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Bleaching, mortality and lengthy recovery on the coral reefs of Lord Howe Island. The 2019 marine heatwave suggests an uncertain future for high-latitude ecosystems [1]

['Tess Moriarty', 'School Of Environmental', 'Life Sciences', 'The University Of Newcastle', 'Ourimbah', 'New South Wales', 'William Leggat', 'Scott F. Heron', 'Physics', 'Marine Geophysical Laboratory']

Date: 2023-05

Oceanic thermal anomalies are increasing in both frequency and strength, causing detrimental impacts to coral reef communities. Water temperatures beyond the corals optimum threshold causeing coral bleaching and mass mortality, impacting our global coral reef ecosystems, including marginal high-latitude reefs. Coral bleaching and mortality were observed at the southernmost coral reef, Lord Howe Island Marine Park, during the summer of 2019, coinciding with anomalously high sea surface temperatures across the reef system from January-April. Here we document the extent of coral impacts within the Lord Howe Island lagoonal reef and the recovery from bleaching eight-months later. Significant differences in bleaching prevalence were observed across the lagoonal coral reef, ranging from 16 to 83% across offshore and inshore reef regions and with variable onset timing. Coral mortality of up to 40% was recorded in the reef’s most severely impacted near-shore area. The four most dominant species, Stylophora pistillata, Pocillopora damicornis, Porites spp. and Seriatopora hystrix, were the most susceptible to bleaching, with all coral colonies found either bleached or dead at the most affected inshore site during and following peak heat stress. Interestingly, during the eight-months following bleaching, there was no evidence of bleaching recovery (i.e., re-establishment of symbiosis) at the offshore lagoonal site. However, there was a significant increase in the abundance of healthy coral colonies at the inshore site, suggesting the recovery of the surviving bleached corals at this site. Importantly, we found no evidence for bleaching or mortality in the Acropora spp. and minimal bleaching and no mortality in Isopora cuneata during the study period, typically highly susceptible species. Given the isolation of high-latitude reefs such as Lord Howe Island, our results highlight the importance of understanding the impacts of bleaching, mortality and bleaching recovery on coral population structure and resilience of high-latitude coral reefs.

Funding: This project was partially funded by the University of New South Wales (UNSW) Scientia program award to T.D.A. 2018-2028, Australian Research Council (ARC) Research funding (DP180103199) The Women's Diving Hall of Fame –Marine Conservation Scholarship awarded to T.M. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Introduction

Coral reefs account for less than 1% of the total ocean benthos. Although these ecosystems make up a small proportion of ocean area, they afford habitat and protection for a quarter of all marine species [1]. They also provide numerous ecological goods and services, including food, coastal protection, income, recreational activities, and cultural and aesthetic values [2]. These ecosystems are predominantly located in tropical, shallow, warm waters, where conditions such as; temperature, light, salinity, aragonite saturation, and nutrients are optimal for coral growth [3]. Coral reef ecosystems are experiencing significant disturbances due to the increased frequency and severity of thermal anomalies [4, 5].

Corals exposed to increased water temperatures over an extended period of time cause coral bleaching. Coral bleaching is the breakdown of the partnership between the coral host and the symbiotic algae, Symbiodiniaceae [6], which provides most corals’ energy requirements [7]. A decline in the symbiotic algae results in a reduction of pigmentation and, in extreme events, the expulsion of a significant amount of the symbiotic algae resulting in translucent coral tissue, giving the coral a white appearance because of the exposed white endoskeleton [8]. Bleached corals are vulnerable to mortality if energy requirements are not fulfilled either through heterotrophic means or by regaining symbionts [7]. Major coral reef systems have already felt mass mortalities from coral bleaching [9].

Coral reefs have been reported to display varying responses to thermal anomalies through acclimation and local reef dynamics [10–13]. Some sites have been resilient during thermal anomalies, whilst others are highly vulnerable to reported while changes in community composition [5, 14, 15]. There is increased concern for the future of coral reefs and whether these sites exhibiting resiliency to climate change can be identified as places of refuge [16, 17]. High-latitude reefs (reefs higher than 28 degrees north and 28 degrees south) have been identified as potential sources of refuge for corals since corals living in these locations are accustomed to being pushed to their geographical and physiological limits [16, 18–20]. Unlike their low-latitude coral reef counterparts, there is a lack of understanding of the outcomes and responses high-latitude reefs experience during thermal anomalies.

The sub-tropical reef lagoon of Lord Howe Island (LHI) Marine Park is a unique coral reef ecosystem located in the southwestern Pacific Ocean, more than 1,000 km south of the Great Barrier Reef. The island is home to the world’s southernmost coral reef and hosts a diverse and abundant reef system of tropical and temperate species [21–25]. The coral reefs of this World Heritage-listed island group have been associated with high endemism and species richness, with many of the 86 described species of coral thought to be endemic [26] and approximately 4% of the 433 shore fish [24, 27] and 15% of the 305 marine algae also endemic.

Species extinctions, loss of habitat structure, ecosystem degradation, declines in coral cover and phase-shifts to algal-dominated systems are common features of coral reefs worldwide [14, 15, 28–30]. Yet high-latitude reefs, such as Lord Howe Island, have previously been hypothesised as refugia for corals in the coming decades [16, 18–20], with some studies suggesting marginal reefs may be protected from the most severe impacts of global warming due to their geographic location (though note the potential opposing effects of ocean acidification; [31]). However, these ecosystems previously thought to be protected from the impacts of climate change are experiencing rapid change [32–38], much like other coral reef ecosystems [6, 9, 28, 39, 40]. High-latitude coral reefs have also been exposed to severe and frequent bleaching events, impacting coral reefs worldwide [32, 37, 41–46].

The first record of bleaching on the reefs of Lord Howe Island was in 1998 [46], coinciding with the most severe global bleaching event at that time [6, 47–49]. Since then, anomalously high seawater temperatures associated with coral bleaching occurred in 2010 and 2011 [45, 46]. In March 2010, up to 99% of Lord Howe Island’s lagoonal corals experienced bleaching, and in deeper reef sites, 17% of corals bleached [45]. The 2011 bleaching event revealed reduced bleaching susceptibility for all coral taxa recorded compared to the 2010 bleaching [45]. The four most common genera Pocillopora, Porites, Seriatopora and Stylophora, had high bleaching susceptibility index (BSI) and were the most severely impacted by bleaching [45]. Acropora and Isopora were reported to have undergone mild bleaching in 2010 and 2011 [45]. The three branching morphology taxa most severely impacted by bleaching (Seriatopora, Stylophora and Pocillopora) also had the highest colony mortality. Coral cover declined by approximately 28% in the most inshore reef areas immediately following the 2010 bleaching event, with coral mortality as high as 69% [45]. Following the 2010/2011 bleaching events surviving plating Acropora colonies were outcompeted by ascidians and algae [45].

Severe bleaching and high mortality levels alter community composition, leading to changes in ecological function. Hard coral cover increased in the three years following the 2010/2011 events. However, this was coupled with a reduction in Acropora colonies, suggesting complex community-level changes on the Lord Howe Island lagoonal reef [45]. Further changes to coral community structure due to recent thermal anomalies have also been reported, as have changes to coral growth and disease resistance [34, 45, 46]. Taxon-specific annual linear coral growth declines of up to 30% were recorded following the 1998 and 2010/2011 thermal anomalies [34]. Two prominent coral species, Acropora yongei and Pocillopora damicornis, declined in average annual linear extensions of 15.9 mm and 5.4 mm, respectively. In contrast, no significant difference in linear extension was reported for Porites sp. and Seriatopora hystrix between 1994/1995 and 2010/2011 [34]. Four coral diseases (growth anomalies, white syndrome, skeletal eroding band and hypermycosis) have also been identified in the lagoon impacting six coral taxa [Moriarty per obvs]. The high-latitude coral reefs of the world’s southernmost reef system are not isolated from the effects of warming oceans and the impacts of heat stress, including bleaching, mortality, disease and reduction in growth experienced in this ecosystem.

Understanding the impact of increasingly severe and more frequent bleaching events across the biogeographic extent of coral reefs and the capacity for ecosystem recovery and resilience is imperative in determining the long-term sustainability of different reef ecosystems. In 1999, climate model predictions of coral bleaching indicated events would increase in frequency and intensity within the coming decades [6]. These predictions have since been realised regionally (e.g., the Caribbean in 2005; [50]) and globally (in 2010 and 2014–2016; [51–53]. Bleaching events are highly variable, and the magnitude in severity is often mediated by local environmental and physical parameters [5, 10, 13, 14, 54–56]. Including bleaching history, in-situ temperature regimes, water flow, nutrients, tropical cyclone-driven cooling, coral taxa, coral taxa morphology and coral taxa abundance [14, 51, 54, 57–63]. For example, coral taxon, tissue thickness and morphology type influenced which coral species had the capacity to be “winners and losers” from the 1998 bleaching event in Okinawa, Japan [14]. Interestingly, subsequent research [64] attributed (1) thermal tolerance of the locally abundant colonies, (2) remnant survivors that rapidly regrew, and (3) regionally abundant colonies characterised as long-term “winning” taxa within the reef ecosystem. “Winners and losers” on coral reefs under climate change reflect complex biophysical factors within each coral reef ecosystem.

Many of the tropical and temperate species of LHI are at their marginal limits [65]. Ongoing periods of increased sea temperatures beyond the thermal tolerance of the diverse community of tropical, temperate and endemic species are likely to lead to significant shifts in community composition and raise questions on the long-term resilience of the World Heritage-listed marine park ecosystem. Here we investigate the heat stress event in early 2019 and the associated coral bleaching on the high latitude reefs of Lord Howe Island Marine Park. We quantify the extent of bleaching, mortality, and taxonomic variation within the lagoon reef system related to the 2019 bleaching event and the recovery of the reef eight months after bleaching occurred. In doing so, we aim to determine the short- and long-term impacts of heatwave events on the Lord Howe Island lagoon coral species.

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[1] Url: https://journals.plos.org/climate/article?id=10.1371/journal.pclm.0000080

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