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Coral reefs are deteriorating worldwide prompting reef managers and stakeholders to increasingly explore new management tools. Following back-to-back bleaching in 2016/2017, multi-taxa coral nurseries were established in 2018 for the first time on the Great Barrier Reef (GBR) to aid reef maintenance and restoration at a “high-value” location–Opal Reef–frequented by the tourism industry. Various coral species (n = 11) were propagated within shallow water (ca. 4-7m) platforms installed across two sites characterised by differing environmental exposure–one adjacent to a deep-water channel (Blue Lagoon) and one that was relatively sheltered (RayBan). Growth rates of coral fragments placed onto nurseries were highly variable across taxa but generally higher at Blue Lagoon (2.1–10.8 cm 2 month -1 over 12 months) compared to RayBan (0.6–6.6 cm 2 month -1 over 9 months). Growth at Blue Lagoon was largely independent of season, except for Acropora tenuis and Acropora hyacinthus , where growth rates were 15–20% higher for December 2018-July 2019 (“warm season”) compared to August-December 2018 (“cool season”). Survivorship across all 2,536 nursery fragments was ca. 80–100%, with some species exhibiting higher survivorship at Blue Lagoon ( Acropora loripes , Porites cylindrica ) and others at RayBan ( A . hyacinthus , Montipora hispida ). Parallel measurements of growth and survivorship were used to determine relative return-on-effort (RRE) scores as an integrated metric of “success” accounting for life history trade-offs, complementing the mutually exclusive assessment of growth or survivorship. RRE scores within sites (across species) were largely driven by growth, whereas RRE scores between sites were largely driven by survivorship. The initial nursery phase of coral propagation therefore appears useful to supplement coral material naturally available for stewardship of frequently visited Great Barrier Reef tourism (high-value) sites, but further assessment is needed to evaluate how well the growth rates and survival for nursery grown corals translate once material is outplanted.

The alarming rate of climate change demands new management strategies to protect coral reefs. Environments such as mangrove lagoons, characterized by extreme variations in multiple abiotic factors, are viewed as potential sources of stress-tolerant corals for strategies such as assisted evolution and coral propagation. However, biological trade-offs for adaptation to such extremes are poorly known. Here, we investigate the reef-building coral Porites lutea thriving in both mangrove and reef sites and show that stress-tolerance comes with compromises in genetic and energetic mechanisms and skeletal characteristics. We observe reduced genetic diversity and gene expression variability in mangrove corals, a disadvantage under future harsher selective pressure. We find reduced density, thickness and higher porosity in coral skeletons from mangroves, symptoms of metabolic energy redirection to stress response functions. These findings demonstrate the need for caution when utilizing stress-tolerant corals in human interventions, as current survival in extremes may compromise future competitive fitness. Corals living in naturally extreme environments such as mangrove lagoons have been considered as ‘super corals’ for reef conservation. However, this study shows that resistance in highly variable conditions comes with biological trade-offs that could compromise the suitability of these stress-tolerant corals for reef management under worsening climate change conditions.

Coral reefs are deteriorating under climate change as oceans continue to warm and acidify and thermal anomalies grow in frequency and intensity. In vitro experiments are widely used to forecast reef-building coral health into the future, but often fail to account for the complex ecological and biogeochemical interactions that govern reefs. Consequently, observations from coral communities under naturally occurring extremes have become central for improved predictions of future reef form and function. Here, we present a semi-enclosed lagoon system in New Caledonia characterised by diel fluctuations of hot-deoxygenated water coupled with tidally driven persistently low pH, relative to neighbouring reefs. Coral communities within the lagoon system exhibited high richness (number of species = 20) and cover (24–35% across lagoon sites). Calcification rates for key species ( Acropora formosa , Acropora pulchra , Coelastrea aspera and Porites lutea ) for populations from the lagoon were equivalent to, or reduced by ca . 30–40% compared to those from the reef. Enhanced coral respiration, alongside high particulate organic content of the lagoon sediment, suggests acclimatisation to this trio of temperature, oxygen and pH changes through heterotrophic plasticity. This semi-enclosed lagoon therefore provides a novel system to understand coral acclimatisation to complex climatic scenarios and may serve as a reservoir of coral populations already resistant to extreme environmental conditions.

Global climate change and localised anthropogenic stressors are driving rapid declines in coral reef health. In vitro experiments have been fundamental in providing insight into how reef organisms will potentially respond to future climates. However, such experiments are inevitably limited in their ability to reproduce the complex interactions that govern reef systems. Studies examining coral communities that already persist under naturally-occurring extreme and marginal physicochemical conditions have therefore become increasingly popular to advance ecosystem scale predictions of future reef form and function, although no single site provides a perfect analogue to future reefs. Here we review the current state of knowledge that exists on the distribution of corals in marginal and extreme environments, and geographic sites at the latitudinal extremes of reef growth, as well as a variety of shallow reef systems and reef-neighbouring environments (including upwelling and CO2 vent sites). We also conduct a synthesis of the abiotic data that have been collected at these systems, to provide the first collective assessment on the range of extreme conditions under which corals currently persist. We use the review and data synthesis to increase our understanding of the biological and ecological mechanisms that facilitate survival and success under sub-optimal physicochemical conditions. This comprehensive assessment can begin to: (i) highlight the extent of extreme abiotic scenarios under which corals can persist, (ii) explore whether there are commonalities in coral taxa able to persist in such extremes, (iii) provide evidence for key mechanisms required to support survival and/or persistence under sub-optimal environmental conditions, and iv) evaluate the potential of current sub-optimal coral environments to act as potential refugia under changing environmental conditions. Such a collective approach is critical to better understand the future survival of corals in our changing environment. We finally outline priority areas for future research on extreme and marginal coral environments, and discuss the additional management options they may provide for corals through refuge or by providing genetic stocks of stress tolerant corals to support proactive management strategies.

Background Elements are the basis of life on Earth, whereby organisms are essentially evolved chemical substances that dynamically interact with each other and their environment. Determining species elemental quotas (their elementome) is a key indicator for their success across environments with different resource availabilities. Elementomes remain undescribed for functionally diverse dinoflagellates within the family Symbiodiniaceae that includes coral endosymbionts. We used dry combustion and ICP-MS to assess whether Symbiodiniaceae (ten isolates spanning five genera Breviolum, Cladocopium, Durusdinium, Effrenium, Symbiodinium ) maintained under long-term nutrient replete conditions have unique elementomes (six key macronutrients and nine micronutrients) that would reflect evolutionarily conserved preferential elemental acquisition. For three isolates we assessed how elevated temperature impacted their elementomes. Further, we tested whether Symbiodiniaceae conform to common stoichiometric hypotheses (e.g., the growth rate hypothesis) documented in other marine algae. This study considers whether Symbiodiniaceae isolates possess unique elementomes reflective of their natural ecologies, evolutionary histories, and resistance to environmental change. Results Symbiodiniaceae isolates maintained under long-term luxury uptake conditions, all exhibited highly divergent elementomes from one another, driven primarily by differential content of micronutrients. All N:P and C:P ratios were below the Redfield ratio values, whereas C:N was close to the Redfield value. Elevated temperature resulted in a more homogenised elementome across isolates. The Family-level elementome was (C 19.8 N 2.6 P 1.0 S 18.8 K 0.7 Ca 0.1 ) · 1000 (Fe 55.7 Mn 5.6 Sr 2.3 Zn 0.8 Ni 0.5 Se 0.3 Cu 0.2 Mo 0.1 V 0.04 ) mmol Phosphorous -1 versus (C 25.4 N 3.1 P 1.0 S 23.1 K 0.9 Ca 0.4 ) · 1000 (Fe 66.7 Mn 6.3 Sr 7.2 Zn 0.8 Ni 0.4 Se 0.2 Cu 0.2 Mo 0.2 V 0.05 ) mmol Phosphorous -1 at 27.4 ± 0.4 °C and 30.7 ± 0.01 °C, respectively. Symbiodiniaceae isolates tested here conformed to some, but not all, stoichiometric principles. Conclusions Elementomes for Symbiodiniaceae diverge from those reported for other marine algae, primarily via lower C:N:P and different micronutrient expressions. Long-term maintenance of Symbiodiniaceae isolates in culture under common nutrient replete conditions suggests isolates have evolutionary conserved preferential uptake for certain elements that allows these unique elementomes to be identified. Micronutrient content (normalised to phosphorous) commonly increased in the Symbiodiniaceae isolates in response to elevated temperature, potentially indicating a common elemental signature to warming.

Organismal phenotyping to identify fitness traits is transforming our understanding of adaptive responses and ecological interactions of species within changing environments. Here we present a portable Multi-Taxa Phenotyping (MTP) system that can retrieve a suite of metabolic and photophysiological parameter across light, temperature, and/or chemical gradients, using real time bio-optical (oxygen and chlorophyll a fluorescence) measurements. The MTP system integrates three well-established technologies for the first time: an imaging Pulse Amplitude Modulated (PAM) chlorophyll a fluorometer, custom-designed well plates equipped with optical oxygen sensors, and a thermocycler. We demonstrate the ability of the MTP system to distinguish phenotypic performance characteristics of diverse aquatic taxa spanning corals, mangroves and algae based on metabolic parameters and Photosystem II dynamics, in a high-throughput capacity and accounting for interactions of different environmental gradients on performance. Extracted metrics from the MTP system can not only provide information on the performance of aquatic taxa exposed to differing environmental gradients, but also provide predicted phenotypic responses of key aquatic organisms to environmental change. Further work validating how rapid phenotyping tools such as the MTP system predict phenotypic responses to long term environmental changes in situ are urgently required to best inform how these tools can support management efforts.

Restoration supports the recovery of ecological attributes such as cover, complexity, and diversity to slow the areal decline of natural ecosystems. Restoration activity is intensifying worldwide to combat persistent stressors that are driving global declines to the extent and resilience of coral reefs. However, restoration is disputed as a meaningful aid to reef ecological recovery, often as an expensive distraction to addressing the root causes of reef loss. We contend this dispute partly stems from inferences drawn from small-scale experimental restoration outcomes amplified by misconceptions around cost-based reasoning. Alongside aggressive emissions reductions, we advocate urgent investment in coral reef ecosystem restoration as part of the management toolbox to combat the destruction of reefs as we know them within decades.

Symbiodiniaceae form associations with extra- and intracellular bacterial symbionts, both in culture and in symbiosis with corals. Bacterial associates can regulate Symbiodiniaceae fitness in terms of growth, calcification and photophysiology. However, the influence of these bacteria on interactive stressors, such as temperature and light, which are known to influence Symbiodiniaceae physiology, remains unclear. Here, we examined the photophysiological response of two Symbiodiniaceae species ( Symbiodinium microadriaticum and Breviolum minutum ) cultured under acute temperature and light stress with specific bacterial partners from their microbiome ( Labrenzia ( Roseibium ) alexandrii , Marinobacter adhaerens or Muricauda aquimarina ). Overall, bacterial presence positively impacted Symbiodiniaceae core photosynthetic health (photosystem II [PSII] quantum yield) and photoprotective capacity (non-photochemical quenching; NPQ) compared to cultures with all extracellular bacteria removed, although specific benefits were variable across Symbiodiniaceae genera and growth phase. Symbiodiniaceae co-cultured with M. aquimarina displayed an inverse NPQ response under high temperatures and light, and those with L. alexandrii demonstrated a lowered threshold for induction of NPQ, potentially through the provision of antioxidant compounds such as zeaxanthin (produced by Muricauda spp . ) and dimethylsulfoniopropionate (DMSP; produced by this strain of L. alexandrii ). Our co-culture approach empirically demonstrates the benefits bacteria can deliver to Symbiodiniaceae photochemical performance, providing evidence that bacterial associates can play important functional roles for Symbiodiniaceae.

Coral restoration efforts have rapidly increased worldwide, including the development of several programmes on the Great Barrier Reef (GBR) in recent years. While many restoration programmes utilise in-water nurseries to accelerate coral biomass yields, the impact of nursery environments on propagule quality has not been examined despite the importance of coral fitness for ensuring resistant populations. Here, we investigated two fitness indicators (lipid diversity and tissue protein abundance) of Acropora millepora adults and eggs grown on coral nurseries versus native reef on the GBR, with adults assessed at two sites (Blue Lagoon and Rayban) and eggs assessed at one site (Blue Lagoon). Lipid profiles of adult colonies varied by site and origin (nursery versus wild reef), with adult nursery corals exhibiting an elevated relative abundance of storage lipids (diacylglycerols and triacylglycerols) and lipid classes responsible for regulating membrane structure (phosphatidylcholines and sterol esters), while wild corals were characterised by a greater relative abundance of fatty acids and classes involved in immunoregulation. Comparing eggs from different origins, nursery offspring were richer in energy-storing triacylglycerols, as well as ceramides and phosphatidylcholines essential for membrane structure, while wild eggs had a greater relative abundance of wax ester species also important for energy storage. No differences were found in total protein abundance (adult or eggs) or egg physical characteristics (count and size) between nursery and wild origins. Variations in lipid profiles are consistent with differences in environmental conditions between reef sites and origin (nursery versus wild), highlighting the need to consider site selection and propagation conditions when planning restoration projects. Importantly, these findings demonstrate that the lipid classes with the highest relative abundance in A. millepora nursery and wild eggs differed from those in adults from the same origin, suggesting that propagation origin is more important for driving lipid profiles in coral eggs compared to parental effects.