Conservation genetics and the resilience of reef-building corals

Coral reefs have suffered long-term decline due to a range of anthropogenic disturbances and are now also under threat from climate change. For appropriate management of these vulnerable and valuable ecosystems it is important to understand the factors and processes that determine their resilience and that of the organisms inhabiting them, as well as those that have led to existing patterns of coral reef biodiversity. The scleractinian (stony) corals deposit the structural framework that supports and promotes the maintenance of biological diversity and complexity of coral reefs, and as such, are major components of these ecosystems. The success of reef-building corals is related to their obligate symbiotic association with dinoflagellates of the genus Symbiodinium. These one-celled algal symbionts (zooxanthellae) live in the endodermal tissues of their coral host, provide most of the host's energy budget and promote rapid calcification. Furthermore, zooxanthellae are the main primary producers on coral reefs due to the oligotrophic nature of the surrounding waters. In this review paper, we summarize and critically evaluate studies that have employed genetics and/or molecular biology in examining questions relating to the evolution and ecology of reef-building corals and their algal endosymbionts, and that bear relevance to coral reef conservation. We discuss how these studies can focus future efforts, and examine how these approaches enhance our understanding of the resilience of reef-building corals.     

Coral reef recovery dynamics in a changing world

Coral reef ecosystems are degrading through multiple disturbances that are becoming more frequent and severe. The complexities of this degradation have been studied in detail, but little work has assessed characteristics that allow reefs to bounce back and recover between pulse disturbance events. We quantitatively review recovery rates of coral cover from pulse disturbance events among 48 different reef locations, testing the relative roles of disturbance characteristics, reef characteristics, connectivity and anthropogenic influences. Reefs in the western Pacific Ocean had the fastest recovery, whereas reefs in the geographically isolated eastern Pacific Ocean were slowest to recover, reflecting regional differences in coral composition, fish functional diversity and geographic isolation. Disturbances that opened up large areas of benthic space recovered quickly, potentially because of nonlinear recovery where recruitment rates were high. The type of disturbance had a limited effect on subsequent rates of reef recovery, although recovery was faster following crown-of-thorns starfish outbreaks. This inconsequential role of disturbance type may be in part due to the role of unaltered structural complexity in maintaining key reef processes, such as recruitment and herbivory. Few studies explicitly recorded potential ecological determinants of recovery, such as recruitment rates, structural complexity of habitat and the functional composition of reef-associated fish. There was some evidence of slower recovery rates within protected areas compared with other management systems and fished areas, which may reflect the higher initial coral cover in protected areas rather than reflecting a management effect. A better understanding of the driving role of processes, structural complexity and diversity on recovery may enable more appropriate management actions that support coral-dominated ecosystems in our changing climate.     

New insights into carbon acquisition and exchanges within the coral–dinoflagellate symbiosis under NH4+ and NO3? supply

Anthropogenic nutrient enrichment affects the biogeochemical cycles and nutrient stoichiometry of coastal ecosystems and is often associated with coral reef decline. However, the mechanisms by which dissolved inorganic nutrients, and especially nitrogen forms (ammonium versus nitrate) can disturb the association between corals and their symbiotic algae are subject to controversial debate. Here, we investigated the coral response to varying N : P ratios, with nitrate or ammonium as a nitrogen source. We showed significant differences in the carbon acquisition by the symbionts and its allocation within the symbiosis according to nutrient abundance, type and stoichiometry. In particular, under low phosphate concentration (0.05 µM), a 3 µM nitrate enrichment induced a significant decrease in carbon fixation rate and low values of carbon translocation, compared with control conditions (N : P = 0.5 : 0.05), while these processes were significantly enhanced when nitrate was replaced by ammonium. A combined enrichment in ammonium and phosphorus (N : P = 3 : 1) induced a shift in nutrient allocation to the symbionts, at the detriment of the host. Altogether, these results shed light into the effect of nutrient enrichment on reef corals. More broadly, they improve our understanding of the consequences of nutrient loading on reef ecosystems, which is urgently required to refine risk management strategies.     

Ongoing collapse of coral-reef shark populations

Marine ecosystems are suffering severe depletion of apex predators worldwide; shark declines are principally due to conservative life-histories and fisheries overexploitation. On coral reefs, sharks are strongly interacting apex predators and play a key role in maintaining healthy reef ecosystems. Despite increasing fishing pressure, reef shark catches are rarely subject to specific limits, with management approaches typically depending upon no-take marine reserves to maintain populations. Here, we reveal that this approach is failing by documenting an ongoing collapse in two of the most abundant reef shark species on the Great Barrier Reef (Australia). We find an order of magnitude fewer sharks on fished reefs compared to no-entry management zones that encompass only 1% of reefs. No-take zones, which are more difficult to enforce than no-entry zones, offer almost no protection for shark populations. Population viability models of whitetip and gray reef sharks project ongoing steep declines in abundance of 7% and 17% per annum, respectively. These findings indicate that current management of no-take areas is inadequate for protecting reef sharks, even in one of the world's most-well-managed reef ecosystems. Further steps are urgently required for protecting this critical functional group from ecological extinction.     

Operationalizing resilience for adaptive coral reef management under global environmental change

Cumulative pressures from global climate and ocean change combined with multiple regional and local‐scale stressors pose fundamental challenges to coral reef managers worldwide. Understanding how cumulative stressors affect coral reef vulnerability is critical for successful reef conservation now and in the future. In this review, we present the case that strategically managing for increased ecological resilience (capacity for stress resistance and recovery) can reduce coral reef vulnerability (risk of net decline) up to a point. Specifically, we propose an operational framework for identifying effective management levers to enhance resilience and support management decisions that reduce reef vulnerability. Building on a system understanding of biological and ecological processes that drive resilience of coral reefs in different environmental and socio‐economic settings, we present an Adaptive Resilience‐Based management (ARBM) framework and suggest a set of guidelines for how and where resilience can be enhanced via management interventions. We argue that press‐type stressors (pollution, sedimentation, overfishing, ocean warming and acidification) are key threats to coral reef resilience by affecting processes underpinning resistance and recovery, while pulse‐type (acute) stressors (e.g. storms, bleaching events, crown‐of‐thorns starfish outbreaks) increase the demand for resilience. We apply the framework to a set of example problems for Caribbean and Indo‐Pacific reefs. A combined strategy of active risk reduction and resilience support is needed, informed by key management objectives, knowledge of reef ecosystem processes and consideration of environmental and social drivers. As climate change and ocean acidification erode the resilience and increase the vulnerability of coral reefs globally, successful adaptive management of coral reefs will become increasingly difficult. Given limited resources, on‐the‐ground solutions are likely to focus increasingly on actions that support resilience at finer spatial scales, and that are tightly linked to ecosystem goods and services.     

Historical reconstruction reveals recovery in Hawaiian coral reefs

Coral reef ecosystems are declining worldwide, yet regional differences in the trajectories, timing and extent of degradation highlight the need for in-depth regional case studies to understand the factors that contribute to either ecosystem sustainability or decline. We reconstructed social-ecological interactions in Hawaiian coral reef environments over 700 years using detailed datasets on ecological conditions, proximate anthropogenic stressor regimes and social change. Here we report previously undetected recovery periods in Hawaiian coral reefs, including a historical recovery in the MHI (~AD 1400-1820) and an ongoing recovery in the NWHI (~AD 1950-2009+). These recovery periods appear to be attributed to a complex set of changes in underlying social systems, which served to release reefs from direct anthropogenic stressor regimes. Recovery at the ecosystem level is associated with reductions in stressors over long time periods (decades+) and large spatial scales (>10(3) km(2)). Our results challenge conventional assumptions and reported findings that human impacts to ecosystems are cumulative and lead only to long-term trajectories of environmental decline. In contrast, recovery periods reveal that human societies have interacted sustainably with coral reef environments over long time periods, and that degraded ecosystems may still retain the adaptive capacity and resilience to recover from human impacts.     

Microorganisms uniquely capture and predict stony coral tissue loss disease and hurricane disturbance impacts on US Virgin Island reefs

Coral reef ecosystems are now commonly affected by major climate and disease disturbances. Disturbance impacts are typically recorded using reef benthic cover, but this may be less reflective of other ecosystem processes. To explore the potential for reef water-based disturbance indicators, we conducted a 7-year time series on US Virgin Island reefs where we examined benthic cover and reef water nutrients and microorganisms from 2016 to 2022, which included two major disturbances: hurricanes Irma and Maria in 2017 and the stony coral tissue loss disease outbreak starting in 2020. The disease outbreak coincided with the largest changes in the benthic habitat, with increases in the percent cover of turf algae and Ramicrusta, an invasive alga. While sampling timepoint contributed most to changes in reef water nutrient composition and microbial community beta diversity, both disturbances led to increases in ammonium concentration, a mechanism likely contributing to observed microbial community shifts. We identified 10 microbial taxa that were sensitive and predictive of increasing ammonium concentration. This included the decline of the oligotrophic and photoautotrophic Prochlorococcus and the enrichment of heterotrophic taxa. As disturbances impact reefs, the changing nutrient and microbial regimes may foster a type of microbialization, a process that hastens reef degradation.     

Predator Crown-of-Thorns Starfish (Acanthaster planci) Outbreak,Mass Mortality of Corals,and Cascading Effects on Reef Fish and Benthic Communities

Outbreaks of the coral-killing seastar Acanthaster planci are intense disturbances that can decimate coral reefs. These events consist of the emergence of large swarms of the predatory seastar that feed on reef-building corals, often leading to widespread devastation of coral populations. While cyclic occurrences of such outbreaks are reported from many tropical reefs throughout the Indo-Pacific, their causes are hotly debated, and the spatio-temporal dynamics of the outbreaks and impacts to reef communities remain unclear. Based on observations of a recent event around the island of Moorea, French Polynesia, we show that Acanthaster outbreaks are methodic, slow-paced, and diffusive biological disturbances. Acanthaster outbreaks on insular reef systems like Moorea''s appear to originate from restricted areas confined to the ocean-exposed base of reefs. Elevated Acanthaster densities then progressively spread to adjacent and shallower locations by migrations of seastars in aggregative waves that eventually affect the entire reef system. The directional migration across reefs appears to be a search for prey as reef portions affected by dense seastar aggregations are rapidly depleted of living corals and subsequently left behind. Coral decline on impacted reefs occurs by the sequential consumption of species in the order of Acanthaster feeding preferences. Acanthaster outbreaks thus result in predictable alteration of the coral community structure. The outbreak we report here is among the most intense and devastating ever reported. Using a hierarchical, multi-scale approach, we also show how sessile benthic communities and resident coral-feeding fish assemblages were subsequently affected by the decline of corals. By elucidating the processes involved in an Acanthaster outbreak, our study contributes to comprehending this widespread disturbance and should thus benefit targeted management actions for coral reef ecosystems.     

三亚珊瑚礁保护区珊瑚礁生态系统现状及其健康状况评价

为评估三亚珊瑚礁国家级自然保护区珊瑚礁生态系统的健康状况, 本文选取东岛、鹿回头、大东海3个站位调查了珊瑚礁群落、珊瑚礁鱼类和大型底栖动物。通过对比分析历史资料、珊瑚礁现场生态调查与监测及组织专家评审, 筛选出一、二级指标并设置权重, 使用综合指数计算了三亚珊瑚礁保护区珊瑚礁生态系统健康指数。结果显示, 三亚珊瑚礁保护区内共有造礁珊瑚10科21属37种, 软珊瑚3种, 造礁珊瑚覆盖率和软珊瑚覆盖率分别为14.31%和0.19%, 其中鹿回头造礁珊瑚覆盖率最高, 为21.58%。珊瑚礁鱼类共14科28属36种, 其中, 雀鲷科的种类数最多, 为11种。鹿回头4 m断面珊瑚礁鱼类密度最大, 为154尾/300 m²。砗磲和龙虾极少发现, 珊瑚天敌核果螺多见。东岛、鹿回头、大东海珊瑚礁生态系统健康状况均处于“一般”。本文所采用的方法是结合常规珊瑚礁监测可获得的指标进行评价, 简便易操作, 通过在三亚珊瑚礁保护区的实践, 能够很好地反映珊瑚礁生态系统现状及其健康状况, 科研和业务化监测部门均可应用。     

Cell biology in model systems as the key to understanding corals

Corals provide the foundation of important tropical reef ecosystems but are in global decline for multiple reasons, including climate change. Coral health depends on a fragile partnership with intracellular dinoflagellate symbionts. We argue here that progress in understanding coral biology requires intensive study of the cellular processes underlying this symbiosis. Such study will inform us on how the coral symbiosis will be affected by climate change, mechanisms driving coral bleaching and disease, and the coevolution of this symbiosis in the context of other host-microbe interactions. Drawing lessons from the broader history of molecular and cell biology and the study of other host-microbe interactions, we argue that a model-systems approach is essential for making effective progress in understanding coral cell biology.     

Marine reserves help coastal ecosystems cope with extreme weather

Natural ecosystems have experienced widespread degradation due to human activities. Consequently, enhancing resilience has become a primary objective for conservation. Nature reserves are a favored management tool, but we need clearer empirical tests of whether they can impart resilience. Catastrophic flooding in early 2011 impacted coastal ecosystems across eastern Australia. We demonstrate that marine reserves enhanced the capacity of coral reefs to withstand flood impacts. Reserve reefs resisted the impact of perturbation, whilst fished reefs did not. Changes on fished reefs were correlated with the magnitude of flood impact, whereas variation on reserve reefs was related to ecological variables. Herbivory and coral recruitment are critical ecological processes that underpin reef resilience, and were greater in reserves and further enhanced on reserve reefs near mangroves. The capacity of reserves to mitigate external disturbances and promote ecological resilience will be critical to resisting an increased frequency of climate‐related disturbance.     

Human activities as a driver of spatial variation in the trophic structure of fish communities on Pacific coral reefs

Anthropogenic activities such as land‐use change, pollution and fishing impact the trophic structure of coral reef fishes, which can influence ecosystem health and function. Although these impacts may be ubiquitous, they are not consistent across the tropical Pacific Ocean. Using an extensive database of fish biomass sampled using underwater visual transects on coral reefs, we modelled the impact of human activities on food webs at Pacific‐wide and regional (1,000s–10,000s km) scales. We found significantly lower biomass of sharks and carnivores, where there were higher densities of human populations (hereafter referred to as human activity); however, these patterns were not spatially consistent as there were significant differences in the trophic structures of fishes among biogeographic regions. Additionally, we found significant changes in the benthic structure of reef environments, notably a decline in coral cover where there was more human activity. Direct human impacts were the strongest in the upper part of the food web, where we found that in a majority of the Pacific, the biomass of reef sharks and carnivores were significantly and negatively associated with human activity. Finally, although human‐induced stressors varied in strength and significance throughout the coral reef food web across the Pacific, socioeconomic variables explained more variation in reef fish trophic structure than habitat variables in a majority of the biogeographic regions. Notably, economic development (measured as GDP per capita) did not guarantee healthy reef ecosystems (high coral cover and greater fish biomass). Our results indicate that human activities are significantly shaping patterns of trophic structure of reef fishes in a spatially nonuniform manner across the Pacific Ocean, by altering processes that organize communities in both “top‐down” (fishing of predators) and “bottom‐up” (degradation of benthic communities) contexts.     

Extinction rate, historical population structure and ecological role of the Caribbean monk seal

The productivity and biomass of pristine coral reef ecosystems is poorly understood, particularly in the Caribbean where communities have been impacted by overfishing and multiple other stressors over centuries. Using historical data on the spatial distribution and abundance of the extinct Caribbean monk seal (Monachus tropicalis), this study reconstructs the population size, structure and ecological role of this once common predator within coral reef communities, and provides evidence that historical reefs supported biomasses of fishes and invertebrates up to six times greater than those found on typical modern Caribbean reefs. An estimated 233,000-338,000 monk seals were distributed among 13 colonies across the Caribbean. The biomass of reef fishes and invertebrates required to support historical seal populations was 732-1018 gm(-2) of reefs, which exceeds that found on any Caribbean reef today and is comparable with those measured in remote Pacific reefs. Quantitative estimates of historically dense monk seal colonies and their consumption rates on pristine reefs provide concrete data on the magnitude of decline in animal biomass on Caribbean coral reefs. Realistic reconstruction of these past ecosystems is critical to understanding the profound and long-lasting effect of human hunting on the functioning of coral reef ecosystems.     

Quantifying Climatological Ranges and Anomalies for Pacific Coral Reef Ecosystems

Coral reef ecosystems are exposed to a range of environmental forcings that vary on daily to decadal time scales and across spatial scales spanning from reefs to archipelagos. Environmental variability is a major determinant of reef ecosystem structure and function, including coral reef extent and growth rates, and the abundance, diversity, and morphology of reef organisms. Proper characterization of environmental forcings on coral reef ecosystems is critical if we are to understand the dynamics and implications of abiotic–biotic interactions on reef ecosystems. This study combines high-resolution bathymetric information with remotely sensed sea surface temperature, chlorophyll-a and irradiance data, and modeled wave data to quantify environmental forcings on coral reefs. We present a methodological approach to develop spatially constrained, island- and atoll-scale metrics that quantify climatological range limits and anomalous environmental forcings across U.S. Pacific coral reef ecosystems. Our results indicate considerable spatial heterogeneity in climatological ranges and anomalies across 41 islands and atolls, with emergent spatial patterns specific to each environmental forcing. For example, wave energy was greatest at northern latitudes and generally decreased with latitude. In contrast, chlorophyll-a was greatest at reef ecosystems proximate to the equator and northern-most locations, showing little synchrony with latitude. In addition, we find that the reef ecosystems with the highest chlorophyll-a concentrations; Jarvis, Howland, Baker, Palmyra and Kingman are each uninhabited and are characterized by high hard coral cover and large numbers of predatory fishes. Finally, we find that scaling environmental data to the spatial footprint of individual islands and atolls is more likely to capture local environmental forcings, as chlorophyll-a concentrations decreased at relatively short distances (>7 km) from 85% of our study locations. These metrics will help identify reef ecosystems most exposed to environmental stress as well as systems that may be more resistant or resilient to future climate change.     

Coral reef conservation in Bali in light of international best practice,a literature review

Bali, Indonesia sits within the coral triangle and is internationally recognised for its high coral reef diversity. The health of Bali’s marine ecosystems has declined in recent decades, and this is thought to be due to threats from climate change, destructive fishing practices, pollution, outbreaks coral eating invertebrates, coral disease and unsustainable tourism. As a response, multiple conservation strategies have been introduced by the island’s communities, non-government organisations and governments, with the aim of preventing further decline, as well as restoring already degraded coral reefs. This literature review provides an in-depth analysis of the tools used to conserve Bali’s coral reefs, and compares them to those used in other countries. In light of international ‘best practice’ in coral reef conservation, this review makes suggestions on how Bali could better conserve its coral reef ecosystems. These include (1) increasing its designation of official Marine Protected Areas (MPAS) and strengthening management of existing ones, (2) creating an MPA network, (3) substantially reducing marine plastic pollution, (4) continuing artificial reef construction in degraded habitats, (5) continuing to develop Bali as an ecotourism destination, (6) increasing engagement in global science to inform marine conservation decision-making, and (7) developing more marine monitoring programmes.     

珊瑚礁生态脆弱性评价--以泰国思仓岛为例

珊瑚礁生态系统受到环境变化、人类活动等各种因素的严重威胁,保护珊瑚礁生态系统是目前全球海洋生态保护的热点,对珊瑚礁开展定量的生态脆弱性评估能够为保护管理对策的制定提供重要科学依据。本研究选取泰国思仓岛作为研究区域,结合空间分析技术建立了具有通用性的珊瑚礁生态脆弱性评估方法。基于ESA模型构建了珊瑚礁生态脆弱性综合指数和评价指标体系,系统分析了思仓岛珊瑚礁脆弱性的来源、构成,并直观展现了脆弱性的区域空间分布。结果表明:思仓岛研究区东北侧的珊瑚礁生态脆弱性大于西南侧,当地珊瑚礁的关键影响因子分别为驳船排污、港口码头、水体透明度等。根据脆弱性评价的结果,提出了当地珊瑚礁保护与修复的空间分区管理对策。本研究为印度-太平洋区系珊瑚礁生态脆弱性评价提供了可行的示例,也为中国的珊瑚礁可持续管理研究提供了借鉴和参照。     

Restricted gene flow and local adaptation highlight the vulnerability of high‐latitude reefs to rapid environmental change

Global climate change poses a serious threat to the future health of coral reef ecosystems. This calls for management strategies that are focused on maximizing the evolutionary potential of coral reefs. Fundamental to this is an accurate understanding of the spatial genetic structure in dominant reef‐building coral species. In this study, we apply a genotyping‐by‐sequencing approach to investigate genome‐wide patterns of genetic diversity, gene flow, and local adaptation in a reef‐building coral, Pocillopora damicornis, across 10 degrees of latitude and a transition from temperate to tropical waters. We identified strong patterns of differentiation and reduced genetic diversity in high‐latitude populations. In addition, genome‐wide scans for selection identified a number of outlier loci putatively under directional selection with homology to proteins previously known to be involved in heat tolerance in corals and associated with processes such as photoprotection, protein degradation, and immunity. This study provides genomic evidence for both restricted gene flow and local adaptation in a widely distributed coral species, and highlights the potential vulnerability of leading‐edge populations to rapid environmental change as they are locally adapted, reproductively isolated, and have reduced levels of genetic diversity.     

Current and future sustainability of island coral reef fisheries

Overexploitation is one of the principal threats to coral reef diversity, structure, function, and resilience [1, 2]. Although it is generally held that coral reef fisheries are unsustainable [3-5], little is known of the overall scale of exploitation or which reefs are overfished [6]. Here, on the basis of ecological footprints and a review of exploitation status [7, 8], we report widespread unsustainability of island coral reef fisheries. Over half (55%) of the 49 island countries considered are exploiting their coral reef fisheries in an unsustainable way. We estimate that total landings of coral reef fisheries are currently 64% higher than can be sustained. Consequently, the area of coral reef appropriated by fisheries exceeds the available effective area by approximately 75,000 km(2), or 3.7 times the area of Australia's Great Barrier Reef, and an extra 196,000 km(2) of coral reef may be required by 2050 to support the anticipated growth in human populations. The large overall imbalance between current and sustainable catches implies that management methods to reduce social and economic dependence on reef fisheries are essential to prevent the collapse of coral reef ecosystems while sustaining the well-being of burgeoning coastal populations.     

A global coral reef probability map generated using convolutional neural networks

Coral reef research and management efforts can be improved when supported by reef maps providing local-scale details across global extents. However, such maps are difficult to generate due to the broad geographic range of coral reefs, the complexities of relating satellite imagery to geomorphic or ecological realities, and other challenges. However, reef extent maps are one of the most commonly used and most valuable data products from the perspective of reef scientists and managers. Here, we used convolutional neural networks to generate a globally consistent coral reef probability map—a probabilistic estimate of the geospatial extent of reef ecosystems—to facilitate scientific, conservation, and management efforts. We combined a global mosaic of high spatial resolution Planet Dove satellite imagery with regional Millennium Coral Reef Mapping Project reef extents to build training, validation, and application datasets. These datasets trained our reef extent prediction model, a neural network with a dense-unet architecture followed by a random forest classifier, which was used to produce a global coral reef probability map. Based on this probability map, we generated a global coral reef extent map from a 60% threshold of reef probability (reef: probability ≥ 60%, non-reef: probability < 60%). Our findings provide a proof-of-concept method for global reef extent estimates using a consistent and readily updateable methodology that leverages modern deep learning approaches to support downstream users. These maps are openly-available through the Allen Coral Atlas.