><tr><td>MA29</td><td>outer barrier</td><td>12</td><td>6</td><td>25</td><td>315</td><td>2,666</td><td>20.2</td></tr><tr><td>MA30</td><td>outer barrier</td><td>12</td><td>6</td><td>25</td><td>357</td><td>2,644</td><td>24.4</td></tr><tr><td>MA19</td><td>channel</td><td>10</td><td>5</td><td>20</td><td>256</td><td>2,165</td><td>27.0</td></tr><tr><td>MA08</td><td>inner barrier</td><td>10</td><td>4</td><td>20</td><td>341</td><td>3,045</td><td>40.2</td></tr><tr><td>MA10</td><td>inner barrier</td><td>10</td><td>3</td><td>11</td><td>248</td><td>4,824</td><td>36.7</td></tr><tr><td>MA32</td><td>inner barrier</td><td>6</td><td>6</td><td>25</td><td>186</td><td>1,175</td><td>90.3</td></tr><tr><td>MA12</td><td>double barrier</td><td>8</td><td>4</td><td>15</td><td>173</td><td>1,923</td><td>27.6</td></tr><tr><td>MA13</td><td>double barrier</td><td>10</td><td>3</td><td>10</td><td>190</td><td>2,880</td><td>47.6</td></tr><tr><td>MA04</td><td>inner</td><td>10</td><td>4</td><td>20</td><td>246</td><td>2,430</td><td>43.8</td></tr><tr><td>MA06</td><td>inner</td><td>10</td><td>5</td><td>20</td><td>305</td><td>2,665</td><td>72.6</td></tr><tr><td>MA07</td><td>inner</td><td>10</td><td>5</td><td>20</td><td>361</td><td>2,945</td><td>41.0</td></tr><tr><td>MA17</td><td>inner</td><td>9</td><td>6</td><td>25</td><td>208</td><td>1,351</td><td>17.9</td></tr><tr><td>MA20</td><td>inner</td><td>8</td><td>6</td><td>25</td><td>218</td><td>1,404</td><td>48.2</td></tr><tr><td>MA23</td><td>inner</td><td>11</td><td>6</td><td>25</td><td>170</td><td>1,643</td><td>22.4</td></tr><tr><td>MA25</td><td>inner</td><td>10</td><td>6</td><td>25</td><td>513</td><td>3,673</td><td>36.4</td></tr><tr><td>MA26</td><td>inner</td><td>11</td><td>6</td><td>25</td><td>236</td><td>1,932</td><td>10.5</td></tr><tr><td>MA34</td><td>inner</td><td>9</td><td>12</td><td>50</td><td>308</td><td>1,028</td><td>31.3</td></tr><tr><td>MA01</td><td>fringe</td><td>10</td><td>2</td><td>7</td><td>112</td><td>2,243</td><td>41.5</td></tr><tr><td>MA02</td><td>fringe</td><td>10</td><td>6</td><td>25</td><td>144</td><td>1,083</td><td>14.2</td></tr><tr><td>MA09</td><td>fringe</td><td>10</td><td>6</td><td>25</td><td>209</td><td>1,710</td><td>13.0</td></tr><tr><td>MA11</td><td>fringe</td><td>8</td><td>5</td><td>23</td><td>144</td><td>1,049</td><td>32.2</td></tr><tr><td>MA21</td><td>fringe</td><td>8</td><td>6</td><td>25</td><td>231</td><td>1,076</td><td>25.8</td></tr><tr><td>MA31</td><td>fringe</td><td>7</td><td>6</td><td>25</td><td>173</td><td>1,135</td><td>28.8</td></tr><tr><td>MA33</td><td>fringe</td><td>4</td><td>6</td><td>25</td><td>284</td><td>2,073</td><td>74.3</td></tr></tbody><tfoot><tr><td colspan="4">Totals</td><td>730</td><td>8,439</td><td>Averages:</td><td>2,327</td><td>41.3</td></tr><tr><td colspan="4"></td><td>176</td><td></td><td></td><td></td><td></td></tr></tfoot></table>
and visual estimation of abundance of coral genera on a 1–5 scale, and of percent coral cover.

Belt transects 1 m wide were used for sampling coral colony sizes. Coral colonies whose center fell within the belt and quadrats) were counted. The largest colony diameter was recorded in the size class bins: 11–20, 21–40, 41–80, 81–160, 161–320 and >320 cm. For corals smaller than 10 cm, subsampling was done using 1 m² quadrats at the 0, 5, 10, 15, 20, and 25 m transect marks, in size class bins 0–2.5, 3–5 and 6–10 cm. Colony condition was recorded as unaffected (no visible effect of thermal stress), pale, bleached, partially dead or fully dead, as exclusive categories by colony. Colonies were assigned to the most severe condition observed if that condition occupied more than 1/5 of the colony surface; i.e., a colony with bleaching and partial mortality was classed as partially dead if more than about 1/5 was dead. A 1 m stick was used to help guide estimation of transect width and mark the 1 m² quadrats, and the stick was marked at 10, 20, 40 and 80 cm to guide size estimation of coral colonies. A standard transect length of 25 m was targeted, but length was often limited by a high density of corals and time available per dive. Seventeen of the 34 sites were sampled with 25-m transects (Table 1). The smallest sampling was of two 1 m² quadrats and a 7-m belt transect, recording 18 small and 94 large corals, respectively. The minimum counts of 11 small and 86 large corals were recorded within a 25-m transect.

Sampling focused on coral genera that were already known to cover a range of bleaching susceptibility from high to low and that are generally common on East African reefs (Obura & Grimsdith, 2009): 1—low resistance to bleaching: *Acropora* (including *Isopora*), *Montipora*, *Pocillopora*, *Seriatopora*, *Stylophora*; 2—intermediate resistance to bleaching: *Echinopora*, *Dipsastraea*, *Favites*, *Goniastrea*, *Leptastrea*, *Platygyra*, *Acanthastrea*, *Coscinaraea*, *Fungia*, *Galaxea*, *Hydnophora*, *Lobophyllia*, *Oxypora*, *Pavona*, *Plerogyra*; 3—high resistance to bleaching: *Porites* (massive and branching morphologies recorded separately) and *Turbinaria*.

The relative abundance of all coral genera at a site was recorded by visual estimate, on a five-point scale (rare, uncommon, common, abundant, dominant) following *Devantier & Turak* (2017). An index of relative abundance for each genus was calculated from these estimates as the average of: the proportion of sites at which a genus was present, its average abundance across all sites, and maximum abundance at any site, all converted to 0–5 scale (Obura & Grimsdith, 2009).

For analysis of the coral size class data, all densities per genus were transformed to a standard area of 100 m². The number and area of colonies per 100 m² was used. Colony area was calculated for each size class using its median diameter and assuming the area of a coral colony is approximated by an ellipse with the second diameter half of the maximum (area = 1/2*pi*r²). Proportions of each of the colony condition classes were calculated based on abundance and area of each in each size class. For some analyses the number of classes was reduced to three, by aggregating pale and bleached (termed bleached) and partially and full dead (termed dead).

To investigate the impact of different approaches to monitoring and reporting bleaching, two variations of the bleaching and mortality data were analyzed. First, we tested the effect of excluding the proportion of normal colonies, because many programmes count or report
<figure><img src="image_8.png" /><figcaption>**Figure 3** Coral cover and condition in Mayotte, June 2010. (A) Coral cover by reef zone (mean ± se). The number of sites sampled in each zone is shown in parentheses in the x axis labels. (B) Proportional bleaching and mortality of corals in Mayotte, in June 2010, by number and area of colonies sampled.</figcaption></figure>

Full-size DOI: 10.7717/peerj.5305/fig-3

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only colonies showing some level of bleaching and/or mortality, and not count the number of normal corals. Second, we tested the effect of weighting conditions of increasing severity, i.e., from pale, to bleached, to partially dead to dead (see McClanahan et al., 2007b). We applied the following weights: 1*pale, 2*bleaching, 3*partial mortality and 4*mortality. Cluster analysis using the Bray-Curtis similarity index was found to give results easy to interpret for the pros and cons of the different approaches. Analysis was conducted in PRIMER v6.0 with significant groupings identified using SIMPROF (Clarke & Warwick, 2001).

Estimates of the potential final mortality of corals were obtained from the size class data based on the assumption that minimum mortality from the event would be equivalent to current levels of partial and full mortality. This was obtained by subtracting the sum of partial and full mortality from the total counts for all size classes for each genus. By contrast, the assumption that all currently bleached corals would die gives an estimate of maximum mortality from the event, thus subtracting the counts of bleached corals plus partial and fully dead corals. We assumed that pale corals survived.

## RESULTS

Thirty-four sites were surveyed overall, in seven reef zones (Table 1, Fig. 2). In total, 8,439 colonies were sampled. Coral cover varied from a maximum of almost 80% on the offshore Banc d'Iris, between 35–45% for outer barrier, inner barrier and small-island reefs within the lagoon, slightly over 30% for fringing reefs on the main island, and <30% in the Passe en ‘S’, the only channel site surveyed (Fig. 3A). Nevertheless, coral cover was not significantly different by reef zone (One Way ANOVA, (F = 1.338, P = 0.275). No patterns were observed, nor have been reported in the literature, of differential coral genus distributions around the island unrelated to reef zone, so all sites were lumped together in
<figure><img src="image_10.png" /><figcaption>**Figure 4** Coral genera abundance, Mayotte, 2010. (A) Relative abundance of all coral genera identified, aggregated across sites. The index of relative abundance ranges from a maximum of 5, with zero representing absence. Site level scores were: rare (1), uncommon (2), common (3), abundant (4) and dominant (5). (B) Area (biomass) of each genus measured in size class transects (in m² per 100 m² of reef area), ranked from highest to lowest. Genera sampled in both methods (A and B) shaded red, genera sampled only in visual estimates (in A) shaded blue.</figcaption></figure>

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DOI: 10.7717/peerj.5305/fig-4

subsequent analyses, to focus on patterns in bleaching by coral traits (taxonomy, colony size). Across all sites, average coral colony abundance was 2327 (±1,253) and area was 41 m² (±21.9) per 100 m² of reef. By abundance, 35% of coral colonies were affected by the bleaching event, with 18.4% being pale, 9.3% bleached, 2% partially dead and 5.3% dead (Fig. 3B). By area, 52% of coral area or biomass was affected by bleaching, with 19.3% being pale, 10.7% bleached, 4.8% partially dead and 17.5% dead.

A total of 60 coral genera were recorded (Fig. 4A), with clear dominance by *Acropora*, followed by *Porites*. All of the most abundant nine genera, and 17 of the top 25, were among those targetted for size class sampling (Fig. 4B). Genera omitted from size class sampling, but that were present at moderate levels of abundance included *Leptoseris* (rank = 10), *Echinophyllia* (11), *Halomitra* (15), *Mycedium* (17), *Pachyseris* (18) and *Podabacia* (20). *Acropora* contributed 58% of the total area of sampled corals (Fig. 4B), about five times greater than *Porites*, the second genus. Sixteen genera were recorded at abundances between 1–10 m² per 100 m² of reef, with four at low abundance between 0.1–1 m², and two at very low abundance (*Stylophora* and *Turbinaria*). For the genera sampled using both methods, the logarithm of the area sampled and their visually assessed relative abundance index were strongly correlated (r² = 0.894), though some genera switched ranks between the two methods (Fig. 4).
Bleaching and mortality varied widely across genera, from 100% bleached in *Turbinaria* to 6% pale in *Acanthastrea*. Genera with fewer than 20 colonies sampled (i.e., *Turbinaria*, *Oxypora*, and *Stylophora*) are excluded from further analysis, so the following results are for the 20 remaining genera. The most susceptible genera to combined bleaching and mortality (Fig. 5A) were *Pocillopora* and *Montipora* (>70% total impact) followed by *Lobophyllia*, *Porites* (massive species), *Dipsastrea*, *Goniastrea*, *Acropora* and a range of others (40–65%). *Leptastrea* and *Acanthastrea* showed lowest levels of combined pale and bleached colonies (≈6%), with no mortality. *Pocillopora* and *Acropora* were the only genera with high levels of mortality (47% and 32%, respectively, combined partially dead and dead), though mortality was also observed in *Porites* (massive and branching species), *Echinopora*, *Favites*, *Seriatopora*, *Platygyra*, and *Hydnophora*. *Pocillopora* showed the most extensive and complex response (18% pale, 14% bleached, 21% partially dead and 26% dead), while *Acanthastrea* was the least impacted (6% pale). Most genera showed a higher degree of paling (up to 50% in *Dipsastraea*) than full bleaching (up to 31% in *Montipora*). Simplified into three categories (unaffected, bleached and dead) and illustrated in a ternary plot, *Acropora* and *Pocillopora* showed intermediate levels of all three (Fig. 5B). Other genera occupy a zone near the axis marking low mortality, at varied levels of unaffected and bleached.

Cluster analyses showed the impact of excluding unaffected colonies, and the use of weighting coefficients (Fig. 5C). Without weights, including ‘unaffected’ as a category distinguished three significant clusters (case 1): (a) *Acropora* and *Pocillopora* due to their high combined bleaching and mortality, (b) a large group of intermediate genera showing some bleaching and limited mortality, and (c) a smaller group of five genera mostly affected by bleaching, but at lower abundance. Excluding ‘unaffected’ (case 2) shifted the boundary between (b) and (c) such that (c) was reduced to two genera (*Leptastrea* and *Acanthastrea*), the other three genera shifting into group (b). Using weighting coefficients and including ‘unaffected’ (case 3) altered case 1 by splitting the five low-response genera into two groups—the three that were pushed into group (b) in one group, and *Acanthastrea* and *Leptastrea* in a separate group. Finally, using weighting coefficients but excluding ‘unaffected’ (case 4) put all of the genera except *Acanthastrea* and *Leptastrea* into a single group, and these two in their own small group.

Two conclusions can be drawn from the above. First, that including normal or 'unaffected' colonies in field counts and analysis is important, as cases 2 and 4 both showed less discrimination of bleaching responses (less discrimination of the first order spatial patterns in Fig. 5B) than cases 1 and 3, respectively. Second, that including weighting coefficients alters the results, but varying with the set of variables included. Comparing cases 2 and 4, adding weighting coefficients worsened the result, removing the distinction between *Acropora* and *Pocillopora* (bleaching with mortality) from the main group of genera (paling and bleaching, no mortality). Comparing cases 1 and 3, adding weighting coefficients added resolution in the low-response low-abundance group, distinguishing *Leptastrea* and *Acanthastrea* (with only minor paling and bleaching, <6%, Fig. 5A) from *Porites* (branching), *Favites* and *Seriatopora* (from 20-33% impacted, and varied amounts of paling, bleaching and mortality). While the latter result adds value to interpretation,
a

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b

<figure><img src="image_13.png" /></figure>

c

<table><thead><tr><th rowspan="2"></th><th colspan="2">Case 1</th><th colspan="2">Case 2</th><th colspan="2">Case 3</th><th colspan="2">Case 4</th></tr><tr><th>no</th><th>no</th><th>yes</th><th>yes</th><th>with</th><th>without</th><th>with</th><th>without</th></tr></thead><tbody><tr><td><strong>Pocillopora</strong></td><td>a</td><td>a</td><td>a</td><td>a</td><td>a</td><td>a</td><td>a</td><td>a</td></tr><tr><td><strong>Acropora</strong></td><td>a</td><td>a</td><td>a</td><td>a</td><td>a</td><td>a</td><td>a</td><td>a</td></tr><tr><td><strong>Montipora</strong></td><td>b</td><td>b</td><td>b</td><td>a</td><td>a</td><td>a</td><td>a</td><td>a</td></tr><tr><td><strong>Porites (m)</strong></td><td>b</td><td>b</td><td>b</td><td>a</td><td>a</td><td>a</td><td>a</td><td>a</td></tr><tr><td><strong>Echinopora</strong></td><td>b</td><td>b</td><td>b</td><td>a</td><td>a</td><td>a</td><td>a</td><td>a</td></tr><tr><td><strong>Lobophyllia</strong></td><td>b</td><td>b</td><td>b</td><td>a</td><td>a</td><td>a</td><td>a</td><td>a</td></tr><tr><td><strong>Hydnophora</strong></td><td>b</td><td>b</td><td>b</td><td>a</td><td>a</td><td>a</td><td>a</td><td>a</td></tr><tr><td><strong>Goniastrea</strong></td><td>b</td><td>b</td><td>b</td><td>a</td><td>a</td><td>a</td><td>a</td><td>a</td></tr><tr><td><strong>Dipsastraea</strong></td><td>b</td><td>b</td><td>b</td><td>a</td><td>a</td><td>a</td><td>a</td><td>a</td></tr><tr><td><strong>Fungia</strong></td><td>b</td><td>b</td><td>b</td><td>a</td><td>a</td><td>a</td><td>a</td><td>a</td></tr><tr><td><strong>Plerogyra</strong></td><td>b</td><td>b</td><td>b</td><td>a</td><td>a</td><td>a</td><td>a</td><td>a</td></tr><tr><td><strong>Platygyra</strong></td><td>b</td><td>b</td><td>b</td><td>a</td><td>a</td><td>a</td><td>a</td><td>a</td></tr><tr><td><strong>Galaxea</strong></td><td>b</td><td>b</td><td>b</td><td>a</td><td>a</td><td>a</td><td>a</td><td>a</td></tr><tr><td><strong>Pavona</strong></td><td>b</td><td>b</td><td>b</td><td>a</td><td>a</td><td>a</td><td>a</td><td>a</td></tr><tr><td><strong>Coscinaraea</strong></td><td>b</td><td>b</td><td>b</td><td>a</td><td>a</td><td>a</td><td>a</td><td>a</td></tr><tr><td><strong>Porites (b)</strong></td><td>c</td><td>b</td><td>c</td><td>a</td><td>a</td><td>a</td><td>a</td><td>a</td></tr><tr><td><strong>Favites</strong></td><td>c</td><td>b</td><td>c</td><td>a</td><td>a</td><td>a</td><td>a</td><td>a</td></tr><tr><td><strong>Seriatopora</strong></td><td>c</td><td>b</td><td>c</td><td>a</td><td>a</td><td>a</td><td>a</td><td>a</td></tr><tr><td><strong>Leptastrea</strong></td><td>c</td><td>c</td><td>d</td><td>b</td><td>b</td><td>b</td><td>b</td><td>b</td></tr><tr><td><strong>Acanthastrea</strong></td><td>c</td><td>c</td><td>d</td><td>b</td><td>b</td><td>b</td><td>b</td><td>b</td></tr></tbody></table>

**Figure 5** Bleaching and mortality of coral genera. (A) Proportion of bleaching and mortality by genus, excluding the two least abundant genera. (B) Ternary plot of unaffected, bleached (pale plus bleached) and dead (partial plus full mortality) for genera sampled in the study. Key genera are indicated using three-letter codes that correspond to the first three letters of genus names in (A) and (C), except for 'fat' (*Favites*), 'mtp' (*Montipora*), 'porb' (branching *Porites*) and 'porm' (massive *Porites*). (C) Cluster analysis results with SIMPROF test to show significant clusters of genera at *p* = 5% level for four cases: unweighted proportions of pale, bleached, partial and full mortality analyzed with (case 1) and without (case 2) the proportion of unaffected colonies; and with weights applied to bleached (x2), partial mortality (x3) and full mortality (x4) (see methods), also with (case 3) and without (case 4) the proportion of unaffected colonies. Letters show significant groups within each test.

Full-size DOI: 10.7717/peerj.5305/fig-5

<figure><img src="image_14.png" /></figure>
weighting should be used with caution and tested on each dataset to which it is applied, to
fully understand how it influences the results.

By area, the coral community was dominated by mature colonies in the 81–160 cm size class (Fig. 6A) followed by younger colonies from 11–80 cm and then the largest colonies above 1.6 m. Numerically, 6–10 and 11–20 cm corals were most abundant. Bleaching and mortality varied by colony size (Fig. 6B). Both bleaching and mortality showed a strong linear increase with coral colony size, up to 1.6 m. Of the smallest colonies only 17% were affected by bleaching, with 3% suffering mortality. These proportions increased progressively to the most impacted size class, 81–160 cm, for which 67% of colonies were affected with 35% mortality. The sample size for corals >160 cm was low, with 20 and 1 in the 160–320 and >320 cm size classes, respectively, compared to from 131 to 4257 colonies in the smaller size classes. For corals <10 cm, the ratio of mortality to bleaching was <0.2, which increased to 0.3–0.5 for intermediate colonies from 10–80 cm. For larger corals, 81–160 and 161–320 cm, mortality exceeded bleaching, with ratios of 1.6 and 1.1 respectively.

DISCUSSION

Bleaching and mortality averaged 30 and 22%, respectively, across all sites (Fig. 3B) though with high levels of variability from near zero at sites in the south to maximum mortality levels at sites in the north and east of Mayotte. These results agree largely with Eriksson, Wickel & Jamon (2012) who found 10% bleached and 40% dead corals on the more highly impacted northern and eastern reefs during May 2010. Percent coral cover varied over a wide range across reef zones in Mayotte (Fig. 3A) though without statistical significance. Accordingly, we aggregate the coral community of Mayotte to analyze variance in bleaching response among genera.

Do genus and size affect coral bleaching?

*Pocillopora* and *Acropora* were the only coral genera to show significant mortality as a result of the 2010 event, setting them apart from the others as the most susceptible genera to bleaching, in accordance with findings throughout the Indo-Pacific (*Marshall & Baird, 2000; Obura, 2001; Loya et al., 2001; McClanahan et al., 2004; Van Woesik et al., 2012*). Cluster analysis of the bleaching responses identified two additional groups of species—a large group with intermediate responses characterized by variable but low mortality and variable levels of pale and bleached colonies (group ‘b’, case 1, Fig. 5C), and a smaller group with low levels of bleaching and variable but low mortality (group ‘c’). The middle group included a wide range of genera including *Porites* (massive species), various merulinids, agariciids, siderastreids, and fungiids. The last group included *Porites* (branching species), *Favites*, *Seriatopora*, *Acanthastrea*, and *Leptastrea*. These groups are in broad agreement with previous reports from East Africa (e.g., massive *Porites* is usually ranked among the least susceptible to bleaching and mortality, branching *Porites* among the most susceptible— *Obura, 2001; McClanahan, 2004*). We have not analyzed the symbiont characteristics of genera sampled here, which has significant effects on bleaching susceptibility and mortality, particularly when different host-symbiont combinations may be possible (e.g., see
<figure><img src="image_15.png" /></figure>

<figure><img src="image_16.png" /><figcaption>**Figure 6** Bleaching and mortality of corals, by colony size. (A) Size class distributions of corals from all sites sampled, by number of colonies (left axis, closed circles) and area (in m²) of colonies (right axis, open triangles) per 100 m² of reef area. (B) Overall bleaching and mortality proportions by colony area in each size class. Data is combined across all coral genera sampled in Mayotte, in June 2010.</figcaption></figure>

Full-size DOI: 10.7717/peerj.5305/fig-6

<figure><img src="image_17.png" /></figure>
<figure><img src="image_18.png" /><figcaption>**Figure 7** Estimates of the minimum and maximum impact of the 2010 coral bleaching event on the coral community of Mayotte, 2010. Size class distribution of all corals by (A) abundance and (B) area in each size class. The following results are presented for the key taxa *Acropora*, *Pocillopora*, *Porites* (massive species) and other genera combined: (C) estimated maximum percentage loss of corals, by number and area of colonies; (D–G) estimated minimum and maximum percentage loss by area in each size class; (H) estimated maximum percentage loss of corals by size class. Legend in plot A applies to plots B and D–G.</figcaption></figure>

Full-size

<figure><img src="image_19.png" /></figure>

DOI: 10.7717/peerj.5305/fig-7

Stat et al., 2009; Baker & Romanski, 2007; Oliver & Palumbi, 2009). Overall, though this appeared to be a severe bleaching event for reefs in Mayotte due to the dominance of *Acropora* and consequent loss of total coral cover, and visual dominance of bleached and dead *Acropora* and *Pocillopora*, the thermal stress to other genera was not sufficient to result in significant mortality.

A clear size differential in bleaching and mortality susceptibility was found, with susceptibility being greatest in large corals. For corals in the three smallest size classes (Fig. 6B) the proportion of bleached colonies increased (15 to 25%) with size, with little increase in the proportion of mortality (<5%). For adult corals from 10 cm and above, the proportion of bleached corals remained relatively stable (25%), but the proportion of mortality increased (10 to 40%), and exceeded the proportion bleached. This response was strongly determined by the size-dependent response of *Acropora*, but it did occur in other genera (Fig. 7H). Lower bleaching levels in small colonies, and particularly recruits,
has been noted in other locations and coral taxa, particularly *Oculina patagonica* in the Mediterranean (*Shenkar, Fine & Loya, 2005*), and three dominant species in the Florida Keys (*Colpophyllia natans*, *Montastrea faveolata*, and *Siderastrea siderea*, (*Brandt, 2009*). However, in a mild bleaching event *Ortiz, Del C Gomez-Cabrera & Hoegh-Guldberg (2009)* found no relation of size to bleaching extent, and *Bak & Meesters (1999)* predicted that bleaching impacts would be selectively higher on small rather than large corals.

From a methodological point of view, these results suggest several important considerations for measuring the impact of bleaching events at colony level, and extrapolating to community level indices. First, colony size is important in the bleaching susceptibility of corals for two reasons—smaller corals are less susceptible to bleaching, and larger corals have an exponentially greater contribution to biomass and area. Second, it is important to include unaffected colonies in the counts, as this improves identification of differential bleaching responses (Fig. 5C), and without total numbers of colonies the prevalence of bleaching and mortality in relation to the total population cannot be determined. Third, a corollary of the first two, is the importance of an unbiased sample of all corals, unaffected and bleached, and across all size classes. Without a strict fixed-area sampling method, such as with a physical transect or quadrat as a guide, unconstrained or haphazard counts are likely to both (a) oversample colonies that show a response over unaffected ones, as observers will tend to count what they are looking for (bleached and dead corals) and many normal colonies are brown and inconspicuous, and (b) small colonies will always be under-sampled compared to larger colonies, particularly when including sizes under 10 cm. Fourth, differential weighting of bleaching and mortality categories can have a strong influence on results, so should be done with caution in each case. In our results it improved discrimination of low-response groups when all colonies (impacted and unaffected) were included, but when unaffected corals were excluded it worsened the result. Thus where sampling is not restricted by physical quadrats or transects, and the size of corals is not measured (one and three above), the impact of weighting on results may not be possible to ascertain.

## Estimating the impact of a bleaching event

The surveys took place in early June, over 1 month after the end of peak temperatures at the end of April 2010 (Fig. 1), so this dataset likely presents peak levels of combined bleaching and mortality. This is a common challenge in interpreting the eventual impact of a bleaching event, as surveys are often targeted for peak bleaching conditions, but unless follow up surveys are done, it cannot be known if bleached corals recovered or died. However, the envelope of possible outcomes of a bleaching event can be estimated from peak bleaching levels assuming further mortality from bleaching is either zero or maximal. That is, currently bleached corals all recover, or die, respectively.

The present dataset allows this to be done across coral size classes and genera, to estimate minimum and maximum potential impact of the bleaching event (Fig. 7). By number of colonies the minimum and maximum loss of corals appears minor (Fig. 7A) but is significant by area (Fig. 7B), particularly for 81–160 cm corals. Maximum mortality by colony abundance is estimated at 10–15% for *Acropora, Porites* (massive) and other
genera (Fig. 7C), but at 50% for *Pocillopora*. By contrast, maximum mortality by colony area is estimated at 40% for *Acropora*, 25% for *Porites* (massive), <20% for other genera (Fig. 7C), but at >60% for *Pocillopora*. By colony abundance, maximum mortality overall is estimated at 16%, but by colony area, 32%, a major difference in result affected by consideration of colony area. This is because the bleaching event preferentially impacted larger colonies, particularly *Acropora*, eliminating the dominance of 81–160 m colonies (Fig. 7D). Reefs in Mayotte are strongly dominated by staghorn and tabular *Acropora* species, and dominance of the 81–160 cm size class in April suggests the community was approaching maturity where the community would be dominated by even larger stands of tabular and staghorn *Acropora*. The bleaching event strongly flattened the size class distribution with similar area in 41–320 cm classes after the event.

*Pocillopora* populations were strongly dominated by 21–40 cm and 11–20 cm colonies pre-bleaching (Fig. 7E), providing the corresponding peak in the overall population curve (Figs. 5A, 6B); their area was reduced by about 60% by the bleaching event (Fig. 7C), though they still remained dominant over other size classes of *Pocillopora*. The population of massive *Porites* was strongly dominated by 81–160 cm corals, which remained dominant after bleaching. The remaining genera were most strongly represented by 11–40 cm colonies, and mortality was relatively minor and evenly spread across them, maintaining the same size class distribution following bleaching. Finally, estimated maximum mortality increased with size for all corals and for the three key genera *Acropora*, *Pocillopora*, and *Porites* (Fig. 7H). Interestingly, these three genera all show a decline in mortality for their largest size class.

## Recurring bleaching in Mayotte

The coral reefs of Mayotte have been impacted by multiple significant bleaching events. In May–June 1983 bleaching was documented at 0–18% for fringing reefs, 30–45% for lagoon reefs and 30–75% for outer barrier reefs, though an indication of the final mortality was not noted (Faure et al., 1984). In 1998, 36% of the reefs had not recovered from the 1983 bleaching event, and mortality of >80% of *Acropora* tables on outer reef slopes was reported from April to August (Quod et al., 2002), which judging by patterns in this study may have reflected approximately 50% mortality including inner reefs. The 2010 event recorded here resulted in 32% mortality of all corals, and just under 40% for *Acropora* alone (Fig. 7C). Observations in 2016 suggest that mortality of corals was between 25 and 50% using the same methods used here (by area, D Obura, pers. obs., 2016), and was recorded at 10–30% by colony number using other methods (Nicet et al., 2016), so roughly comparable to the 2010 event.

In all four events, higher impact occurred on outer barrier reefs and lower levels in the lagoon and on fringing reefs, and the most dramatic bleaching and mortality was of tabular and staghorn *Acropora* colonies on outer reefs. Because of its dominance of the coral community, *Acropora's* response to thermal stress dominated the overall community response. The intervals between these major bleaching events has progressively declined—from 16 years to ten and six years. Across all of these events the reefs have apparently achieved considerable recovery and maintained the same dominance by *Acropora*. This
suggests a high degree of community resilience, likely partly a result of high levels of connectivity (Crochelet et al., 2016) due to the complex eddies that maintain high self-seeding of reefs within the northern Mozambique channel (Obura et al., 2018; Bigot et al., 2018).

However, anthropogenic stresses in Mayotte from both fisheries and water quality degradation (Wickel & Thomassin, 2005) are increasingly evident in the greater prevalence of coral disease and chronic mortality from unknown sources (D Obura, pers. obs., 2016). This will likely undermine the natural resilience of the reefs (Obura, 2005; Hughes et al., 2010) and may reduce their ability to recover from the 2016 bleaching event.

Between latitude S 12–13.5 and longitudes E 44.5–45.5 (a box around Mayotte) SST has warmed by 0.096 °C per decade for the thirty-year period from 1981–2010 (Reynolds et al., 2002), slightly less than the global level of 0.147 °C per decade (Rayner et al., 2003). Mayotte is in the region with the lowest SST rise in Eastern Africa (McClanahan et al., 2007a). Donner (2009) estimated a rate of SST rise to which corals must adapt to avoid catastrophic coral decline, of 1.5 °C in 50–80 years. This is 0.2–0.3 °C per decade, some two to three times higher than the rise in temperatures that coral reefs in Mayotte have experienced over the course of four bleaching events. While Mayotte's reefs have shown remarkable resilience so far, it is not clear that they are acclimating or adapting sufficiently to the rise experienced of 0.1 °C per decade. Further, the shorter intervals for recovery between events, matching the global pattern now at sub-decadal levels (Hughes et al., 2018), is approaching limits for recovery consistently used in framing the onset of 'catastrophic' bleaching (Sheppard, 2003; Van Hooidonk et al., 2016).

## CONCLUSION

The most recent analysis identifies 2030 as approximately the year in which Mayotte will experience Annual Severe Bleaching under RCP 8.5 (business as usual scenario, equivalent to today's CO2 emission rates; Van Hooidonk et al., 2016). That the reefs are already experiencing decadal severe bleaching only 15–20 years earlier is strong indication that the trajectory for coral reefs in the region towards decline may be inexorable on the time scales at hand, and that the reefs cannot withstand annual occurrence of the scale of bleaching documented in 1983, 1998 and 2010, and repeated in 2016 (Nicet et al., 2016). Although the Northern Mozambique Channel may be a center of diversity and of key significance to the Western Indian Ocean at large (Obura, 2012; Obura et al., 2018), it may not be a refuge from warming for coral reefs (McClanahan et al., 2014) and urgent and emergency planning is needed to identify what can be done to secure the best possible future not just for the reefs of Mayotte or the WIO, but also more broadly on a global scale (Beyer et al., 2018).

## ACKNOWLEDGEMENTS

We are grateful to Etienne Bourgois, the Tara schooner and its captain Hervé Bourmand, Mathieu Oriot (Diving Officer), the Tara crew, the Oceans Consortium, and James Mbugua. Tara Oceans would not exist without continuous support from 23 institutes
(http://oceans.taraexpeditions.org). This article is contribution number 77 of the Tara Oceans Expedition 2009–2012.

**ADDITIONAL INFORMATION AND DECLARATIONS**

**Funding**

Funding for David Obura was provided by the Western Indian Ocean Marine Science Association, Grant No: MASMA/OR/2008/05. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

**Grant Disclosures**

The following grant information was disclosed by the authors:
Western Indian Ocean Marine Science Association: MASMA/OR/2008/05.

**Competing Interests**

The authors declare there are no competing interests.

**Author Contributions**

* David O. Obura conceived and designed the experiments, performed the experiments, analyzed the data, contributed reagents/materials/analysis tools, prepared figures and/or tables, authored or reviewed drafts of the paper, approved the final draft.

* Lionel Bigot performed the experiments, contributed reagents/materials/analysis tools, authored or reviewed drafts of the paper, approved the final draft.

* Francesca Benzoni conceived and designed the experiments, approved the final draft, expedition leader and funding.

**Data Availability**

The following information was supplied regarding data availability:
The raw data are provided in a [Supplemental File](#).

**Supplemental Information**

Supplemental information for this article can be found online at [http://dx.doi.org/10.7717/peerj.5305#supplemental-information](http://dx.doi.org/10.7717/peerj.5305#supplemental-information).

**REFERENCES**

**Ateweberhan M, McClanahan TR. 2010.** Relationship between historical sea-surface temperature variability and climate change-induced coral mortality in the western Indian Ocean. *Marine Pollution Bulletin* **60**:964–970
DOI 10.1016/j.marpolbul.2010.03.033.

**Bak RPM, Meesters E. 1999.** Population structure as a response of coral communities to global change. *American Zoologist* **39**:56–67 DOI 10.1093/icb/39.1.56.

**Baker AC, Romanski AM. 2007.** Multiple symbiotic partnerships are common in scleractinian corals, but not in octocorals: comment on Goulet (2006). *Marine Ecology Progress Series* **335**:237–242 DOI 10.3354/meps335237.
Beyer HL, Kennedy EV, Beger M, Chen CA, Cinner J, Darling E, Eakin CM, Gates R, Heron SF, Knowlton N, Obura DO, Palumbi SR, Possingham HP, Puotinen M, Runting RK, Skirving W, Spalding M, Wilson K, Wood S, Veron JE, Hoegh-Guldberg O. 2018. Long-term risk-sensitive planning for conserving coral reefs under rapid climate change. *Conservation Letters* Epub ahead of print June 27 2018 DOI 10.1111/conl.12587.

Bigot L, Chabanet P, Cuet P, Cauvin B, Durville P, Mulochau T, Nicet JB, Tessier E, Thomassin B, Wickel J, Naim O. 2018. The French territories in the South Western Indian Ocean. In: Sheppard Charles, ed. *World seas: an environmental valuation, volume II: the Indian Ocean to the Pacific*. Second Edition. Elsevier.

Brandt ME. 2009. The effect of species and colony size on the bleaching response of reef-building corals in the Florida Keys during the 2005 mass bleaching event. *Coral Reefs* 28:911–924 DOI 10.1007/s00338-009-0548-y.

Chin A, Lison De Loma T, Reytar K, Planes S, Gerhardt K, Clua E, Burke L, Wilkinson C. 2011. *Status of coral reefs of the Pacific and outlook: 2011*. Paris and Apia: Publishers Global Coral Reef Monitoring Network, 1–260.

Clarke KR, Warwick RM. 2001. *Change in marine communities: an approach to statistical analysis and interpretation*. Second Edition. Plymouth: PRIMER-E.

Crochelet E, Roberts J, Lagabrielle E, Obura DO, Petit M, Chabanet P. 2016. A model-based assessment of reef larvae dispersal in the Western Indian Ocean reveals regional connectivity patterns—potential implications for conservation policies. *Regional Studies in Marine Science* 7:159–167 DOI 10.1016/j.rsma.2016.06.007.

Devantier L, Turak E. 2017. Species richness and relative abundance of reef-building corals in the Indo-West Pacific. *Diversity* 9:Article 25 DOI 10.3390/d9030025.

Donner SD. 2009. Coping with commitment: projected thermal stress on coral reefs under different future scenarios. *PLOS ONE* 4:e5712 DOI 10.1371/journal.pone.0005712.

Donner SD, Rickbeil GJM, Heron SF. 2017. A new, high-resolution global mass coral bleaching database. *PLOS ONE* 12(4):e0175490 DOI 10.1371/journal.pone.0175490.

Eakin CM, Morgan JA, Heron SF, Smith TB, Liu G, Alvarez-Filip L, Baca B, Bartels E, Bastidas C, Bouchon C, Brandt M, Bruckner AW, Bunkley-Williams L, Cameron A, Causey BD, Chiappone M, Christensen TRL, Crabbe MJC, Day O, La Guardia de E, Diaz-Pulido G, DiResta D, Gil-Agudelo DL, Gilliam DS, Ginsburg RN, Gore S, Guzmán HM, Hendee JC, Hernández-Delgado EA, Husain E, Jeffrey CFG, Jones RJ, Jordán-Dahlgren E, Kaufman LS, Kline DI, Kramer PA, Lang JC, Lirman D, Mallela J, Manfrino C, Maréchal J-P, Marks K, Mihaly J, Miller WJ, Mueller EM, Muller EM, Orozco Toro CA, Oxenford HA, Ponce-Taylor D, Quinn N, Ritchie KB, Rodríguez S, Ramírez AR, Romano S, Samhouri JF, Sanchez JA, Schmahl GP, Shank BV, Skirving WJ, Steiner SCC, Villamizar E, Walsh SM, Walter C, Weil E, Williams EH, Roberson KW, Yusuf Y. 2010. Caribbean corals in crisis: record thermal stress, bleaching, and mortality in 2005. *PLOS ONE* 5:e13969 DOI 10.1371/journal.pone.0013969.
Eriksson H, Wickel J, Jamon A. 2012. Coral bleaching and associated mortality in Mayotte, Western Indian Ocean. *Western Indian Ocean Journal of Marine Science* 11:113–118.

Faure G, Guillaume M, Payri C, Thomassin BA, Van Praet M, Vasseur P. 1984. Sur un phénomène remarquable de blanchiment et de mortalité massive des madréporaires dans le complexe récifal de l’île Mayotte (SW Ocean Indien). *Comptes Rendus de l'Académie des Sciences* 299-III-15:637–642.

Goreau T, McClanahan TR, Hayes R, Strong A. 2000. Conservation of coral reefs after the 1998 global bleaching event. *Conservation Biology* 14:5–15
DOI 10.1046/j.1523-1739.2000.00011.x.

Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME. 2007. Coral reefs under rapid climate change and ocean acidification. *Science* 318:1737–1742
DOI 10.1126/science.1152509.

Hughes TP, Anderson KD, Connolly SR, Heron SF, Kerry JT, Lough JM, Baird AH, Baum JK, Berumen ML, Bridge TC, Claar DC, Eakin CM, Gilmour JP, Graham NAJ, Harrison H, Hobbs J-PA, Hoey AS, Hoogenboom M, Lowe RJ, McCulloch MT, Pandolfi JM, Pratchett M, Schoepf V, Torda G, Wilson SK. 2018. Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. *Science* 359:80–83 DOI 10.1126/science.aan8048.

Hughes TP, Barnes ML, Bellwood DR, Cinner JE, Cumming GS, Jackson JBC, Kleypas J, Van de Leemput IA, Lough JM, Morrison TH, Palumbi SR, Van Nes EH, Scheffer M. 2017a. Coral reefs in the Anthropocene. *Nature* 546:82–90
DOI 10.1038/nature22901.

Hughes TP, Graham NAJ, Jackson JBC, Mumby PJ, Steneck RS. 2010. Rising to the challenge of sustaining coral reef resilience. *Trends in Ecology & Evolution* 25:633–642 DOI 10.1016/j.tree.2010.07.011.

Hughes TP, Kerry JT, Álvarez-Noriega M, Álvarez-Romero JG, Anderson KD, Baird AH, Babcock RC, Beger M, Bellwood DR, Berkelmans R, Bridge TC, Butler IR, Byrne M, Cantin NE, Comeau S, Connolly SR, Cumming GS, Dalton SJ, Diaz-Pulido G, Mark Eakin C, Figueira WF, Gilmour JP, Harrison HB, Heron SF, Hoey AS, Hobbs J-PA, Hoogenboom MO, Kennedy EV, Kuo C-Y, Lough JM, Lowe RJ, Liu G, McCulloch MT, Malcolm HA, McWilliam MJ, Pandolfi JM, Pears RJ, Pratchett MS, Schoepf V, Simpson T, Skirving WJ, Sommer B, Torda G, Wachenfeld DR, Willis BL, Wilson SK. 2017b. Global warming and recurrent mass bleaching of corals. *Nature* 543:373–377 DOI 10.1038/nature21707.

Jackson JBC, Donovan MK, Cramer KL, Lam VYY, Bak RPM, Chollett I, Connolly SR, Cortés J, Dustan P, Eakin CM, Friedlander AM, Greenstein BJ, Heron SF, Hughes T, Miller J, Mumby P, Pandolfi JM, Rogers CS, Steneck R, Weil E, Alemu I JB, Alevizon WS, Arias-González JE, Atkinson A, Ballantine DL, Bastidas C, Bouchon C, Bouchon-Navaro Y, Box S, Brathwaite A, Bruno JF, Caldow C, Carpenter RC, Charpentier BH, Causey B, Chiappone M, Claro R, Cróquer A, Debrot AO,
Edmunds P, Fenner D, Fonseca A, Ford MC, Forman K, Forrester GE, Garza-Pérez JR, Gayle PMH, Grimsditch GD, Guzmán HM, Harborne AR, Hardt MJ, Hixon M, Idjadi J, Jaap W, Jeffrey CFG, Johnson AE, Jordán-Dahlgren E, Koltes K, Lang JC, Loya Y, Majil I, Manfrino C, Maréchal J-P, McCoy CMR, McField MD, Murdoch T, Nagelkerken I, Nemeth R, Nugues MM, Oxenford HA, Paredes G, Pitt JM, Polunin NVC, Portillo P, Reyes HB, Rodríguez-Martínez RE, Rodriguez-Ramirez A, Ruttenberg BI, Ruzicka R, Sandin S, Shulman MJ, Smith SR, Smith TB, Sommer B, Stallings C, Torres RE, Tunnell Jr JW, Vermeij MJA, Williams ID, Witman JD. 2014. Part I: overview and synthesis for the wider Caribbean. In: Jackson JBC, Donovan MK, Cramer KL, Lam V, eds. *Status and trends of Caribbean coral reefs: 1970–2012*. Gland: IUCN publications, 18–111.

Loya Y, Sakai K, Yamasato K, Nakano Y, Sambali H, Van Woesik R. 2001. Coral bleaching: the winners and the losers. *Ecology Letters* 4:122–131
DOI 10.1046/j.1461-0248.2001.00203.x.

Marshall PA, Baird AH. 2000. Bleaching of corals on the Great Barrier Reef: differential susceptibilities among taxa. *Coral Reefs* 19:155–163 DOI 10.1007/s003380000086.

McClanahan TR. 2004. The relationship between bleaching and mortality of common corals. *Marine Biology* 144(6):1239–1245 DOI 10.1007/s00227-003-1271-9.

McClanahan TR, Ateweberhan M, Darling ES, Graham NAJ, Muthiga NA. 2014. Biogeography and change among regional coral communities across the Western Indian Ocean. *PLOS ONE* 9:e93385 DOI 10.1371/journal.pone.0093385.

McClanahan TR, Ateweberhan M, Muhando C, Maina J, Mohammed SM. 2007a. Effects of climate and seawater temperature variation on coral bleaching and mortality. *Ecological Monographs* 77:503–525 DOI 10.1890/06-1182.1.

McClanahan TR, Ateweberhan M, Ruiz Sebastian C, Graham NAJ, Wilson SK, Bruggemann JH, Guillaume MMM. 2007b. Predictability of coral bleaching from synoptic satellite and in situ temperature observations. *Coral Reefs* 26:695–791
DOI 10.1007/s00338-006-0193-7.

McClanahan TR, Baird AH, Marshall PA, Toscano MA. 2004. Comparing bleaching and mortality responses of hard corals between southern Kenya and the Great Barrier Reef, Australia. *Marine Pollution Bulletin* 48:327–335
DOI 10.1016/j.marpolbul.2003.08.024.

McClanahan TR, Maina J, Moothien-Pillay R, Baker AC. 2005. Effects of geography, taxa, water flow, and temperature variation on coral bleaching intensity in Mauritius. *Marine Ecology Progress Series* 298:131–142 DOI 10.3354/meps298131.

McPhaden MJ, Zebiak SE, Glantz MH. 2004. ENSO as an integrating concept in earth science. *Science* 314:1740–1745 DOI 10.1126/science.1132588.

Nicet JB, Pennober G, Buckleen M, Wickel J, Bigot L, Chabanet P, Obura D. 2016. Intensité et impact du blanchissement corallien massif de 2016 sur les récifs coralliens français de l'océan Indien. Projet BECOMING 2016 Rapport MAREX, ESPACEDEV, ENTROPIE, UR, IRD, SEAS-OI, CORDIO, AAMP, PNMM, PNMG, TAAF, RNMR, DEAL Réunion, RNB, IFRECOR, UE, 1–87. Available at http://www.ifrecor-doc.fr/items/show/1744.
**Obura DO. 2001.** Can differential bleaching and mortality among coral species offer useful indicators for assessment and management of reefs under stress? *Bulletin of Marine Science* **69**:421–442.

**Obura DO. 2005.** Resilience and climate change: lessons from coral reefs and bleaching in the western Indian Ocean. *Estuarine Coastal and Shelf Science* **63**:353–372
DOI 10.1016/j.ecss.2004.11.010.

**Obura DO. 2012.** The diversity and biogeography of Western Indian Ocean reef-building corals. *PLOS ONE* **7**(9):e45013 DOI 10.1371/journal.pone.0045013.

**Obura DO. 2016.** An Indian Ocean centre of origin revisited: Palaeogene and Neogene influences defining a biogeographic realm. *Journal of Biogeography* **43**:229–242
DOI 10.1111/jbi.12656.

**Obura DO, Bandeira SO, Bodin N, Burgener V, Braulik G, Chassot E, Gullström M, Kochzius M, Nicoll M, Osuka K, Ralison HO, Richmond M, Samoilys MA, Scheren P, Ternon J-F. 2018.** The Northern Mozambique Channel. In: Sheppard Charles, ed. *World seas: an environmental valuation, volume II: the Indian Ocean to the Pacific*. Second Edition. New York: Elsevier.

**Obura DO, Grimsdith G. 2009.** Resilience assessment of coral reefs—assessment protocol for coral reefs, focusing on coral bleaching and thermal stress. In: *IUCN working group on climate change and coral reefs*. Gland: IUCN.

**Obura DO, Gudka M, Abdou Rabi F, Bacha Gian S, Bigot L, Bijoux J, Freed S, Maharavo J, Munbodhe V, Mwaura J, Porter S, Sola E, Wickel J, Yahya S, Ahamada S. 2017.** Coral reef status report for the Western Indian Ocean. Global Coral Reef Monitoring Network (GCRMN)/International Coral Reef Initiative (ICRI), 1–144. Available at https://www.icriforum.org/sites/default/files/COI%20REEF%20LR%20F2.compressed.pdf.

**Oliver T, Palumbi S. 2009.** Distributions of stress-resistant coral symbionts match environmental patterns at local but not regional scales. *Marine Ecology Progress Series* **378**:93–103 DOI 10.3354/meps07871.

**Ortiz JC, Del C. Gomez-Cabrera M, Hoegh-Guldberg O. 2009.** Effect of colony size and surrounding substrate on corals experiencing a mild bleaching event on Heron Island reef flat (southern Great Barrier Reef, Australia). *Coral Reefs* **28**:999–1003 DOI 10.1007/s00338-009-0546-0.

**Quod J, Dahalani Y, Bigot L, Nicet J-B, Ahamada S, Maharavo J. 2002.** Status of Coral Reefs at Réunion, Mayotte and Madagascar. In: Linden O, Souter D, Wilhelmsson D, Obura D, eds. Coral reef degradation in the India Ocean, Status reports 2002. CORDIO/SAREC Marine Science Program, 185–189.

**Rayner NA, Parker DE, Horton EB, Folland CK, Alexander LV, Rowell DP, Kent EC, Kaplan A. 2003.** Global analyses of sea surface temperature sea ice and night marine air temperature since the late nineteenth century. *Journal of Geophysical Research* **108**(D14):Article 4407 DOI 10.1029/2002JD002670.

**Reynolds RW, Rayner NA, Smith TM, Stokes DC, Wang W. 2002.** An improved in situ and satellite SST analysis for climate. *Journal of Climate* **15**:1609–1625 DOI 10.1175/1520-0442(2002)015<1609:AIISAS>2.0.CO;2.
**Saji NH, Goswami BN, Vinayachandran PN, Yamagata T. 1999.** A dipole mode in the tropical Indian Ocean. *Nature* **401**:360–363 DOI 10.1038/43854.

**Shenkar N, Fine M, Loya Y. 2005.** Size matters: bleaching dynamics of the coral *Oculina patagonica*. *Marine Ecology Progress Series* **294**:181–188 DOI 10.3354/meps294181.

**Sheppard CR. 2003.** Predicted recurrences of mass coral mortality in the Indian Ocean. *Nature* **425**:294–297 DOI 10.1038/nature01987.

**Souter D, Obura DO, Linden O. 2000.** Coral reef degradation in the India Ocean. Status reports 2000. CORDIO/SAREC Marine Science Program.

**Stat M, Loh WKW, LaJeunesse TC, Hoegh-Guldberg O, Car DA. 2009.** Stability of coral-endosymbiont associations during and after a thermal stress event in the southern Great Barrier Reef. *Coral Reefs* **28**:709–713 DOI 10.1007/s00338-009-0509-5.

**Thomassin BA. 2001.** Mayotte (SW Indian Ocean): recent demographical and economic rise induced by anthropisation and/or climatic variations on the littoral and on lagoonal ecosystems. *Journal de Recherche Océanographique* **26**:Article 60.

**UNEP-WCMC, WorldFish Centre, WRI, TNC. 2010.** Global distribution of warm-water coral reefs, compiled from multiple sources including the Millennium Coral Reef Mapping Project. Version 3.0. In: *Includes contributions from IMaRS-USF and IRD (2005), IMaRS-USF (2005) and Spalding et al. (2001)*. Cambridge: UN Environment World Conservation Monitoring Centre.

**Van Hooidonk R, Maynard J, Tamelander J, Gove J, Ahmadia G, Raymundo L, Williams G, Heron SF, Planes S. 2016.** Local-scale projections of coral reef futures and implications of the Paris agreement. *Scientific Reports* **6**:Article 39666 DOI 10.1038/srep39666.

**Van Woesik R, Sakai K, Ganase A, Loya Y. 2012.** Revisiting the winners and the losers a decade after coral bleaching. *Marine Ecology Progress Series* **434**:67–76 DOI 10.3354/meps09203.

**Wickel J, Thomassin BA. 2005.** Les récifs coralliens frangeants de l'île de Mayotte (Grande Terre): bilan de l'état de santé en 2004 et évolution depuis 1989.

**Wilkinson C. 2000.** *Status of coral reefs of the world: 2000*. Townsville: Australian Institute of Marine Science.

**Wilkinson C, Linden O, Cesar H, Hodgson G, Rubens J, Strong A. 1999.** Ecological and socioeconomic impacts of 1998 coral mortality in the Indian Ocean: an ENSO impact and a warning of future change? *Ambio* **28**:188–196.