Successive marine heatwaves cause disproportionate coral bleaching during a fast phase transition from El Niño to La Niña

Science of the Total Environment 715 (2020) 136951

Contents lists available at ScienceDirect

Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv

Successive marine heatwaves cause disproportionate coral bleaching during a fast phase transition from El Niño to La Niña Steven J. Dalton a,b,⁎, Andrew G. Carroll c,d, Eugenia Sampayo a, George Roff a, Peter L. Harrison c, Kristina Entwistle c, Zhi Huang d, Anya Salih e, Sandra L. Diamond f a

Australian Research Council Centre of Excellence for Coral Reef Studies, School of Biological Sciences, The University of Queensland, St Lucia, Queensland 4072, Australia National Marine Science Centre, Southern Cross University, PO Box 4321, Coffs Harbour, NSW 2450, Australia Marine Ecology Research Centre, Southern Cross University, PO Box 157, Lismore, NSW 2480, Australia d National Earth and Marine Observations Branch, Geoscience Australia, GPO Box 378, Canberra, ACT 2601, Australia e Western Sydney University, Confocal Bio-Imaging Facility, Hawkesbury Campus, PO Box 1797, Penrith, NSW 2751, Australia f Western Sydney University, School of Science and Health, Hawkesbury Campus, Box 1797, Penrith, NSW 2751, Australia b c

H I G H L I G H T S

G R A P H I C A L

A B S T R A C T

• Marine heatwaves have intensified recently at high-latitude coral reefs. • Lord Howe Island experienced unprecedented bleaching events in 2010 and 2011. • Warm oceans were associated with a fast phase transition from El Niño to La Niña. • Coral bleaching varied among taxa, with up to 99% affected at shallow sites. • Despite immediate mortality coral cover returned to pre-bleaching levels in 3 years.

a r t i c l e

i n f o

Article history: Received 22 October 2019 Received in revised form 24 January 2020 Accepted 24 January 2020 Available online 28 January 2020 Editor: Henner Hollert Keywords: Climate change Ocean warming Southern oscillation index High-latitude reefs Resilience Lord Howe Island

a b s t r a c t The frequency and intensity of marine heatwaves that result in coral bleaching events have increased over recent decades and led to catastrophic losses of reef-building corals in many regions. The high-latitude coral assemblages at Lord Howe Island, which is a UNESCO listed site is the world southernmost coral community, were exposed to successive thermal anomalies following a fast phase-transition of the record-breaking 2009 to 2010 warm pool El Niño in the Central Pacific to a strong La Niña event in late 2010. The coral community experienced severe and unprecedented consecutive bleaching in both 2010 and 2011. Coral health surveys completed between March 2010 and September 2012 quantified the response and recovery of approximately 43,700 coral colonies to these successive marine heatwaves. In March 2010, coral bleaching ranged from severe, with 99% of colonies bleached at some shallow lagoon sites, to mild at deeper reef slope sites, with only 17% of individuals affected. Significant immediate mortality from thermal stress was evident during the peak of the bleaching event. Overall, species in the genera Pocillopora, Stylophora, Seriatopora and Porites were the most affected, while minimal bleaching and mortality was recorded among members of other coral families (e.g. Acroporidae, Dendrophyllidae & Merulinidae). Surviving corals underwent a subsequent, but much less intense, thermal anomaly in 2011 that led to a disproportionate bleaching response among susceptible taxa. While this observation indicates that the capacity of thermally susceptible high-latitude corals to acclimatize to future ocean warming may be limited, particularly if bleaching events occur annually, our long-term survey data shows that coral cover at most sites recovered to pre-bleaching levels within three years in the absence of further thermal anomalies. Crown Copyright © 2020 Published by Elsevier B.V. All rights reserved.

⁎ Corresponding author at: National Marine Science Centre, Southern Cross University, PO Box 4321, Coffs Harbour, NSW 2450, Australia. E-mail address: [email protected] (S.J. Dalton).

https://doi.org/10.1016/j.scitotenv.2020.136951 0048-9697/Crown Copyright © 2020 Published by Elsevier B.V. All rights reserved.

2

S.J. Dalton et al. / Science of the Total Environment 715 (2020) 136951

1. Introduction Coral reefs throughout the world are increasingly affected by global disturbances associated with climate change, as well as the impacts of acute and chronic local stressors. Average seawater temperatures have risen at a rate of 0.07 °C per decade over the past century (EPA, 2016) with marine heatwaves tightly linked to significant and dramatic declines in coral cover and diversity of reef regions across the globe (Donner et al., 2017; Hughes et al., 2018a; Oliver et al., 2018; Wilkinson, 2008). Multiple and successive thermal stress events have resulted in over 20% global decline in coral cover during this century (Berkelmans et al., 2004; Heron et al., 2016; Hughes et al., 2017; Hughes et al., 2018b) with phase shifts from coral to algal dominated assemblages seen in heavily impacted areas (e.g. Cheal et al., 2010; Graham et al., 2015). The steady increase of ocean temperatures is causing many shallowwater, tropical, reef-building corals to live in excess of their upper thermal tolerance limits (Fitt et al., 2001). Thermal thresholds vary geographically and regionally following adaptation over hundreds to thousands of years to local long-standing yearly maximum and seasonal temperature trends (see Berkelmans and Willis, 1999; Pineda et al., 2013). Thermal anomalies above these long-term conditions lead to a breakdown of the symbiotic relationship of corals with single-celled dinoflagellates (Symbiodinium spp.), whereby the symbionts are lost from the coral tissue and cause it to pale and appear bleached (Glynn, 1996; Loya et al., 2001; McClanahan et al., 2004). Severe coral bleaching often results in coral colony death through starvation and/or increased susceptibility to secondary stressors (Boyett et al., 2007; Bruno et al., 2007; Leggat et al., 2019; Miller et al., 2006). The expanding geographic footprint of recurrent bleaching events has led to increased concerns regarding the resilience of coral reefs to repeated thermal anomalies (Hughes et al., 2017). These concerns are magnified by the apparently limited capacity of reef building corals to acclimatize or adapt to future climate threats, particularly given the rate at which thermal change is occurring (van Oppen et al., 2017 but see Matz et al., 2018 & Torda et al., 2017). During the last two decades, global coral bleaching events have intensified and are occurring at higher frequencies, giving coral communities little time for recovery, and resulting in widespread losses of coral cover and species diversity from tropical coral reef systems (Hughes et al., 2018a; Hughes et al., 2017). Recent evidence shows that subtropical, high-latitude coral communities may be equally susceptible to thermal stress events and are likely to undergo long-term changes in the assemblage structure (Kim et al., 2019). A diverse subset of coral species comprise the various subtropical coral communities found along the coasts of South Africa, Western Australia, eastern Australia, Japan and the eastern Pacific (Dalton and Roff, 2013; Denis et al., 2013; Harriott and Banks, 2002; McClanahan et al., 2014; Speed et al., 2013). These coral species are either subtropical specialists (often local endemics) or cosmopolitan coral species that exist at their range margins (Baird et al., 2017; Schmidt-Roach et al., 2013; Sommer et al., 2017). Geological records and present-day range shifts suggest that tropicalisation of highlatitude coral communities is likely to occur as ocean temperatures warm (e.g. Greenstein and Pandolfi, 2008; Mizerek et al., 2016; Yamano et al., 2011). However, the directionality and rate of change in coral assemblages is likely dependant on the sensitivity of local and established high-latitude communities to thermal anomalies (Tuckett et al., 2017; Wernberg et al., 2016). Corals inhabiting various diverse high-latitude marginal reef communities have shown to be susceptible to warming ocean waters (Abdo et al., 2012; Dalton and Carroll, 2011; Goyen et al., 2019; Harrison et al., 2011; Moore et al., 2012; Thomson et al., 2011). For example, extensive coral bleaching was observed on the various highlatitude communities along the Australian eastern and western seaboards during 2010, 2011 and 2016 and affected even the most southern reef community at Lord Howe Island (LHI; Harrison et al., 2011;

Hughes et al., 2017; Moore et al., 2012; Thomson et al., 2011). To date a limited number of studies have examined the susceptibility of coral assemblages exposed to successive annual thermal bleaching events (e.g. Carroll et al., 2017; Harrison et al., 2019; Hughes et al., 2019; Penin et al., 2013). These studies revealed genus specific variation in bleaching susceptibly and note that patterns in bleaching response were depth dependent, which were consistent between bleaching events. While some studies report no acclimatization between subsequent bleaching events (Carroll et al., 2017), others observed acclimatization where corals experienced reduced bleaching sensitivity at a subsequent bleaching event (Penin et al., 2013). Here we focus on the consecutive bleaching events that occurred in 2010 and 2011 at Lord Howe Island. These bleaching events were caused by successive thermal anomalies (Fig. 1; Suppl. A) associated with the 2009/10 El Niño, which was not only the highest reported Central Pacific sea surface temperature (SST) anomaly (Lee and McPhaden, 2010) but also went through the fastest phase transition to La Niña recorded to date (Kim et al., 2011). Although this fast phase transition allowed some respite from thermal stress on the tropical Great Barrier Reef, specific oceanographic conditions associated with this phase transition led to severe thermal stress along the west coast of Australia where unprecedented warming of the Leeuwin current caused widespread coral bleaching across 1200 km of tropical/temperate reefs (Feng et al., 2013; Moore et al., 2012). During December 2009, when the El Niño event was at its peak, ocean waters surrounding LHI also quickly rose above long-term thermal thresholds and exposed the local coral communities to 19 consecutive weeks of seawater temperatures above long-term thermal thresholds (Dalton and Carroll, 2011) between December 2009 and April 2010, which resulted in 99% coral bleaching at the most affected site within the lagoon (Harrison et al., 2011). Following this 2010 bleaching event, a second, much less intense, thermal anomaly occurred in 2011 along the subtropical and temperate eastern Australian coast regions that led to a second, consecutive, bleaching event at LHI. Interestingly, the intensity and duration of this second bleaching event was similar to warming that occurred in early 2009, prior to the significant heatwave of 2010, but did not lead to any bleaching among LHI coral communities. Here we aim to investigate the impacts of these successive annual thermal events leading to significant bleaching of corals at LHI. Specifically, we: i) contrast spatial and temporal patterns of bleaching during March 2010 and March 2011; ii) determine biological/environmental factors driving these bleaching patterns iii) ascertain differential bleaching susceptibility and mortality within coral genera; and iv) quantify long-term dynamics of coral communities at LHI following repeat thermal stress events. 2. Methods 2.1. Study site Lord Howe Island (LHI; 31.5°S, 159.0°E) lies approximately 600 km east of mainland northern New South Wales, Australia. This isolated island represents the remaining portion of a large eroded volcanic seamount and consists of a narrow strip of land extending 11 km north to south, and between 0.3 and 3 km in width. Benthic reef assemblages at LHI are unique and represent a bio-geographical zone containing tropical, subtropical and temperate marine species, leading to local high species diversity (Harriott et al., 1995; Veron and Done, 1979). While LHI is located N1000 km from the southernmost parts of the GBR, approximately 100 scleractinian coral species occur on fringing reefs and on deeper rocky substrates (Harriott et al., 1995; Veron and Done, 1979), and many of these species are at their southern-most limits of distribution (Harriott et al., 1995; Veron and Done, 1979). To determine the level of bleaching and recovery following successive bleaching events at LHI, the benthic community was evaluated at seven sites on the leeward/western side of the island: North Bay Wreck (NBW), Stephen's Hole (StH), Comet's Hole (CH, flat and slope

S.J. Dalton et al. / Science of the Total Environment 715 (2020) 136951

3

Fig. 1. The highest monthly temporal anomaly of satellite (MODIS) derived sea surface temperature (SST_A), for the warmest 3-month periods in 2009–10 and in 2011 that provides regional context to this study at Lord Howe Island. The monthly temporal anomaly was calculated against the long-term monthly mean between 2002 and 2016. The unit of the SST_A is °C; the positive (negative) values indicate positive (negative) SST anomalies.

habitats), Sylph's Hole (SpH, flat and slope habitats), Erscott's Hole (EH), Little Island (LI) and Erscott's Blind Passage (EBP) (Fig. 2). Seawater depth for the two sites located on the outer slope ranged between 7 and 10 m (LI and EBP, Fig. 2), while sites within the lagoon ranged between 2 and 5 m. 2.2. Environmental data: sea surface temperature and thermal stress To obtain a long-term historical baseline for the thermal conditions at LHI and compare an overall thermal profile of the consecutive bleaching events, we downloaded sea surface temperature (SST, daily average) and Southern Oscillation Index (SOI, monthly value) data (https://podaac.jpl.nasa.gov) from a 4 × 4 km grid on the leeward/western side of LHI spanning a 15-year period (Jun 2002–2017). The SST data was used to calculate two heat stress metrics that correspond with deviations from the long-term mean monthly maximum temperature (MMMSST - the mean of the warmest month of each year between 2002 and 2017 but excluding 2010, 2011 (Strong et al., 1997). We then calculated two metrics: (i) d N MMMSST, indicating the cumulative days over the long-term mean maximum temperature, whereby each day that the MMMSST was exceeded the days were summed, and (ii) Tacc N MMMSST, indicating the cumulative days over the long-term mean maximum temperature, whereby the total number of degrees were summed once MMMSST was exceeded. As opposed to the more commonly used threshold where 1 °C is added to the MMM, after which thermal anomaly is accumulated, we used the MMM as a direct bleaching threshold because research indicates that corals suffer significant heat stress as soon as the MMM is exceeded (Ainsworth et al.,

2016; Berkelmans, 2002; Grottoli et al., 2014; Kim et al., 2019; van Hooidonk and Huber, 2009). To investigate the site-specific responses and examine environmental predictors to explain differences in the bleaching response, we used in situ temperature data obtained from loggers. While the long-term SST data provides a good estimate of the thermal history on site, it lacks the spatial scale (4 × 4 km) to investigate site-based differences in bleaching severity among our study sites that are only separated by several hundred meters (Fig. 1). Not surprisingly, thermal stress indexes calculated from in situ data were recently shown to be a better predictor of heat stress responses in coral communities (Safaie et al., 2018). We obtained in situ data from underwater data loggers (Reefnet Sensus Ultra third generation) that were located on the reef complex at four of our seven study sites (Table 1) from March 2009 to May 2013. These loggers recorded sea temperature and pressure, every 10 min, with data uploaded onto the Australian Institute of Marine Science (AIMS) National Interactive Sea Surface Temperature Observing System annually. Raw temperature data were downloaded from the AIMS website (Australian Institute of Marine Science, 2014) and descriptive statistics were calculated. For analyses, we used logger data (LD) from sites in a similar reef environment for those sites where no logger data was available (see Table 1). For each logger site, the upper thermal threshold (mean monthly maximum; MMMLD) and the heat stress metrics, d N MMMLD and Tacc N MMMLD were calculated as described above and excluded the bleaching years 2010 and 2011. Because the logger data was only available for a few years, we compared the MMM value to the MODIS obtained 15-year dataset and both returned a very similar MMM (Table 1), indicating that the MMM from our logger derived data,

4

S.J. Dalton et al. / Science of the Total Environment 715 (2020) 136951

Fig. 2. Map of Lord Howe Island showing location of sites where coral bleaching and benthic community composition surveys were completed. Lagoon sites – Sylph's Hole (SpH) and Comet's Hole (CH); Reef Crest sites - North Bay Wreck (NBW), Stephen's Hole (StH) and Erscott's Hole (EH); and Reef Slope sites – Erscott's Blind Passage (EBP) and Little Island (LI). Insets for each site display the mean percent (±SE) of corals affected by bleaching (percent bleached colonies, red lines) and total coral cover (±SE; blue lines) recorded throughout the survey period (2010–2014). In situ temperature loggers were located adjacent to NBW, SpH and LI sites. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

albeit short, is representative of a long-term mean. In addition, to describe site specific thermal characteristics (not related to the thermal anomaly), we calculated the overall average temperature (TavgLD) and fluctuation (difference between daily maximum and minimum) in temperature (TflucLD) calculated from daily logger temperature data over the entire period (including 2010 and 2011: Table 1). 2.3. Coral health assessment and bleaching metrics The corals at each of the seven locations were monitored during March, May and September 2010, as well as in March 2011 and September 2012. Colony-level coral health assessments were completed in situ by randomly placing four 2 m × 20 m belt transects at each site. The 2-m

width of the belt was determined using a 1-m length of conduit attached to an underwater slate, and the 1 m region on either side of the tape was evaluated. Each coral colony along the transect was identified to species level in the field where possible and the bleaching response was visually assessed and scored into one of five categories: 1) healthy with no visible signs of bleaching (unbleached = UB), 2) moderately bleached (MB, 1–50% tissue paling), 3) severely bleached (SB, 51–100% tissue paling), 4) bleached with recent partial tissue mortality (PM) or 5) complete mortality (CM). Coral colouration was standardised between observers using coral category colour codes on the Coral Health Monitoring Chart (CHMC; Siebeck et al., 2006) and in water calibration dives were completed prior to all survey periods to eliminate observer biases. Colonies were only recorded as bleached if

Table 1 Environmental variables for the seven study sites at Lord Howe Island and mean values obtained from the long-term MODIS data set (2002–2017). In situ logger data was available from 3 locations, and these data were used as a proxy for sites within a similar habitat. Tavg = average temperature, Tfluc = average daily temperature fluctuation, MMM mean monthly maximum temperature, Days N MMM = number of days over the MMM, Tacc N MMM = accumulated number of degrees Celsius (°C) above the MMM. Site

Sylph's Hole (SyH) Comet's Hole North Bay Wreck (NBW) Stephen's Hole Erscott's Hole Little Island (LI) Erscott's Blind Passage MODIS

Logger

Yes No, use SyH Yes No, use NBW No, use NBW Yes No, use LI No, Satellite

Depth (m)

1–3 1–3 1–2 1–2 1–3 8–10 8–10 0

Tavg

Tfluc

MMM

Days N MMM

Tacc N MMM

2010

2011

2010

2011

21.11

1.60

24.64

91

54

106

39

21.93

1.38

24.52

115

56

124

33

21.52

0.45

24.48

89

46

79

24

21.55

n.a.

24.50

91

60

88

31

S.J. Dalton et al. / Science of the Total Environment 715 (2020) 136951

there was a distinct difference in the colour paling of individuals compared to normal pigmentation quantified during previous assessments using the CHMC (see Dalton and Godwin, 2005). The bleaching response was expressed using two different metrics. The first metric was irrespective of the severity of bleaching, where the proportion of colonies affected were divided by the total number of colonies present (% bleached colonies). This data was used to express the total percentage of affected colonies irrespective of their identity on a site level only. The second metric scaled the bleaching response based on severity of bleaching for each individual taxon. This scaled metric called “Bleaching Susceptibility Index” (BSI) was calculated for each coral taxa using a modification of the bleaching index cf. McClanahan (2004), using: BSI ¼ ð0  UB þ 1  MB þ 2  SB þ 3  PM þ 4  CMÞ=4 where bleaching proportional data from one of five health score categories (unbleached = UB, moderately bleached = MB, severely bleached = SB, bleached with recent tissue mortality = PM and complete mortality = CM) were recorded during surveys conducted in March 2010 and March 2011. This formula weighted each category to account for increased stress into a metric scaled from zero - indicating no bleaching, to one hundred - indicating all individuals bleached with complete mortality. Dominant taxa were grouped according to the genus level (Acropora, Isopora, Pocillopora, Porites, Seriatopora & Stylophora), and minor genera (absent at some sites) were grouped to the family level instead (Merulinidae) or ‘other’. Differences in percent colonies bleached (% bleached) among sites and time were analyzed using a linear model (‘stats’ package) in R Software (R Core Team, 2019). Differences in BSI among taxa and time were tested with a linear mixed effects model using the ‘lme4’ package in R (Bates et al., 2015) with sites as a random factor. To explore whether thermal stress (Tacc N MMMLD) predicted BSI and mortality among taxa, we used a linear mixed effects model with sites as a random factor. Conditional Pseudo-R-squared for linear mixed effect models were calculated using the ‘MuMIn’ package (Bartoń, 2019) and estimated marginal means (least-squares) were computed using the ‘emmeans’ package (Lenth, 2019).

5

3. Results 3.1. Variation in seawater temperatures Long-term satellite data for sea surface temperature (SST) showed that waters adjacent to Lord Howe Island (LHI) exceeded the longterm mean monthly maximum (MMMSST) in 2009, 2010 and 2011 (Fig. 3a, Table 1). While 2010 showed the highest anomaly both in the number of days (Fig. 3b) and the cumulative temperature (Fig. 3c) above the long-term mean maximum monthly (MMMSST), thermal excesses were very similar in 2009 and 2011 (if not slightly higher in 2009). The analyses of the in-situ logger data revealed that long-term and thermal stress parameters differed between sites. Average summer temperatures on the reef slope at Little Island were lower compared to the reef crest and lagoon sites by 0.34 and 0.39 °C, respectively (Table 1). Daily fluctuation in temperature was high at North Bay Wreck (1.38 °C) and Sylphs Hole (1.60 °C), while temperatures at Little Island were more stable (0.45 °C daily fluctuations). Average daily temperatures plotted by site highlighted that Sylph's Hole experienced colder temperatures for longer periods over winter (Fig. S1). The thermal stress metrics also highlighted that differences between sites were present. During the El Niño event that began in November 2009 and continued until June 2010 (Fig. 3a), average daily seawater temperature exceeded MMMLD at the North Bay Wreck, Sylph's Hole and Little Island sites for a total of 115, 91 and 89 days, with an accumulated temperature of 124, 106 and 79 °C respectively (Table 1). In 2011, during the period of La Niña influence that began in late August 2010 and eased in July 2011 (Fig. 3a), a second thermal anomaly of much lower severity was recorded and this was reflected with around a third less temperature accumulation and approximately half as many days above MMM compared to the 2010 anomaly. At North Bay Wreck, Sylph's Hole and Little Island temperature exceeded MMMLD on 56, 54 and 46 days with an accumulated temperature of 33, 39 and 24 °C (Table 1). Overall, the thermal history was more stable with lower summer temperatures and MMMLD and thermal stress was less severe at Little Island (reef slope) compared to the lagoon logger sites (North Bay Wreck and Sylph's Hole).

2.4. Decadal patterns of change in coral assemblages (2005–2014)

3.2. Coral bleaching response

The benthic communities at lagoon sites were evaluated in May 2005 and that dataset provided a baseline for subsequent assessments of bleaching and changes in benthic community composition through time (Dalton and Godwin, 2005). During March 2010, March 2011, September 2012 and November 2014, four 30 m transects were randomly positioned at each site and a Ricoh 10-megapixel camera (placed into an underwater housing with a 20-mm wide-angle lens) was used to photograph benthic community composition at each site. A SCUBA diver swam along each transect with the camera pointed downwards, approximately 50 cm above the substratum and recorded 30 consecutive images per transect. Digital images were subsequently analyzed using Coral Point Count with Excel extension software (CPCe; Kohler and Gill, 2006). Each transect image was uploaded into CPCe and ten random points were overlaid onto each consecutive image, resulting in 300 points per transect; thus, maintaining consistency of sampling effort between previous surveys completed in 2005. A permutation-based ANOVA (PERMANOVA; Anderson et al., 2008) (PRIMER software) was used to examine changes in community composition of corals between 2005 and 2014. Sites and years were considered fixed factors. Mean percent change in coral cover (2005–2014) within each genus was compared with bleaching susceptibility data (2010−2011) using a linear model (‘stats’ package) to determine the relative relationship between BSI recorded during March 2010 and long-term changes in coral cover at the genus level.

All the Lord Howe Island study sites displayed signs of significant bleaching stress during both the 2010 and 2011 thermal events. Interestingly, even though the coral communities were exposed to similar thermal excesses in 2009 as in 2011 (Fig. 3), no bleaching was seen in 2009. In our 2010 to 2012 surveys, the health status of 43,700 individual coral colonies was recorded (Table S1). In March and May 2010, extensive coral bleaching and associated immediate partial colony mortality was apparent across all seven study sites. Overall, the total percentage of corals that displayed signs of bleaching recorded during initial surveys in 2010 ranged from 98.6 ± 0.5 SE % of colonies bleached to only 17.4 ± 3.4% of colonies bleached (Fig. 2, insets). The number of affected bleached colonies (% bleached) differed significantly among sites (Fig. 2; Table S2). Overall, bleaching in 2010 was most severe at North Bay Wreck, Stephen's Hole, Sylph's Hole and Comet's Hole with between 80 and 99% bleached individuals, intermediate at Erscott's Hole and Erscott's Blind Passage with between 35 and 60% individuals affected and lowest at Little Island (b 20% bleached, Fig. 2). We found that between the successive thermal events of 2010 and 2011, the bleaching response was significantly related to site and year (March 2010 compared to March 2011; Table S2). For all sites, with the exception of Little Island, the mean percent bleached colonies were significantly higher in March 2010 compared to 2011 (66.9% versus 49.7% bleached colonies average across sites) (Fig. 2). Coral health surveys conducted at all sites in September 2012 revealed a significant decline in the percentage

6

S.J. Dalton et al. / Science of the Total Environment 715 (2020) 136951

Fig. 3. Satellite derived sea surface temperatures (SST) from nearshore waters around Lord Howe Island were used to examine long term trends in (a) seasonal variability and excesses of SST (MODIS, 5 km, red line) above the mean monthly maximum (MMMSST) and average monthly Southern Oscillation Index (SOI, black line). The yellow shaded area highlights the 2010 & 2011 bleaching events and the fast-phase transition between the 2009–2010 El Niño and 2010–2011 La Niña. Two thermal stress indicators were calculated from this dataset and show significant excesses above the MMMSST expressed as (b) total the number of days over MMMSST and (c) the total cumulative temperature over MMMSST (Tacc N MMMSST). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

of colonies bleached at all sites and during the 2014 surveys no visible bleaching was observed (Fig. 2). While the percent bleached colonies indicate how many individuals within the community are affected, it does not provide any information on the severity with which colonies are affected. To assess the severity of bleaching, the Bleaching Susceptibility Index (BSI) was used at a site level. The overall BSI was calculated using all scored colonies at each site regardless of their identity and we found a significant effect of site and year in terms of bleaching severity (March 2010 vs March 2011, Table S3). The BSI was significantly lower in March 2011 (BSI b 20) compared to March 2010 at four of the sites, Sylph's Hole (flat and slope habitats), Stephen's Hole, North Bay and Comet's Hole (flat habitat). There were no significant differences in the BSI between years at Comet's Hole slope, Erscott's Hole, Erscott's Blind Passage and Little Island. Little Island and Erscott's Blind Passage had the lowest overall bleaching severity (Fig. 4a, BSI ~ 10), followed by Comet's Hole slope, Erscott's Hole, North Bay Wreck and Stephen's Hole (Fig. 4a, BSI = 15–20) and the highest bleaching severity at Sylph's Hole (flat and slope habitats) and Comet's Hole flat (Fig. 4a, BSI N 20). To test for differences between the consecutive 2010 and 2011 events at the taxon level, we analyzed the taxa specific BSI for each site between years and found a significant interaction of time and taxon (Table S3). At the taxon level, the BSI during March 2010 (Fig. 4b) was higher than March 2011 for Stylophora, Pocillopora, Porites, Seriatopora and Isopora. There was no difference between years in the Acropora, Merulinidae and the ‘other’ category, all of which had overall very low levels of bleaching (BSI b 5). Porites exhibited the most substantial decline in susceptibility between events, with a threefold decline in BSI from 33.5 (±2.2 SE) in 2010 to 10.2 (±2.4 SE) in 2011 (Fig. 4b). Taxon specific bleaching responses were apparent from field observations in 2010, where strongly bleached Stylophora pistillata (Fig. 4c) and Pocillopora damicornis (Fig. 4d) co-existed adjacent to visually pigmented and apparently healthy Acropora colonies (Fig. 4c, d). 3.3. Bleaching associated immediate mortality Following the summer 2010 thermal event, coral cover declined at all sites (Fig. 2, blue lines). The largest decline was recorded at Comet's

Hole, where coral cover dropped from 39.0% (±1.4 SE) in March 2010 to 27.8% (±2.1 SE) in March 2011. At a colony level, immediate bleaching related mortality (partial & complete mortality combined; Table S1) ranged between 27 and 69% in the shallow lagoon coral community (Table S1). Many severely bleached colonies were observed with up to 95% tissue mortality, with live tissue only visible on shaded underside regions of colonies. At deeper reef slope sites, 6% of all colonies displayed recent partial or complete mortality. Further coral tissue loss occurred between May and September 2010 (Table S1), which was notably higher at the shallow Sylph's Hole flat lagoon site (64%) than at the other lagoon slope and reef crest sites. Comparing the two bleaching events, the degree of bleaching susceptibility and colony mortality (March 2010 vs March 2011) among sites was strongly related to the degree of thermal stress (Tacc N MMMLD) with an interactive effect of taxon (Table S5, Fig. 5). The genera Stylophora, Seriatopora, Pocillopora and Porites exhibited linear increases of BSI with increasing thermal stress (Fig. 5a), whereas other taxa exhibited an overall low BSI and no relationship with increasing thermal stress (b 10, not show in Fig. 5a). Porites exhibited the greatest slope and became rapidly more susceptible (increasing BSI) as thermal stress increased (Fig. 5a). Colony mortality followed a similar pattern with Stylophora, Seriatopora, Pocillopora experiencing increased immediate mortality with increasing thermal stress (Fig. 5b). While these three genera underwent immediate mortality even at the lowest thermal stress levels, Porites only experienced mortality at higher thermal stress levels (Fig. 5b). Mortality was overall low (b 5%) for all other taxa (Isopora, Acropora, Merulinidae and ‘other’) and showed no relationship with thermal stress (data not shown in Fig. 5b). A clear relationship was evident between BSI and colony mortality (March 2010 vs 2011) among taxa (Fig. 5c). 3.4. Long-term patterns of bleaching susceptibility and coral loss Generally, there was a positive correlation between bleaching susceptiblity and average percent coral cover loss within genera in the LHI lagoon (Fig. 6). Bleaching susceptibility index explained approximately 45% of the patterns of change in genera percent coral cover between 2005 and 2012 (Fig. 6). Coral taxa that were severely bleached

S.J. Dalton et al. / Science of the Total Environment 715 (2020) 136951

7

Fig. 4. a) Bleaching Susceptibility Index (BSI) calculated in 2010 and 2011 at Comet's Hole flat (CF), Comet's Hole slope (CS), Erscott's Blind Passage (EB), Erscott's Hole (EH), Little Island (LI), North Bay Wreck (NBW), Stephen's Hole (StH), Sylph's Hole flat (SF) and Sylph's Hole slope (SF) and b) taxa differences in bleaching between 2010 and 2011, c) and d) differential bleaching susceptibility showing Acropora are robust and Stylophora pistillata and Pocillopora damicornis are bleaching susceptible. * indicate significant differences in BSI at p b .05 within a site between consecutive bleaching years.

Fig. 5. Thermal stress and a) bleaching susceptibility index, and b) proportion of colonies exhibiting mortality (± 95% confidence intervals) c) relationship between average BSI (2010 and 2011) and mortality in 2010 and 2011 among taxa (±95% confidence intervals).

8

S.J. Dalton et al. / Science of the Total Environment 715 (2020) 136951

in both 2010 and 2011 suffered a significant loss in live coral cover, notably Seriatopora, Stylopora, Pocillopora and Montipora (Fig. 6). These taxa orientated towards the top right quadrat that indicates a high BSI and relatively high loss in coral cover (loss between 25 and 60%). In contrast, Porites displayed a high BSI but only a 12% decline in cover (bottom right quadrant; Fig. 6). Low bleaching susceptible Acropora (low BSI/high coral loss: Fig. 6) coral cover declining by 22% overall. Corals from the family Merulinidae (genera Platygyra and Astrea) displayed low bleaching susceptibility and increased in cover within the lagoon between 2005 and 2012 (Fig. 6).

3.5. Decadal patterns of change in coral assemblages (2005–2014) Long-term patterns of coral cover fluctuated between 2005 and 2014 (Fig. 7). Generally, coral cover declined marginally at four of the sites between 2005 and 2010 (North Bay Wreck, Comet's Hole flat, Sylph's Hole flat, Stephen's Hole) but slightly increased at Sylph's Hole slope or stayed stable at Erscott's Hole (Fig. 7). At all locations, a decrease in coral cover was seen following the 2010 bleaching (September 2010) but no further reduction in cover was recorded following the 2011 bleaching (Fig. 2, Fig. 7). Subsequent surveys of coral cover in 2014 revealed remarkable recovery to pre-bleaching levels of coral cover (± 5%) at all sites except Sylph's Hole slope, where coral cover increased by approximately 15% compared to pre-bleaching values after decreasing the most of all sites as a result of bleaching (Fig. 7). While long-term trends at Little Island and Erscott's Blind Passage are difficult to discern due to a lack of data, coral cover at North Bay Wreck and Stephen's Hole declined preceding the bleaching and overall Acropora cover significantly declined post bleaching for 4 of the sites (North Bay Wreck, Steven's Hole, Erscott's Hole, Comet's Hole, Fig. 7). The PERMANOVA analysis of changes in coral cover (Table 2) revealed a significant interaction between years and sites, indicating that the overall patterns of change varied spatially and temporally at LHI. Pairwise comparisons in species composition between 2005 and 2014 (Table 2) revealed a significant decrease in coral cover occurred only at North Bay Wreck and Stephen's Hole (Fig. 7), while the remaining sites (Comet's Hole, Sylph's Hole, Erscott's Hole) showed no overall change in coral assemblages (Table 2). Similarly, pairwise comparisons between 2010 and 2014 revealed significant differences only at three of the seven

-60

Low bleaching High mortality

High bleaching

Stylophora High mortality Seriatophora

-50

Pocillopora

% change coral cover

-40

Montipora

-30 Acropora -20 Cyphastrea Isopora

Porites

-10 Favites 0

Platygyra Astrea

10

High bleaching Low mortality

Low bleaching Low mortality

20 0

10

20

30

40

Bleaching susceptibility index Fig. 6. Average site bleaching susceptibility index (March 2010) and percent change in coral cover from pre (May 2005) and post (September 2012) successive bleaching events. Line indicates goodness-of-fit relationship based on a linear model.

sites (Table 2), indicating temporal stability in coral assemblages following the successive bleaching events. 4. Discussion High-latitude marginal reefs are threatened by the effects of global climate change with an increasing incidence of marine heatwaves and coral bleaching affecting subtropical and temperate regions over the last decade (Camp et al., 2018; Kim et al., 2019). The fast transition from a warm pool El Niño to La Niña event in 2010/2011 resulted in consecutive thermal anomalies in sea surface temperatures, which were particularly pronounced in the subtropics and led to extensive bleaching (up to 99%) of several dominant coral taxa at Lord Howe Island (LHI). Our results highlight that these high-latitude coral communities contain several locally dominant taxa (e.g. Porites, Pocillopora, Stylophora) that are highly sensitive to thermal excesses, suffering high mortality and declines in the coral cover (up to 62%). Surprisingly, despite the sensitivity of these communities to repeated punctuated thermal events, recovery was relatively fast and coral cover returned to pre-bleaching levels within three years. Thermal stress was more prolonged and of a higher intensity during the 2010 heatwave compared to the 2011 event (Fig. 3). The outcome of this was particularly evident at LHI lagoon sites, where bleaching was the most severe (Figs. 2 and 4a). The second 2011 heatwave saw recurrent bleaching of the same taxa as in 2010, regardless of the lower thermal stress during the second event. This suggests that bleaching susceptible coral colonies that survived after the first heatwave were either still sub-lethally physiologically challenged or displayed limited to no acclimatization capacity at such short (annual) temporal scales. This finding is the opposite pattern to recent back-to-back bleaching recorded in the Coral Sea, where the bleaching response was less severe in 2017 than in the preceding event in 2016, despite a higher exposure to heat stress (Harrison et al., 2019). Thermal stress during 2011 was of similar magnitude and duration as experienced in 2009 (Fig. 3), yet no visible bleaching was observed during 2009. The initial stress from the 2010 thermal anomaly may have contributed to the disproportionate bleaching response during the 2011 thermal event, resulting in additional stress of surviving colonies. Recent studies indicate that high-frequency temperature variability prior to acute thermal stress events can reduce the impact of coral bleaching (e.g. Ainsworth et al., 2016; Safaie et al., 2018). In addition, some corals may have the capacity to acclimatize to thermal stress as a result of long-term thermal history (Brown et al., 2002; Oliver and Palumbi, 2011), which enhance increased resistance to subsequent stress events (Hughes et al., 2019; Penin et al., 2013; Schoepf et al., 2015; Sully et al., 2019). Here we found that sites with the highest temperature fluctuations (e.g. Sylph's Hole, Table 1) exhibited the highest rates of bleaching (80–100%, Fig. 2), while sites with the lowest daily temperature fluctuations (e.g. Little Island, Table 1) exhibited the lowest rates of bleaching (b 20%, Fig. 2). It is likely that the ability to acclimatize to repeated stress events is not only highly species specific (Schoepf et al., 2015) but is also dependant on local thermal optima coupled with long-term and short term environmental fluctuations. The degree of thermal heat stress (Tacc N MMMLD) was correlated to both the severity of the coral bleaching response and subsequent mortality as well as decreases in coral cover at LHI (Fig. 5). The level of bleaching susceptibility at the site level was attributable, in part, to differences in species assemblages. This is similar to the recent findings of Kim et al. (2019) who found that assemblage-scale bleaching severity was disproportionately influenced by local differences in species abundance and taxon-specific bleaching responses, during a wide spread bleaching event of eastern Australian high-latitude coral communities. Sites dominated by Pocillopora damicornis, Stylophora pistillata and Porites heronensis (e.g. Sylph's Hole and Comet's Hole), consistently experienced a stronger bleaching response than sites where these species were less abundant. Similar to tropical coral reefs, Pocillopora and

S.J. Dalton et al. / Science of the Total Environment 715 (2020) 136951

9

Fig. 7. Long-term trajectories of coral cover among taxa and sites at Lord Howe Island for seven of the most dominant coral taxa as well as a group of less dominant taxa that were merged (‘Other’). Surveys completed in May 2005, March, May and September 2010, March 2011, September 2012 and November 2014. Following the 2010 bleaching event a decline in coral cover is seen at most sites but no further loss occurred following the 2011 bleaching.

Stylophora corals at LHI are highly susceptible to thermal stress (Marshall and Baird, 2000; McClanahan et al., 2004). In contrast, many tropical Porites species are usually thermally tolerant (Loya et al., 2001; Marshall and Baird, 2000), whereas at LHI they appear highly susceptible to bleaching. Again, this is consistent to the findings of Kim et al. (2019) and is likely due to the fact that the dominant Porites species at LHI is the subtropical specialist species Porites heronensis, which has a limited geographical distribution (Veron, 2000). A long-term adaptation to cooler seawater temperatures over evolutionary time scales therefore likely limits the capacity of P. heronensis to cope or rapidly acclimatize to elevated temperatures. Interestingly, bleaching severity of colonies in

2011 was much less severe than 2010 (Fig. 4) but we cannot discern whether this was due to the lower level of thermal stress or that surviving colonies were more tolerant. Despite high bleaching and subsequent mortality, rapid recovery following the 2010 and 2011 bleaching events suggests that P. heronensis may be robust to repeat disturbances. Our field-observations indicate that this rapid recovery appears to be driven from recovery from cryptic tissues within the skeletal matrix rather than new skeletal growth or new recruits into the community. Similar responses have been observed in tropical massive Porites spp. and this so-called ‘phoenix effect’ can drive rapid post-bleaching recovery of coral cover (Roff et al., 2014).

Table 2 Results of PERMANOVA for coral assemblages from seven sites survey before, during and after successive bleaching events at Lord Howe Island. CH: Comet's Hole, StH: Stephen's Hole, SH: Sylph's Hole (flat and slope habitats). NBW: North Bay Wreck, EH: Erscott's Hole, EBP: Erscott's Blind Passage, LI: Little Island. ≠ and years bolded indicate significant difference within site between years. Coral assemblage PERMANOVA Source

df

Year Site Ye*Si Residual Total

SS

4 7 26 114 151

1.1 1.0 4.3 7.7 2.4

MS ∗ ∗ ∗ ∗ ∗

4

2.8 1.5 1.6 6.8

10 105 104 104 105

∗ ∗ ∗ ∗

3

10 104 103 102

F

P

4.19 21.96 2.41

0.001 0.001 0.001

Pairwise comparisons CH

StH

SH (flat)

SH (slope)

NBW

EH

EBP

LI

2005 ≠ 2010 2005 = 2014 2010 ≠ 2014

2005 ≠ 2010 2005 ≠ 2014 2010 = 2014

2005 = 2010 2005 = 2014 2010 = 2014

2005 = 2010 2005 = 2014 2010 = 2014

2005 ≠ 2010 2005 ≠ 2014 2010 = 2014

2005 = 2010 2005 = 2014 2010 = 2014

No data No data 2010 = 2014

No data No data 2010 ≠ 2014

10

S.J. Dalton et al. / Science of the Total Environment 715 (2020) 136951

Consistent with previous studies (Guest et al., 2012; Loya et al., 2001) coral taxa that were bleaching susceptible exhibited greater loss of coral cover at LHI. Branching Pocillopora spp. that exhibited severe bleaching responses declined significantly in coral cover following repeated thermal bleaching whereas massive, encrusting and column forming species with either high (e.g. Porites spp) or intermediate bleaching responses (e.g. Isopora cuneata) displayed only moderate losses. Loya et al. (2001) reported a similar structural shift following the 1998 mass-bleaching (at Okinawa, Japan) and attributed this to a significant increase in the cover of massive and encrusting poritid and merulinid (“winners”) species and a loss of branching and fast growing acroporid and pocilloporid (“losers”) species. These results are consistent with the hypothesis of Gates and Edmunds (1999) that corals with low growth rates and low metabolic rates, such as massive species, acclimatize more effectively than those with high growth rates and high metabolic rates, characteristic of branching species. Those sites dominated by Acropora spp. in our study (North Bay Wreck and Erscott's Hole) displayed relatively lower levels of bleaching compared to sites with low Acropora cover (Fig. 4c, d). These results contrast with recent mass-bleaching events in Australia from the Great Barrier Reef and Western Australia where Acropora species are highly susceptible to thermal stress compared with other coral genera (Depczynski et al., 2013; Hughes et al., 2018a; Hughes et al., 2017; Marshall and Baird, 2000; McClanahan et al., 2004). High bleaching susceptibility in Acropora and subsequent declines in cover have also been recorded from the Red Sea (Furby et al., 2013), the Great Barrier Reef (Baird and Marshall, 2002), and French Polynesia, while less vulnerable taxa such as Porites exhibited lower rates of bleaching and losses in cover (Carroll et al., 2017; Depczynski et al., 2013; Hoegh-Guldberg and Salvat, 1995; McClanahan et al., 2004; Penin et al., 2007; Pratchett et al., 2013). However, our findings are consistent with those of Kim et al. (2019), who found that differences in bleaching susceptibility between similar genera from tropical and subtropical regions are likely a characteristic of the particular species that inhibit these high-latitude coral communities, which are living at their latitudinal limits of thermal minima (Veron, 2000). Despite moderate to high levels of partial mortality at LHI following the 2010 and 2011 bleaching events (Table S2), coral cover recovered to pre-bleaching levels within three years post bleaching events at four of the seven sites (Fig. 7). Such recovery is surprisingly rapid compared with other mass bleaching events in the Pacific, where recovery has taken between 7 and 10 years (Gilmour et al., 2013), or where impacted reefs have failed to recover at all (e.g. Baker et al., 2008). At LHI, substantial long-term declines in coral cover at some sites (N 50%) between 2005 and 2014 were driven by long-term declines in the cover of Acropora species, despite only mild levels of bleaching for this bleaching in the 2010 and 2011 events. Long-term losses of Acropora cover at some sites may be attributed to subaerial exposure during extremely low tides that coincided with clear hot days, resulting in mortality in the upper sections of coral colonies followed by rapid colonisation of turfing algae. In contrast to resilient corals such as P. heronensis that exhibited a remarkable regenerative capacity, Acropora species appear to be limited in regenerative capacity. Field observations following the bleaching event at Stephen's Hole and Erscott's Hole indicated that surviving bleached plating Acropora species were overgrown and outcompeted by colonial ascidians and the algae Caulerpa taxifolia. These organisms initiated at bleached coral margins and expanded across regions of apparently healthy tissue, resulting in whole colony mortality. Similar patterns of colonisation and expansion of substrates following bleaching events has been observed on the Great Barrier Reef (Tebbett et al., 2019), and has been hypothesised to result from increased localised nutrient availability from coral tissue loss, and reduced predation due to a decline in the abundance of planktivorous fishes that prey heavily on dispersing ascidian larvae (Tebbett et al., 2019). The recovery of coral reefs following severe disturbances is largely dependent on larval supply and successful recruitment (e.g.

Gilmour et al., 2013). High-latitude reefs such as LHI exist at the edges of coral ranges (Sommer et al., 2017), and are therefore likely to be slower to recover from severe disturbances due to their geographic and genetic isolation from coral populations on other reefs (Ayre and Hughes, 2004; Noreen et al., 2009, 2013, 2015) that could potentially supply allochthonous coral larvae for recruitment (Harrison, 2008; Jones et al., 2009). Coral larval settlement patterns at LHI exhibit strong seasonal and spatial variation (Cameron and Harrison, 2016), with dominance of brooding corals evident at some sites (Cameron and Harrison, 2016; Harriott, 1992). Densities of juvenile coral recruits on shallow LHI reefs are 5–200 times lower than on tropical reefs (Hoey et al., 2011), which suggests that post-settlement mortality of recruits is comparatively high (Cameron and Harrison, 2016). The rising temperature of the world's oceans and increasing incidence of marine heatwaves have become a major threat to coral reefs globally as the severity and frequency of mass coral bleaching and mortality events increase (Eakin et al., 2019; Fordyce et al., 2019; Heron et al., 2016; Hughes et al., 2017; Leggat et al., 2019). Satellite observations suggest that the intensity of El Niño events in the central equatorial Pacific (CP) has almost doubled in the past three decades, with the strongest warming occurring in 2009–10 (Lee and McPhaden, 2010). This is related to the increasing intensity as well as occurrence frequency of the CP El Niño events since the 1990s (Lee and McPhaden, 2010). If the recent Indian Ocean warming trend continues as predicted (Luo et al., 2012) and El Niño events continue to intensify in response to global warming, fast phase transition of warm pool El Niño like the 2009/10 event may become more frequent in the future (although see discussion in Kim et al., 2011). Successive coral bleaching events in 2010 and 2011 significantly impacted the shallow coral communities of LHI, resulting initially in losses of coral cover of bleaching sensitive taxa. Despite high levels of bleaching and mortality, recovery was rapid, and coral cover returned to pre-bleaching levels within three years following the second bleaching event. While such recovery indicates resilience in coral assemblages at LHI to recurrent bleaching events, increased frequency of bleaching events and reduced return time between successive events may result in declines in diversity driven by the loss of dominant bleaching sensitive genera such as Pocillopora, Stylophora and Seriatopora. This may ultimately result in coral communities becoming dominated by macroalgae and fewer more resistant coral species. Immediate national and global action is necessary to reduce future warming that leads to extreme thermal events if we are to maintain the unique biodiversity of this unique, isolated and pristine World Heritage site. Supplementary data to this article can be found online at https://doi. org/10.1016/j.scitotenv.2020.136951.

CRediT authorship contribution statement Steven J. Dalton: Conceptualization, Methodology, Investigation, Formal analysis, Writing - original draft, Writing - review & editing, Visualization, Funding acquisition. Andrew G. Carroll: Conceptualization, Methodology, Investigation, Formal analysis, Writing - original draft, Writing - review & editing, Visualization, Funding acquisition. Eugenia Sampayo: Conceptualization, Formal analysis, Writing - original draft, Writing - review & editing, Visualization. George Roff: Conceptualization, Formal analysis, Writing - original draft, Writing - review & editing, Visualization. Peter L. Harrison: Conceptualization, Methodology, Investigation, Writing - review & editing, Funding acquisition. Kristina Entwistle: Investigation, Formal analysis. Zhi Huang: Formal analysis, Writing - review & editing, Visualization. Anya Salih: Investigation, Writing - review & editing. Sandra L. Diamond: Investigation, Writing - review & editing.

S.J. Dalton et al. / Science of the Total Environment 715 (2020) 136951

Acknowledgements This project was primarily funded by a research grant from the NSW Northern Rivers Catchment Management Authority. Lord Howe Island Marine Park provided financial support and in-kind contribution including field support and access to boats while on the island, enabling the collection of data. We sincerely thank Ian Kerr, Sallyann Gudge and Tasman Douglas (Marine Park officers) who assisted with the fieldwork on the island. The NSW Marine Parks Authority, Marine Ecology Research Centre and National Marine Science Centre – Southern Cross University, provided financial and in-kind support. We thank all LHI marine operators for their support and engagement during this project, particularly Brian and Peter Busteed. Ray Berkelmans (Australian Institute of Marine Science) provided advice and access to in situ seawater temperature data. We thank Neil Caldwell, Silvio Mezzomo and Martine Bilen (Geoscience Australia) for their assistance with visualisations and graphics. AC & ZH publish with the permission of the Chief Executive Officer of Geoscience Australia. All authors confirm no conflict of interest. Finally, we thank Science of the Total Environment reviewers for providing comments that have improved the manuscript. Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. References Bartoń, K., 2019. MuMIn: Multi-Model Inference. R Package Version 1.43.6. Abdo, D.A., Bellchambers, L.M., Evans, S.N., 2012. Turning up the heat: increasing temperature and coral bleaching at the high latitude coral reefs of the Houtman Abrolhos Islands. PLoS One 7, e43878. Ainsworth, T.D., Heron, S.F., Ortiz, J.C., Mumby, P.J., Grech, A., Ogawa, D., et al., 2016. Climate change disables coral bleaching protection on the Great Barrier Reef. Science 352, 338. Anderson, M.J., Gorley, R.N., Clarke, K.R., 2008. PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods. PRIMER-E, Plymouth, UK. Australian Institute of Marine Science, 2014. AIMS Data Centre. 2008. Australian Institute of Marine Science, Townsville, Queensland. Ayre, D.J., Hughes, T.P., 2004. Climate change, genotypic diversity and gene flow in reefbuilding corals. Ecol. Lett. 7, 273–278. Baird, A.H., Marshall, P.A., 2002. Mortality, growth and reproduction in scleractinian corals following bleaching on the Great Barrier Reef. Mar. Ecol. Prog. Ser. 237, 133–141. Baird, A.H., Hoogenboom, M.O., Huang, D., 2017. Cyphastrea salae, a new species of hard coral from Lord Howe Island, Australia (Scleractinia, Merulinidae). ZooKeys 49–66. Baker, A.C., Glynn, P.W., Riegl, B., 2008. Climate change and coral reef bleaching: an ecological assessment of long-term impacts, recovery trends and future outlook. Estuar. Coast. Shelf Sci. 80, 435–471. Bates, D., Mächler, M., Bolker, B., Walker, S., 2015. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 48. Berkelmans, R., 2002. Time-integrated thermal bleaching thresholds of reefs and their variation on the Great Barrier Reef. Mar. Ecol. Prog. Ser. 229, 73–82. Berkelmans, R., Willis, B.L., 1999. Seasonal and local spatial patterns in the upper thermal limits of corals on the inshore central Great Barrier Reef. Coral Reefs 18, 219–228. Berkelmans, R., De’ath, G., Kininmonth, S., Skirving, W.J., 2004. A comparison of the 1998 and 2002 coral bleaching events on the Great Barrier Reef: spatial correlation, patterns, and predictions. Coral Reefs 23, 74–83. Boyett, H.V., Bourne, D.G., Willis, B.L., 2007. Elevated temperature and light enhance progression and spread of black band disease on staghorn corals of the Great Barrier Reef. Mar. Biol. 151, 1711–1720. Brown, B., Dunne, R., Goodson, M., Douglas, A., 2002. Experience shapes the susceptibility of a reef coral to bleaching. Coral Reefs 21, 119–126. Bruno, J.F., Selig, E.R., Casey, K.S., Page, C.A., Willis, B.L., Harvell, C.D., et al., 2007. Thermal stress and coral cover as drivers of coral disease outbreaks. PLoS Biol. 5, 1220–1227. Cameron, K.A., Harrison, P.L., 2016. Patterns of scleractinian coral recruitment at Lord Howe Island, an isolated subtropical reef off eastern Australia. Coral Reefs 35, 555–564. Camp, E.F., Schoepf, V., Mumby, P.J., Hardtke, L.A., Rodolfo-Metalpa, R., Smith, D.J., et al., 2018. The future of coral reefs subject to rapid climate change: lessons from natural extreme environments. Front. Mar. Sci. 5. Carroll, A.G., Harrison, P.L., Adjeroud, M., 2017. Susceptibility of coral assemblages to successive bleaching events at Moorea, French Polynesia. Mar. Freshw. Res. 68, 760–771. Cheal, A.J., MacNeil, M.A., Cripps, E., Emslie, M.J., Jonker, M., Schaffelke, B., et al., 2010. Coral–macroalgal phase shifts or reef resilience: links with diversity and functional roles of herbivorous fishes on the Great Barrier Reef. Coral Reefs 29, 1005–1015.

11

Dalton, S.J., Carroll, A.G., 2011. Monitoring coral health to determine coral bleaching response at high latitude eastern Australian reefs: an applied model for a changing climate. Diversity 3, 592–610. Dalton, S.J., Godwin, S., 2005. Preliminary Evaluation of Coral Stressors (Disease, Bleaching and Predation) at Lord Howe Island Marine Park. University of New England, National Marine Science Centre, Coffs Harbour NSW. Dalton, S.J., Roff, G., 2013. Spatial and temporal patterns of eastern Australia subtropical coral communities. PLoS One 8, e75873. Denis, V., Mezaki, T., Tanaka, K., Kuo, C.-Y., De Palmas, S., Keshavmurthy, S., et al., 2013. Coverage, diversity, and functionality of a high-latitude coral community (Tatsukushi, Shikoku Island, Japan). PLoS One 8, e54330. Depczynski, M., Gilmour, J.P., Ridgway, T., Barnes, H., Heyward, A.J., Holmes, T.H., et al., 2013. Bleaching, coral mortality and subsequent survivorship on a West Australian fringing reef. Coral Reefs 32, 233–238. Donner, S.D., Rickbeil, G.J.M., Heron, S.F., 2017. A new, high-resolution global mass coral bleaching database. PLoS One 12, e0175490. Eakin, C., Sweatman, H., Brainard, R., 2019. The 2014–2017 global-scale coral bleaching event: insights and impacts. Coral Reefs 38, 539–545. EPA US, 2016. Climate Change Indicators in the United States, 2016. Fourth edition. . Feng, M., McPhaden, M.J., Xie, S.-P., Hafner, J., 2013. La Niña forces unprecedented Leeuwin Current warming in 2011. Sci. Rep. 3, 1277. Fitt, W.K., Brown, B.E., Warner, M.E., Dunne, R.P., 2001. Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals. Coral Reefs 20, 51–65. Fordyce, A.J., Ainsworth, T.D., Heron, S.F., Leggat, W., 2019. Marine heatwave hotspots in coral reef environments: physical drivers, ecophysiological outcomes, and impact upon structural complexity. Front. Mar. Sci. 6. Furby, K.A., Bouwmeester, J., Berumen, M.L., 2013. Susceptibility of central Red Sea corals during a major bleaching event. Coral Reefs 32, 505–513. Gates, R.D., Edmunds, P.J., 1999. The physiological mechanism of accilimatisation in tropical reef corals. Am. Zool. 39, 30–43. Gilmour, J.P., Smith, L.D., Heyward, A.J., Baird, A.H., Pratchett, M.S., 2013. Recovery of an isolated coral reef system following severe disturbance. Science 340, 69. Glynn, P.W., 1996. Coral reef bleaching: facts, hypotheses and implications. Glob. Chang. Biol. 2, 495–509. Goyen, S., Camp, E.F., Fujise, L., Lloyd, A., Nitschke, M.R., LaJeunensse, T., et al., 2019. Mass coral bleaching of P. versipora in Sydney Harbour driven by the 2015–2016 heatwave. Coral Reefs 38, 815–830. Graham, N.A.J., Jennings, S., MacNeil, M.A., Mouillot, D., Wilson, S.K., 2015. Predicting climate-driven regime shifts versus rebound potential in coral reefs. Nature 518, 94. Greenstein, B.J., Pandolfi, J.M., 2008. Escaping the heat: range shifts of reef coral taxa in coastal Western Australia. Glob. Chang. Biol. 14, 513–528. Grottoli, A.G., Warner, M.E., Levas, S.J., Aschaffenburg, M.D., Schoepf, V., McGinley, M., et al., 2014. The cumulative impact of annual coral bleaching can turn some coral species winners into losers. Glob. Chang. Biol. 20, 3823–3833. Guest, J.R., Baird, A.H., Maynard, J.A., Muttaqin, E., Edwards, A.J., Campbell, S.J., et al., 2012. Contrasting patterns of coral bleaching susceptibility in 2010 suggest an adaptive response to thermal stress. PLoS One 7, e33353. Harriott, V.J., 1992. Recruitment patterns of scleractinian corals in an isolated sub-tropical reef system. Coral Reefs 11, 215–219. Harriott, V.J., Banks, S.A., 2002. Latitudinal variation in coral communities in eastern Australia: a quantitative biophysical model of factors regulating coral reefs. Coral Reefs 21, 83–94. Harriott, V.J., Harrison, P.L., Banks, S.A., 1995. The coral communities of Lord Howe Island. Mar. Freshw. Res. 46, 457–465. Harrison, P.L., 2008. Coral spawn slicks at Lord Howe Island, Tasman Sea, Australia; the world’s most southerly coral reef. Coral Reefs 27, 35. Harrison, H.B., Álvarez-Noriega, M., Baird, A.H., Heron, S.F., MacDonald, C., Hughes, T.P., 2019. Back-to-back coral bleaching events on isolated atolls in the Coral Sea. Coral Reefs 38, 713–719. Harrison, P.L., Dalton, S.J., Carroll, A.G., 2011. Extensive coral bleaching on the world’s southernmost coral reef at Lord Howe Island, Australia. Coral Reefs 30, 775. Heron, S.F., Maynard, J.A., van Hooidonk, R., Eakin, C.M., 2016. Warming trends and bleaching stress of the world’s coral reefs 1985–2012. Sci. Rep. 6, 38402. Hoegh-Guldberg, O., Salvat, B., 1995. Periodic mass-bleaching and elevated sea temperatures: bleaching of outer reef slope communities in Moorea, French Polynesia. Mar. Ecol. Prog. Ser. 121, 181–190. Hoey, A.S., Pratchett, M.S., Cvitanovic, C., 2011. High macroalgal cover and low coral recruitment undermines the potential resilience of the world’s southernmost coral reef assemblages. PLoS One 6, e25824. van Hooidonk, R., Huber, M., 2009. Quantifying the quality of coral bleaching predictions. Coral Reefs 28, 579–587. Hughes, T.P., Kerry, J.T., Álvarez-Noriega, M., Álvarez-Romero, J.G., Anderson, K.D., Baird, A.H., et al., 2017. Global warming and recurrent mass bleaching of corals. Nature 543, 373–377. Hughes, T.P., Anderson, K.D., Connolly, S.R., Heron, S.F., Kerry, J.T., Lough, J.M., et al., 2018a. Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359, 80. Hughes, T.P., Kerry, J.T., Baird, A.H., Connolly, S.R., Dietzel, A., Eakin, C.M., et al., 2018b. Global warming transforms coral reef assemblages. Nature 556, 492–496. Hughes, T.P., Kerry, J.T., Connolly, S.R., Baird, A.H., Eakin, C.M., Heron, S.F., et al., 2019. Ecological memory modifies the cumulative impact of recurrent climate extremes. Nat. Clim. Chang. 9, 40–43. Jones, G.P., Almany, G.R., Russ, G.R., Sale, P.F., Steneck, R.S., van Oppen, M.J.H., et al., 2009. Larval retention and connectivity among populations of corals and reef fishes: history, advances and challenges. Coral Reefs 28, 307–325.

12

S.J. Dalton et al. / Science of the Total Environment 715 (2020) 136951

Kim, W., Yeh, S., Kim, J., Kug, J., Kwon, M., 2011. The unique 2009–2010 El Niño event: a fast phase transition of warm pool El Niño to La Niña. Geophys. Res. Lett. 38, L15809. Kim, S.W., Sampayo, E.M., Sommer, B., Sims, C.A., Gómez-Cabrera, M., Dalton, S.J., et al., 2019. Refugia under threat: mass bleaching of coral assemblages in high-latitude eastern Australia. Glob. Chang. Biol. 25, 3918–3931. Kohler, K.E., Gill, S.M., 2006. Coral point count with excel extension (CPCe): a visual basic program for the determination of coral and substrate coverage using random point count methodology. Comput. Geosci. 32, 1259–1269. Lee, T., McPhaden, M.J., 2010. Increasing intensity of El Niño in the central-equatorial Pacific. Geophys. Res. Lett. 37, L14603. Leggat, W.P., Camp, E.F., Suggett, D.J., Heron, S.F., Fordyce, A.J., Gardner, S., et al., 2019. Rapid coral decay is associated with marine heatwave mortality events on reefs. Curr. Biol. 29, 2723–2730.e4. Lenth, R., 2019. emmeans: Estimated Marginal Means, aka Least-Squares Means. R package version 1.3.3. . Loya, Y., Sakai, K., Yamazato, K., Nakano, Y., Sambali, H., van Woesik, R., 2001. Coral bleaching; the winners and the losers. Ecol. Lett. 4, 122–131. Luo, J., Sasaki, W., Masumoto, Y., 2012. Indian Ocean warming modulates Pacific climate change. Proc. Natl. Acad. Sci. U. S. A. 109, 18701–18706. Marshall, P.A., Baird, A.H., 2000. Bleaching of corals on the Great Barrier Reef: differential susceptibilities among taxa. Coral Reefs 19, 155–163. Matz, M.V., Treml, E.A., Aglyamova, G.V., Bay, L.K., 2018. Potential and limits for rapid genetic adaptation to warming in a Great Barrier Reef coral. PLoS Genet. 14, e1007220. McClanahan, T.R., 2004. The relationship between bleaching and mortality of common corals. Mar. Biol. 144, 1239–1245. McClanahan, T.R., Baird, A.H., Marshall, P.A., Toscano, M.A., 2004. Comparing bleaching and mortality responses of hard corals between southern Kenya and the Great Barrier Reef, Australia. Mar. Pollut. Bull. 48, 327–335. McClanahan, T.R., Ateweberhan, M., Darling, E.S., Graham, N.A.J., Muthiga, N.A., 2014. Biogeography and change among regional coral communities across the Western Indian Ocean. PLoS One 9, e93385. Miller, J., Waara, R., Muller, E., Rogers, C., 2006. Coral bleaching and disease combine to cause extensive mortality on reefs in US Virgin Islands. Coral Reefs 25, 418. Mizerek, T.L., Baird, A.H., Beaumont, L.J., Madin, J.S., 2016. Environmental tolerance governs the presence of reef corals at latitudes beyond reef growth. Glob. Ecol. Biogeogr. 25, 979–987. Moore, J., Bellchambers, L., Depczynski, M., Evans, R., Evans, S., Field, S., et al., 2012. Unprecedented mass bleaching and loss of coral across 12 degrees of latitude in Western Australia in 2010. PLoS One 7, e51807. Noreen, A.M.E., Harrison, P.L., Van Oppen, M.J.H., 2009. Genetic diversity and connectivity in a brooding reef coral at the limit of its distribution. Proceeding of the Royal Society B 276, 3927–3935. Noreen, A.M.E., van Oppen, M.J.H., Harrison, P.L., 2013. Genetic diversity and differentiation among high-latitude broadcast-spawning coral populations disjunct from the core range. Mar. Ecol. Prog. Ser. 491, 101–109. Noreen, A.M.E., Schmidt-Roach, S., Harrison, P.L., van Oppen, M.J.H., 2015. Diverse associations among coral host haplotypes and algal endosymbionts may drive adaptation at geographically peripheral and ecologically marginal locations. J. Biogeogr. 42, 1639–1650. Oliver, T.A., Palumbi, S.R., 2011. Do fluctuating temperature environments elevate coral thermal tolerance? Coral Reefs 30, 429–440. Oliver, E.C.J., Donat, M.G., Burrows, M.T., Moore, P.J., Smale, D.A., Alexander, L.V., et al., 2018. Longer and more frequent marine heatwaves over the past century. Nat. Commun. 9, 1324. van Oppen, M.J.H., Gates, R.D., Blackall, L.L., Cantin, N., Chakravarti, L.J., Chan, W.Y., et al., 2017. Shifting paradigms in restoration of the world’s coral reefs. Glob. Chang. Biol. 23, 3437–3448. Penin, L., Adjeroud, M., Schrimm, M., Lenihan, H., 2007. High spatial variability in coral bleaching around Moorea, French Polynesia: patterns across reefs, locations, and water depths. Comptes Rendus Biologies 330, 171–181.

Penin, L., Vidal-Dupiol, J., Adjeroud, M., 2013. Response of coral assemblages to thermal stress: are bleaching intensity and spatial patterns consistent between events? Environ. Monit. Assess. 185, 5031–5042. Pineda, J., Starczak, V., Tarrant, A., Blythe, J., Davis, K., Farrar, T., et al., 2013. Two spatial scales in a bleaching event: corals from the mildest and the most extreme thermal environments escape mortality. Limnol. Oceanogr. 58, 1531–1545. Pratchett, M.S., McCowan, D., Maynard, J.A., Heron, S.F., 2013. Changes in bleaching susceptibility among corals subject to ocean warming and recurrent bleaching in Moorea, French Polynesia. PLoS One 8, e70443. R Core Team, 2019. A Language and Environment for Statistical Computing. R: Foundation for Statistical Computing, Vienna, Austria Available at. https://www.r-project.org/. Roff, G., Bejarano, S., Bozec, Y.-M., Nugues, M., Steneck, R.S., Mumby, P.J., 2014. Porites and the Phoenix effect: unprecedented recovery after a mass coral bleaching event at Rangiroa Atoll, French Polynesia. Mar. Biol. 161, 1385–1393. Safaie, A., Silbiger, N.J., McClanahan, T.R., Pawlak, G., Barshis, D.J., Hench, J.L., et al., 2018. High frequency temperature variability reduces the risk of coral bleaching. Nat. Commun. 9 (1671), 1–12. Schmidt-Roach, S., Miller, K., Andreakis, N., 2013. Pocillopora aliciae: a new species of scleractinian coral (Scleractinia, Pocilloporidae) from subtropical Eastern Australia. Zootaxa 3626 (4), 576–582. Schoepf, V., Grottoli, A.G., Levas, S.J., Aschaffenburg, M.D., Baumann, J.H., Matsui, Y., et al., 2015. Annual coral bleaching and the long-term recovery capacity of coral. Proceedings. Biological sciences 282, 20151887. Siebeck, U., Marshall, N., Klüter, A., Hoegh-Guldberg, O., 2006. Monitoring coral bleaching using a colour reference card. Coral Reefs 25, 453–460. Sommer, B., Sampayo, E.M., Beger, M., Harrison, P.L., Babcock, R.C., Pandolfi, J.M., 2017. Local and regional controls of phylogenetic structure at the high-latitude range limits of corals. Proc. R. Soc. B Biol. Sci. 284. Speed, C.W., Babcock, R.C., Bancroft, K.P., Beckley, L.E., Bellchambers, L.M., Depczynski, M., et al., 2013. Dynamic stability of coral reefs on the West Australian Coast. PLoS One 8, e69863. Strong, A.E., Barrientos, C.S., Duda, C., Sapper, J., 1997. Improved satellite techniques for monitoring coral reef bleaching. Proceeding of the 8th International Coral Reef Symposium. 2, pp. 1495–1498. Sully, S., Burkepile, D.E., Donovan, M.K., Hodgson, G., van Woesik, R., 2019. A global analysis of coral bleaching over the past two decades. Nat. Commun. 10 (1264), 1–5. Tebbett, S.B., Streit, R.P., Bellwood, D.R., 2019. Expansion of a colonial ascidian following consecutive mass coral bleaching at Lizard Island, Australia. Mar. Environ. Res. 144, 125–129. Thomson, D.P., Bearham, D., Graham, F., Eagle, J.V., 2011. High latitude, deeper water coral bleaching at Rottnest Island, Western Australia. Coral Reefs 30, 1107. Torda, G., Donelson, J.M., Aranda, M., Barshis, D.J., Bay, L., Berumen, M.L., et al., 2017. Rapid adaptive responses to climate change in corals. Nat. Clim. Chang. 7, 627. Tuckett, C., de Bettignies, T., Fromont, J., Wernberg, T., 2017. Expansion of corals on temperate reefs: direct and indirect effects of marine heatwaves. Coral Reefs 36, 947–956. Veron, J.E.N., 2000. Corals of the World. 3. Australian Institute of Marine Science, Townsville. Veron, J.E.N., Done, T.J., 1979. Corals and coral communities of Lord Howe Island. Australian Journal of Freshwater Research 30, 203–236. Wernberg, T., Bennett, S., Babcock, R.C., de Bettignies, T., Cure, K., Depczynski, M., et al., 2016. Climate-driven regime shift of a temperate marine ecosystem. Science 353, 169–172. Wilkinson, C.R., 2008. Status of Coral Reefs of the World. AIMS, Townsville, p. 2008. Yamano, H., Sugihara, K., Nomura, K., 2011. Rapid poleward range expansion of tropical reef corals in response to rising sea surface temperatures. Geophys. Res. Lett. 38.