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Photogrammetry is a common tool for evaluating ecosystem-scale questions on coral reefs due to the ability to measure complex structures in situ. This technique is also increasingly being used at smaller scales to collect growth and morphometric data about individual coral fragments in manipulative experiments. However, there are substantial uncertainties in data quality and interpretation and limited reporting of the parameters useful for standardization across studies. There is a need to characterize the capabilities of photogrammetry as applied to coral fragments, to establish validation metrics for reporting, and to determine sources of variation in measurements to refine and improve methods. Here, we used fragments of two common reef-building corals (Montipora capitata and Porites compressa) and known size standards to evaluate accuracy and precision and present suggested validation metrics. We also used a tiered experimental design to evaluate sources of error in a photogrammetry workflow in a manipulative experiment using a purpose-built multi-camera workstation. We demonstrate extremely high accuracy (R2 > 0.999) in determining the surface area and volume of known objects, as well as very high precision (average CV < 0.01) in coral measurements during tests of reproducibility. These outcomes show the utility of fragment photogrammetry for experimental coral reef science and present suggested validation metrics and approaches that can help standardize data evaluation and interpretation in any application of photogrammetry to coral fragments.

Abstract All biology happens in space, and spatial structuring plays an important role in mediating biological processes at all scales from cells to ecosystems. However, the metabolomic structuring of the coral holobiont has yet to be fully explored. Here, we present a method to detect high-quality metabolomic data from individual coral polyps and apply this method to study the patterning of biochemicals across multiple spatial (~1 mm - ~100 m) and organizational scales (polyp to population). The data show a strong signature for individual coral colonies, a weaker signature of branches within colonies, and variation at the polyp level related to the polyps’ location along a branch. Mapping metabolites to either the coral or algal components of the holobiont reveals that polyp-level variation along the length of a branch was largely driven by molecules associated with the cnidarian host as opposed to the algal symbiont, predominantly putative sulfur-containing metabolites. This work yields insights on the spatial structuring of biochemicals in the coral holobiont, which is critical for design, analysis, and interpretation of studies on coral reef biochemistry.

Abstract Coral reefs are iconic examples of climate change impacts because climate-induced heat stress causes the breakdown of the coral-algal symbiosis leading to a spectacular loss of color, termed ‘coral bleaching’. To examine the fine-scale dynamics of this process, we re-sampled 600 individually marked Montipora capitata colonies from across Kāne’ohe Bay, Hawai’i and compared the algal symbiont composition before and after the 2019 bleaching event. The relative proportion of the heat-tolerant symbiont Durusdinium in corals increased in most parts of the bay following the bleaching event. Despite this widespread increase in abundance of Durusdinium, the overall algal symbiont community composition was largely unchanged, and hydrodynamically defined regions of the bay retained their distinct pre-bleaching compositions. We explain ~ 21% of the total variation, of which depth and temperature variability were the most significant environmental drivers of Symbiodiniaceae community composition by site regardless of bleaching intensity or change in relative proportion of Durusdinium. We hypothesize that the plasticity of symbiont composition in corals may be constrained to adaptively match the long-term environmental conditions surrounding the holobiont, despite an individual coral’s stress and bleaching response.

The biodiversity of coral reef habitats is rapidly declining due to the effects of anthropogenic climate change, prompting the use of active restoration as a mitigation strategy. Sexual propagation can maintain or enhance genetic diversity in restoration of these ecosystems, but these approaches suffer from a range of inefficiencies in rearing and husbandry. Algal overgrowth of juveniles is a major bottleneck in the production of sexually propagated corals that may be alleviated by co-culture with herbivores. We reared juvenile Montipora capitata alongside juvenile native Hawaiian collector urchins, Tripneustes gratilla, for 15 weeks and documented significant ecological benefits of co-culture. Urchin treatments significantly increased the survivorship of coral aggregates (14%) and individual settlers (24%). We also documented a significant increase in coral growth in the presence of urchins. These results demonstrate the utility of microherbivory in promoting coral growth and survivorship in ex situ conditions, providing valuable insight for restoration pipelines of native Hawaiian coral species.

Corals are habitat-forming organisms on tropical and sub-tropical reefs, often displaying diverse phenotypic behaviors that challenge field-based monitoring and assessment efforts. Symbiont chlorophyll (Chl) is a long-recognized indicator of intra- and inter-specific variation in coral’s response to environmental variability and stress, but the quantitative Chl assessment of corals at the reef scale continues to prove challenging. We integrated field, airborne, and laboratory techniques to test and apply the use of reflectance spectroscopy for in situ and reef-scale estimation of Chl a and Chl c2 concentrations in a shallow reef environment of Kāne‘ohe Bay, O‘ahu. High-fidelity spectral signatures (420–660 nm) derived from field and airborne spectroscopy quantified Chl a and Chl c2 concentrations with demonstrable precision and accuracy. Airborne imaging spectroscopy revealed a 10-fold range of Chl concentrations across the reef ecosystem. We discovered a differential pattern of Chl a and Chl c2 use in symbiont algae in coexisting corals indicative of a physiological response to decreasing light levels with increasing water depth. The depth-dependent ratio of Chl c2:a indicated the presence of two distinct light-driven habitats spanning just 5 m of water depth range. Our findings provide a pathway for further study of coral pigment responses to environmental conditions using field and high-resolution airborne imaging spectroscopy.

Phenotypic plasticity is an important response for organisms experiencing climate change. Here, Drury et al. show that stress-hardening can produce durable improvements in coral thermal tolerance, masking substantial variation between individuals.

Abstract Coral bleaching, precipitated by the expulsion of the algal symbionts that provide colonies with fixed carbon is a global threat to reef survival. To protect corals from anthropogenic stress, portable tools are needed to detect and diagnose stress syndromes and assess population health prior to extensive bleaching. Here, medical grade Urinalysis strips, used to detect an array of disease markers in humans, were tested on the lab stressed Hawaiian coral species, Montipora capitata (stress resistant) and Pocillopora acuta (stress sensitive), as well as samples from nature that also included Porites compressa. Of the 10 diagnostic reagent tests on these strips, two appear most applicable to corals: ketone and leukocytes. The test strip results from M. capitata were explored using existing transcriptomic data from the same samples and provided evidence of the stress syndromes detected by the strips. We designed a 3D printed smartphone holder and image processing software for field analysis of test strips (TestStripDX) and devised a simple strategy to generate color scores for corals (reflecting extent of bleaching) using a smartphone camera (CoralDX). Our approaches provide field deployable methods, that can be improved in the future (e.g., coral-specific stress test strips) to assess reef health using inexpensive tools and freely available software.

Coral bleaching and mortality can show significant spatial and taxonomic heterogeneity at local scales, highlighting the need to understand the fine-scale drivers and impacts of thermal stress. In this study, we used structure-from-motion photogrammetry to track coral bleaching, mortality, and changes in community composition during the 2019 marine heatwave in Kāneʻohe Bay, Hawaiʻi. We surveyed 30 shallow reef patches every 3 weeks for the duration of the bleaching event (August-December) and one year after, resulting in a total of 210 large-area, high-resolution photomosaics that enabled us to follow the fate of thousands of coral colonies through time. We also measured environmental variables such as temperature, sedimentation, depth, and wave velocity at each of these sites, and extracted estimates of habitat complexity (rugosity R and fractal dimension D) from digital elevation models to better understand their effects on patterns of bleaching and mortality. We found that up to 80% of corals experienced moderate to severe bleaching in this period, with peak bleaching occurring in October when heat stress (Degree Heating Weeks) reached its maximum. Mortality continued to accumulate as bleaching levels dropped, driving large declines in more heat-susceptible species (77% loss of Pocillopora cover) and moderate declines in heat-tolerant species (19% and 23% for Porites compressa and Montipora capitata, respectively). Declines in live coral were accompanied by a rapid increase in algal cover across the survey sites. Spatial differences in bleaching were significantly linked to habitat complexity and coral species composition, with reefs that were dominated by Pocillopora experiencing the most severe bleaching. Mortality was also influenced by species composition, fractal dimension, and site-level differences in thermal stress. Our results show that spatial heterogeneity in the impacts of bleaching are driven by a mix of environmental variation, habitat complexity, and differences in assemblage composition.

Selective breeding of corals with different bleaching phenotypes demonstrates the potential for climate adaptation in vertically transmitting species.

Corals form symbiotic relationships with dinoflagellate algae of the family Symbiodiniaceae, bacteria, and other microbes. Central to that relationship is the regulation of nutrition flux between the animal host and the photosynthetic Symbiodiniaceae that it is reliant on for the majority of metabolic needs. Nitrogen availability controls the growth and density of Symbiodiniaceae within coral tissues and has been proposed to play a role in host derived symbiosis regulation. Warming ocean temperatures and subsequent increases in dissolved organic carbon can potentially increase nitrogen fixation and lead to bleaching. We investigated the importance of nitrogen metabolism in vivo with LC-MS based stable isotope tracing using nubbins from three species of Hawaiian coral, the more heat tolerant Montipora capitata and Porites compressa and the more heat sensitive Pocillopora acuta, that were collected from reefs in Kāne’ohe Bay, O’ahu. In addition to 15N incorporation into nucleotides, amino acids, and urea cycle metabolites, we also observed significant isotopic labeling in dipeptides, supporting their previous identification as major heat stress response metabolites. Surprisingly, the dipeptides are highly enriched in 15N compared to free amino acids, which are the biosynthetic precursors for dipeptides. This suggests that there is a high turnover of dipeptide pools and distinct biosynthetic mechanisms that separately mediate amino acid and dipeptide production. These preliminary data show that nitrogen assimilation in the coral holobiont is likely compartmentalized, with rapid assimilation and quick dipeptide turnover occurring in one region of the holobiont and slow turnover of other nitrogen containing metabolites in other region(s).

Global coral reef decline is largely driven by the breakdown of the coral-algal symbiosis during temperature stress. Corals can acclimatize to higher temperatures, but the cellular processes underlying this ability are poorly understood. We show that preconditioning-based improvements in thermal tolerance in Pocillopora acuta are accompanied by increases in host glutathione reductase (GR) activity and gene expression, which prevents DNA damage. A strong correlation between GR and BI-1 expressions in heat-stressed preconditioned corals and the presence of an antioxidant response element (ARE) in the GR promoter suggest BI-1 could regulate GR expression through Nrf2/ARE pathway. To fortify this link, we developed and GFP-validated an siRNA-mediated gene knockdown protocol and targeted the coral BI-1 gene. BI-1 knock-down specifically decreased GR expression and activity and increased oxidative DNA damage in heat-stressed preconditioned corals, showing that a BI-1-mediated, enhanced antioxidant response during acute heat stress is a key mechanism that prevents oxidative DNA damage after preconditioning.

The survival of most reef-building corals is dependent upon a symbiosis between the coral and the community of Symbiodiniaceae. Montipora capitata, one of the main reef-building coral species in Hawai'i, is known to host a diversity of symbionts, but it remains unclear how they change spatially and whether environmental factors drive those changes. Here, we surveyed the Symbiodiniaceae community in 600 M. capitata colonies from 30 sites across Kāne'ohe Bay and tested for host specificity and environmental gradients driving spatial patterns of algal symbiont distribution. We found that the Symbiodiniaceae community differed markedly across sites, with M. capitata in the most open-ocean (northern) site hosting few or none of the genus Durusdinium, whereas individuals at other sites had a mix of Durusdinium and Cladocopium. Our study shows that the algal symbiont community composition responds to fine-scale differences in environmental gradients; depth and temperature variability were the most significant predictor of Symbiodiniaceae community, although environmental factors measured in the study explained only about 20% of observed variation. Identifying and mapping Symbiodiniaceae community distribution at multiple scales is an important step in advancing our understanding of algal symbiont diversity, distribution and evolution and the potential responses of corals to future environmental change.

Coral reefs are threatened by climate change, overfishing, and pollution. Artificial reefs may provide havens for corals, both to escape warming surface waters and to assist in the geographic migration of corals to more habitable natural reef conditions of the future. The largest artificial reefs have been generated by nearly 2000 shipwrecks around the world, but the coral diversity on these wrecks is virtually unknown. Ship size and hull material, location relative to natural reef, time since sinking, ocean currents, and water depth may affect coral diversity. As a test of the biodiversity capacity of very large sunken structures relative to surrounding natural reef, we carried out technical diver-based surveys to quantify genus-level coral diversity on 29 warships sunk in Bikini Atoll and Chuuk Lagoon. We also assessed whether ship length, as an index of substrate availability, and water depth, as an indicator of light and temperature, can serve as predictors of coral diversity. We surveyed a total of 9105 scleractinian corals. The total number of genera identified at Bikini was 34, and at Chuuk it was 51, representing 67% and 72% of genera found on natural reefs at Bikini and Chuuk, respectively. Ship length, but not water depth, was positively correlated with relative abundance and richness at the genus level. Our results suggest that very large wrecks can serve as havens for reef-building corals with a broad genetic diversity, expressed at the genus level, commensurate with corals found on neighboring natural reefs. The role of large artificial reefs could include protecting coral biodiversity from warming surface waters.