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Repeat bleaching of a central Pacific coral reef over the past six decades (1960–2016)

The oceans are warming and coral reefs are bleaching with increased frequency and severity, fueling concerns for their survival through this century. Yet in the central equatorial Pacific, some of the world’s most productive reefs regularly experience extreme heat associated with El Niño. Here we use skeletal signatures preserved in long-lived corals on Jarvis Island to evaluate the coral community response to multiple successive heatwaves since 1960. By tracking skeletal stress band formation through the 2015-16 El Nino, which killed 95% of Jarvis corals, we validate their utility as proxies of bleaching severity and show that 2015-16 was not the first catastrophic bleaching event on Jarvis. Since 1960, eight severe (>30% bleaching) and two moderate (<30% bleaching) events occurred, each coinciding with El Niño. While the frequency and severity of bleaching on Jarvis did not increase over this time period, 2015–16 was unprecedented in magnitude. The trajectory of recovery of this historically resilient ecosystem will provide critical insights into the potential for coral reef resilience in a warming world.

The oceans are warming and coral reefs are bleaching with increased frequency and severity, fueling concerns for their survival through this century. Yet in the central equatorial Pacific, some of the world's most productive reefs regularly experience extreme heat associated with El Niño. Here we use skeletal signatures preserved in long-lived corals on Jarvis Island to evaluate the coral community response to multiple successive heatwaves since 1960. By tracking skeletal stress band formation through the 2015-16 El Nino, which killed 95% of Jarvis corals, we validate their utility as proxies of bleaching severity and show that 2015-16 was not the first catastrophic bleaching event on Jarvis. Since 1960, eight severe (>30% bleaching) and two moderate (<30% bleaching) events occurred, each coinciding with El Niño. While the frequency and severity of bleaching on Jarvis did not increase over this time period, 2015-16 was unprecedented in magnitude. The trajectory of recovery of this historically resilient ecosystem will provide critical insights into the potential for coral reef resilience in a warming world. are significant changes in ocean biogeochemistry, as wind-driven and topographic upwelling weaken or cease altogether, driving changes in upper ocean nutrient concentrations, primary productivity 7,8 , and carbonate system chemistry 9 .
Such environmental extremes are felt strongly by the coral communities of Jarvis Island, an uninhabited coral reef ecosystem within the US Pacific Remote Islands Marine National Monument (0.37°S, 159.99°W). Here, degree heating weeks (DHW), a metric of accumulated temperature stress 10 , approached and/or exceeded 10°C-weeks six times since 1982 (Fig. 1). While such conditions are considered conducive for repeat episodes of catastrophic bleaching and mortality, Jarvis appears to have remained highly productive over much of this time. Surveys conducted between 2000 and 2009 revealed total cover of reef-building organisms (primarily corals and coralline algae) close to 50%, exceeding the central Pacific average for uninhabited islands, and turf and macroalgal cover significantly lower than average 11 . Further, fish populations on Jarvis are dominated by the highest trophic levels, and represent one of the largest concentrations of fish biomass for coral reefs in the central and western Pacific 12 . These observations have raised questions about the nature of the response of the Jarvis coral communities, and others located in the central equatorial Pacific, to repeated exposure to extreme conditions at frequencies expected to devastate most tropical reefs by mid-century 13 .  Fig. 1 A comparative history of thermal stress represented by Degree Heating Weeks (DHWs) and cumulative DHWs or Total Hotspot on a Jarvis Island, central equatorial Pacific, b Palau, western tropical Pacific, and c northern Great Barrier Reef since 1980. DHWs > 4 (red dashed line) are considered conducive for coral bleaching and > 8 for severe bleaching and mortality. Jarvis corals experienced seven > 4 and six > 8 DHW episodes since 1980. Palau corals experienced two episodes > 4 DHW (1998 and2010). For corals in the northern GBR, the 2016 thermal anomaly was their first encounter with ocean conditions considered conducive for bleaching. Here, DHWs are calculated using a percentile method rather than the traditional mean monthly maximum (MMM) to estimate maximum mean SST experienced by each reef. This approach was taken to enable direct comparison between regions dominated by inter-annual SST variability (central equatorial Pacific) and those dominated by seasonal SST variability (western tropical Pacific). A detailed description of the percentile method and the comparison with traditional NOAA DHWs for these three sites are provided in the Methods and Supplementary Information Here we present a history of the Jarvis coral community response to repeat El Niño-induced heatwaves spanning the last six decades, reconstructed using a bleaching proxy archived in the skeletons of massive corals that survived these events. Stress bands, anomalously high-density bands revealed in the skeletons of massive, long-lived corals by x-radiography or 3-D computerized tomography (CT) scanning, have long been qualitatively associated with coral bleaching [14][15][16][17][18] . Recently, Barkley and Cohen 19 demonstrated a strong correlation between the proportion of stress bands in populations of massive Porites corals in Palau and the observed severity of community-wide bleaching at eleven lagoon, patch, and barrier reef stations during the 1997-8 and 2009-10 El Niño's. This finding provided a quantitative tool with which to evaluate the severity of the coral reef response to historical thermal stress in the absence of real-time visual observations.
In this study, we use ecological surveys conducted on Jarvis in November 2015 during the peak of the 2015-16 El Niño, and data from Howland Island in 2010, to validate the use of the skeletal bleaching proxy outside of Palau. Skeletal cores extracted from massive Jarvis Porites corals before (2010, 2012), during (2015) and after (2016, 2017) the bleaching event allow us, for the first time to our knowledge, to link stress band formation with active bleaching, to evaluate the underlying mechanism for stress band formation, and to track the incorporation of the bleaching signal into the growing skeleton. Finally, we use stress bands archived in the skeletons of long-lived coral survivors to reconstruct a quantitative history of bleaching on Jarvis and to place the severity of the 2015-16 event on Jarvis in the context of the last six decades.

Results
The 2015-16 coral bleaching event at Jarvis. Multiple ecological surveys of Jarvis have been conducted by the Ecosystem Sciences Division of the National Oceanic and Atmospheric Administration (NOAA) Pacific Islands Fisheries Science Center since 2000 20 . However, prior to 2015, none of these surveys coincided with peak El Niño conditions. Minor bleaching (~3%) was recorded in April 2010, although those surveys occurred after the El Niño had subsided 21 . We conducted an expedition to Jarvis Island from 13 th to 16 th November 2015 coinciding with the peak SST anomaly associated with the 2015-16 El Niño. Our expedition provided the first opportunity to directly observe and measure the reef response to extreme heat. At the time of our arrival on site, SST anomalies in the region had exceeded 3°C for 20 consecutive weeks (Fig. 1, Supplementary Figures 1-2). Photographic surveys conducted along triplicate 50 m transects spanning 5 m to 25 m depth revealed average live coral cover of 25.3% cover (±2.5% SE) with visible bleaching in 95.4% (±1.8% SE) of coral-covered substrate, and a small but significant decrease with depth (two-way ANOVA, F 2,14 = 6.64, p = 0.009) (Fig. 2, Supplementary Tables 1-2). Levels of bleaching near 100% were observed in fast-growing Montipora colonies dominant on the island's western (leeward) side, branching Pocillopora colonies abundant on the island's eastern (windward) side, and massive Porites colonies, some exceeding 100 years in age. Discrete water samples and instrument deployments documented a dramatic shift in nearshore chemistry concurrent with elevated temperatures. Nitrate concentrations on the reef decreased from the climatological mean of 5 µM 22 to levels at or below detection. Both pH and aragonite saturation state (Ω ar ) increased above climatology 22 , likely due to a combination of upwelling cessation and a reduction in reef calcification ( Supplementary Figures 3-4, Supplementary Table 3).
Skeletal cores extracted in November 2015 from bleached Porites colonies revealed the impact of prolonged bleaching on skeletal growth. In 3-D Computerized Tomography (CT) scans, unusually high-density bands (called stress bands), otherwise invisible to the naked eye, were observed forming at the top of 88% of the cores (Fig. 3a, b). In addition, the cores revealed añ 50% decrease in tissue thickness, from an average ( ± SE) of 8.3 mm ( ± 0.4 mm) in colonies we had sampled during neutral periods of the El Niño-Southern Oscillation (September 2012 and April 2010) to 4.8 mm (±0.4 mm) in colonies we sampled in November 2015 (Two-sided Welch T-test, t = 6.3, df = 33.9, 95% CI = 2.3, 4.6, p < 0.001). The decrease in tissue thickness, which likely reflects the bleached corals' metabolism of their own biomass to fuel basic physiological functioning during starvation 17,23 , plays a major role in stress band formation by limiting the ability of the coral to extend its skeleton upward during calcification 18 . Consequently, instead of using newly accreted calcium carbonate to extend upward, the bleached coral thickens existing skeleton, resulting in a discrete, anomalously high-density band visible in the CT image. The prolonged 2015-16 bleaching event on Jarvis led to severe coral mortality (Fig. 2). Low temperature spikes recorded by in situ temperature loggers deployed on the west side of the island, as well as elevated concentrations of dissolved inorganic nutrients in discrete water samples and decreases in both pH and Ω ar , revealed that upwelling had resumed by the time of our follow-up expedition in May 2016 ( Supplementary Figures 2-4). However, live coral cover had plummeted from 25.3% ( ± 2.5% SE) to 1.7% ( ± 0.6% SE) (Three-way ANOVA with post hoc Tukey HSD; 2015-2016: diff = −23.6%, 95% CI = -28.3, −18.9, p < 0.001; Supplementary Tables 1-2). Along our survey transects, evaluated in both 2015 and in 2016, mortality of non-massive genera, including previously dominant Montipora and Pocillopora corals, was nearly 100%, consistent with results of independent island-wide surveys 20 . Amongst the surviving corals, we observed colonies of Acropora, Hydnophora, Pavona, and Favia spp., as well as massive Porites which exhibited extensive partial mortality (Fig. 4).
We returned to Jarvis Island again in April 2017, 18 months after peak bleaching. Coral cover had not measurably increased ( Fig. 2), but initial signs of recovery were evident. Live juvenile colonies of eleven Scleractinian genera, including Pocillopora, Porites, Leptoseris, Favia, and Psammocora were observed and counted (Supplementary Figure Table 5). Several massive Porites colonies that appeared dead with no sign of living polyps in 2016 were once again covered with healthy zooxanthellate-laden tissue, and tissue thickness had recovered to pre-bleaching levels (average 8.21 mm ± 0.14, n = 12) (Figs. 3c, 4). CT scans of skeletal cores extracted from the recovered colonies in 2017 revealed the 2015 stress bands and mortality scars now entrapped beneath a new layer of skeletal growth (Figs. 3c, 4). In some colonies, post-2015 growth appeared to have been initiated by the same polyps that created the stress band but were presumed dead from the prolonged bleaching. In these colonies, the individual corallite tracks of these polyps are traceable from beneath and across the stress band and into the post-bleaching skeletal growth (Fig. 4d).
Skeletal reconstructions of historical coral bleaching. Visual surveys during three separate expeditions during and after the 2015-16 El Niño recorded catastrophic bleaching and mortality on Jarvis in response to extreme and prolonged heat. Further, massive, long-lived Porites corals that bleached, starved, lost tissue mass, and subsequently recovered, archived a record of the bleaching event as anomalously high-density stress bands within their skeletons (Fig. 3). The proportion of Porites colonies presenting with 2015-16 stress bands was consistent with the catastrophic scale of bleaching and mortality in the Jarvis coral community (Fig. 5a).
However, examination of the CT scans of longer skeletal cores extracted from Jarvis Porites indicate that 2015-16 was not the first time these corals had formed stress bands. Indeed, multiple stress bands are apparent down the length of the majority of the cores (Fig. 3e, Supplementary Figure 7). We used annual high-low density band counts combined with annual extension rates estimated by the distance between successive monthly dissepiments 18 to assign ages to all the historical stress bands. Two cores extend back to the turn of the 20 th century, and the earliest stress bands appear in these cores in 1912, indicating that bleaching occurred on Jarvis over 100 years ago. However, the error on the stress band proportions derived from only two cores was too large to support a meaningful interpretation of bleaching severity in the context of the observational data. Therefore, in this study, we quantified stress band proportions-the fraction of coral cores with a stress band in a given year relative to the total number of cores examined-and reconstructed a history of beaching severity for the period 1960-2016, with a minimum of 7 cores represented in each year (Supplementary Tables 6-7).
The Extended Reconstructed Sea Surface Temperature (ERSST) data product (https://iridl.ldeo.columbia.edu/SOURCES/.NOAA/. NCDC/.ERSST/.version3b) provides monthly resolved SST estimates in a 2°× 2°grid box centered on Jarvis Island. We used this data product to evaluate the magnitude of the 2015-16 SST anomaly on Jarvis in the context of the historical record of SST at this site, 1960-2016. The magnitude of the 2015-16 thermal anomaly on Jarvis was unprecedented since 1960 (Fig. 5c), and our historical bleaching reconstruction reveals that the severity of community-wide bleaching was similarly exceptional. However, contrary to the global trend 24 25 . Taken together, these observations suggest uncommon resilience of a coral reef community exposed to repeated, dramatic fluctuations in ocean temperature and biogeochemical change.
Recovery potential of Jarvis coral reefs. Under certain circumstances, coral reefs are able to recover from catastrophic bleaching-induced mortality, but require time to do so [26][27][28] . Thus, concerns about coral reef futures under 21 st century ocean warming are centered primarily around high-frequency, repeat bleaching events which may prevent coral communities from achieving full recovery before bleaching occurs again and may preclude adaptation 24 . Our historical bleaching reconstruction reveals a coral reef community that has bleached frequently, and at times catastrophically, yet appears to have maintained a healthy state over time. Understanding the mechanisms underlying such resilience could provide key insights into the conditions under which reefs might tolerate 21 st century ocean warming and help to advance successful management strategies under global climate change.
Our data suggest that Jarvis corals are not resistant to thermal stress, as are some coral reef communities considered to be climate refugia 29 . Indeed, our bleaching record indicates that the severity of bleaching of the Jarvis coral community has been proportional to the level of thermal stress imposed over the last six decades. Furthermore, our skeletal records show that Jarvis a b c d Fig. 4 Bleaching, tissue loss and recovery of a massive Porites coral on Jarvis Island, and incorporation of the bleaching signal into the skeleton. a Porites ID 497 at 16.5 m depth on the west side of the island (0.369°S, 160.008°W) bleached in 2015, and in May 2016, no live tissue was evident on the colony surface. b, c By April 2017, the coral exhibited almost full recovery. In (d) A 3-D CT scan of a core removed from the recovered colony in 2017 revealed almost 1 cm of new growth above the stress band, a growth rate~30% lower than pre-bleaching rates (scale bar = 1 cm). A mortality scar (arrow), signaling complete localized loss of tissue for an extended period, is also visible in the scan. Corallite tracks, which are the skeletons of individual polyps, are continuous across the mortality scar, indicating some polyps survived the bleaching deep inside the skeleton, revived and continued to extend their original corallites once ocean conditions returned to normal corals bleach repeatedly and, based on our observations of the impact of the 2015-16 heatwave, it is likely that many probably die during the most extreme events. Enhanced productivity of the central equatorial Pacific, fueled by trade wind and topographic upwelling 30 , as well as the remote location of the Jarvis system relative to human populations 31 , may play key roles in its recovery. On Jarvis, extreme El Niño events that cause bleaching are generally followed by an abrupt resumption of upwelling during which cool, nutrient-rich waters fuel rapid tissue biomass renewal in some species (Fig. 4, Supplementary Figures 2-4). Jarvis hosts dense populations of herbivorous fish 12 that prevent fast-growing macroalgae from overgrowing the reef substrate 13,32 , and likely stall the shift from coral to algal dominated systems as occurred in the Caribbean 33 Table 5). This step in coral community recovery is critical because CCA helps to stabilize the substrate following coral mortality and is a favored settlement substrate for coral larvae 35 (Supplementary Figure 5, Supplementary Table 4). Finally, Montipora and Pocillopora species, abundant on Jarvis prior to 2015, are fast-growing coral genera capable of quickly recolonizing a devastated reef following successful recruitment 36,37 . Indeed the dominance of these genera in Jarvis' highly productive, albeit relatively depauperate, coral community may be a strategic trade-off that enhances the resilience of coral reefs in highly stressful environments.
With less than 5% live corals remaining in 2017, it is uncertain whether new recruits are being supplied primarily by the few survivors, from deeper dwelling corals that may have been unaffected by the bleaching, or by larvae from neighboring islands. The magnitude and duration of the 2015 heat stress was likely the highest and longest that Jarvis Island coral communities have ever experienced, a fact that will likely prolong its recovery relative to prior years. Yet, the historical record implies that Jarvis has recovered from catastrophic events in the past and gives reason to hope that Jarvis will regain its previously vibrant and productive coral-based ecosystem. Further, the protected status of Jarvis in the Pacific Remote Islands Marine National Monument ensures intact populations of grazers, and eliminates land-based sources of sediment and pollution, additional safeguards that are known to maximize the chances of recovery.

Conclusions
The coral communities on Jarvis Island, a highly productive coral reef ecosystem in the central equatorial Pacific, experienced catastrophic bleaching and mortality during the 2015-16 El Niño. Massive long-lived Porites corals that bleached, starved, suffered extensive partial mortality, and recovered from the prolonged heatwave, archived a record of the reef-wide bleaching event as discrete high-density stress bands within their skeletons. In this study, we showed that the proportion of stress bands in populations of Porites corals sampled on three reef systems including Jarvis, scales with the severity of bleaching in the coral  19 . This relationship allows us to reconstruct the history of bleaching on Jarvis in the absence of visual observations. b Percent of Jarvis Porites corals with a stress band in a given year scale with the level of thermal stress experienced by the community that year, indicating that the Jarvis coral community responds predictably to thermal stress. Total Hotspot, an index of the cumulative thermal stress during a specific event, is calculated from weekly satellite SST spanning the time period 1982-2016. In (c) six decades of coral reef bleaching on Jarvis Island (vertical bars, mean ± one standard error), 1960-2016, constructed from stress bands using the calibration in (a). The time series of ERSST anomalies over the same time period, for a 2°× 2°grid centered on Jarvis, is shown in blue. All bleaching events coincide with high SST anomalies communities as recorded by visual observations. Applying this relationship to down-core records of Jarvis Porites stress bands reveals that multiple historical bleaching events, three of them catastrophic, occurred on Jarvis Island between 1960 and 2016. We found that the frequency and severity of bleaching events did not increase over this time period. Nevertheless, the magnitude of the 2015-16 thermal anomaly at Jarvis and the severity of the 2015-16 bleaching were unprecedented in the record. We believe that the timing and trajectory of recovery of this historically resilient ecosystem will provide critical new insights into the potential for coral reef survival in an era of unprecedented ocean change.

Methods
Percentile-based method for calculated thermal stress. The traditional DHW calculation (1°C above the Maximum Monthly Mean or MMM) cannot be meaningfully applied to regions dominated by inter-annual SST variability, prohibiting a comparison of thermal stress on a global scale. The MMM is average temperature of the warmest month over several pre-specified years. However in the central equatorial Pacific, peak temperatures do not occur during the same month in every year and the traditional MMM calculation generally underestimates the high end of temperatures that corals normally see at these sites. Consequently, central equatorial Pacific DHWs calculated using the traditional method are generally overestimated (Supplementary Figure 1). To enable direct comparison of thermal stress on reefs dominated by seasonal-vs. inter-annual SST variability, a percentile-based thermal threshold was developed to estimate the maximum temperature corals normally experience. Average weekly satellite-based SSTs (IGOSS Reyn_Smith OIv2, 1°× 1°resolution, https://iridl.ldeo.columbia.edu/ SOURCES/.IGOSS/.nmc/.Reyn_SmithOIv2) during neutral years of the El Niño-Southern Oscillation (1984-5, 1990, 1993, 1996) Table 8). Analysis of temperature time series was conducted in MATLAB (2017a). Coral cores were oven-dried and scanned with a Siemens Volume Zoom Helical Computerized Tomography (CT) Scanner at WHOI and at the University of North Carolina Biomedical Research Imaging Facility. Density banding and stress band presence was evaluated in 3-D CT scans of coral cores using the automated coralCT software 39 . Density time series were extracted and averaged from individual polyp growth tracks, which accounts for the different ages of skeleton in horizontal cross sections due to uneven growth geometry, in 0.1 mm increments from the top of the skeletal core up to 70 cm down core. Density values were converted to Z-scores by subtracting the long-term core mean density from each raw density value and dividing by the long-term standard deviation. High-density stress bands were defined as bands greater than 1 mm thick that spread across the entire width of the core where density values exceeded two standard deviations of the whole core density mean (i.e., a Z-score greater than 2). Stress bands that formed prior to 2010 were identified based on density banding patterns counted downward from the core top. Stress bands that were forming in 2015-16 were dated based on their location at the very top of the core (indicating that they were forming during the time of collection). Coral tissue thickness, measured as the vertical distance between the top of the core to the most recently accreted dissepiment, was measured on a slice of skeleton cut from the top of each core using a Nikon SMZ1500 stereomicroscope and SPOT imaging software. , mid and deep: 0.367°S, 159.979°W) of the island. Each replicate 50 m transect was laid~5 m apart in the cross-shore direction, and a photograph of a 0.5 m × 0.5 m quadrat taken every meter. Photographs were analyzed using Coral Point Count with Excel extensions 40 . Live coral cover of each photograph was evaluated by randomly overlaying ten points on each image and identifying the type of substrate (coral vs. non-coral) and any coral colony to the genus level, with 500 points identified per transect and 1500 points identified per depth. In 2015, random points that fell on live coral were identified as healthy (pigmented tissue) or bleached (non-pigmented living tissue), with the bleached cover calculated as the total number of random points located on bleached tissue divided by the total number of points identified as live (healthy + bleached) coral. In 2016 and 2017, no corals in the transects were still bleached, and were therefore identified as either live or dead. Transect survey data met assumptions for normality (Shapiro Test) and homoscedasticity (Levene's test) and were analyzed with three-way ANOVA tests with post hoc Tukey Honest Significant Difference tests to evaluate the effect of side (west and east), depth (shallow, mid-depth, and deep), and year (2015, 2016, 2017) on live coral cover and. A two-way ANOVA with post hoc Tukey Honest Significant Difference test was used to evaluate the effect of side and depth on bleached coral cover. All statistical analyses were conducted in R (version 3.0.1). Crustose coralline algae cover and juvenile coral data were provided by the Ecosystem Sciences Division of the NOAA Pacific Islands Fisheries Science Center.
Water sampling. Discrete seawater samples were collected during each sampling period for salinity, nutrients, total alkalinity (TA), and dissolved inorganic carbon (DIC). Temperature and depth were recorded with Seabird Electronics ( . TA and DIC analyses were performed using a Versatile Instrument for the Determination of Total inorganic carbon and titration Alkalinity (Marianda Analytics and Data) and standardized using certified reference materials obtained from Andrew Dickson (Scripps Institution of Oceanography). Salinity samples were analyzed at WHOI using a Guildline autosal salinometer, and nutrient samples were run at the WHOI Nutrient Analytical Facility. Full CO 2 system parameters were calculated from temperature, salinity, TA, and DIC using CO2SYS with the constants of Mehrbach et al. 41  Instrument deployments. In situ, long-term temperature logger data were provided by NOAA and were collected by SBE 39 and SBE 56 temperature loggers (Sea-bird Electronics, 5-30 min sampling interval) on the west (0.369°S, 160.008°W) and east (0.372°S, 159.983°W) sides of Jarvis. Short-term oceanographic instrument deployments were conducted at the same sites on 12-15 November 2015 and 16-23 May 2016. Instrument package deployments included a SAMI-pH sensor (Sunburst Sensors, 15 min sampling interval), SBE-37 Microcat (Sea-Bird Electronics, 20 s sampling interval), and dissolved oxygen sensor (RBR, 1 min sampling interval) which were affixed to the reef at 7 m (east) and 10 m (west) depth.

Data availability
Coral skeletal core, ecological, and oceanographic data analyzed in the current study are presented in the Supplementary Materials and are available in the BCO-DMO data collection (https://www.bco-dmo.org/project/687813). Additional longterm oceanographic data and temperature time series collected as part of the National Coral Reef Monitoring Program are available from Data.gov (http:// catalog.data.gov/).