ReScape: transforming coral-reefscape images for quantitative analysis.

Ever since the first image of a coral reef was captured in 1885, people worldwide have been accumulating images of coral reefscapes that document the historic conditions of reefs. However, these innumerable reefscape images suffer from perspective distortion, which reduces the apparent size of distant taxa, rendering the images unusable for quantitative analysis of reef conditions. Here we solve this century-long distortion problem by developing a novel computer-vision algorithm, ReScape, which removes the perspective distortion from reefscape images by transforming them into top-down views, making them usable for quantitative analysis of reef conditions. In doing so, we demonstrate the first-ever ecological application and extension of inverse-perspective mapping-a foundational technique used in the autonomous-driving industry. The ReScape algorithm is composed of seven functions that (1) calibrate the camera lens, (2) remove the inherent lens-induced image distortions, (3) detect the scene's horizon line, (4) remove the camera-roll angle, (5) detect the transformable reef area, (6) detect the scene's perspective geometry, and (7) apply brute-force inverse-perspective mapping. The performance of the ReScape algorithm was evaluated by transforming the perspective of 125 reefscape images. Eighty-five percent of the images had no processing errors and of those, 95% were successfully transformed into top-down views. ReScape was validated by demonstrating that same-length transects, placed increasingly further from the camera, became the same length after transformation. The mission of the ReScape algorithm is to (i) unlock historical information about coral-reef conditions from previously unquantified periods and localities, (ii) enable citizen scientists and recreational photographers to contribute reefscape images to the scientific process, and (iii) provide a new survey technique that can rigorously assess relatively large areas of coral reefs, and other marine and even terrestrial ecosystems, worldwide. To facilitate this mission, we compiled the ReScape algorithm into a free, user-friendly App that does not require any coding experience. Equipped with the ReScape App, scientists can improve the management and prediction of the future of coral reefs by uncovering historical information from reefscape-image archives and by using reefscape images as a new, rapid survey method, opening a new era of coral-reef monitoring.

Increasing comparability among coral bleaching experiments.

Coral bleaching is the single largest global threat to coral reefs worldwide. Integrating the diverse body of work on coral bleaching is critical to understanding and combating this global problem. Yet investigating the drivers, patterns, and processes of coral bleaching poses a major challenge. A recent review of published experiments revealed a wide range of experimental variables used across studies. Such a wide range of approaches enhances discovery, but without full transparency in the experimental and analytical methods used, can also make comparisons among studies challenging. To increase comparability but not stifle innovation, we propose a common framework for coral bleaching experiments that includes consideration of coral provenance, experimental conditions, and husbandry. For example, reporting the number of genets used, collection site conditions, the experimental temperature offset(s) from the maximum monthly mean (MMM) of the collection site, experimental light conditions, flow, and the feeding regime will greatly facilitate comparability across studies. Similarly, quantifying common response variables of endosymbiont (Symbiodiniaceae) and holobiont phenotypes (i.e., color, chlorophyll, endosymbiont cell density, mortality, and skeletal growth) could further facilitate cross-study comparisons. While no single bleaching experiment can provide the data necessary to determine global coral responses of all corals to current and future ocean warming, linking studies through a common framework as outlined here, would help increase comparability among experiments, facilitate synthetic insights into the causes and underlying mechanisms of coral bleaching, and reveal unique bleaching responses among genets, species, and regions. Such a collaborative framework that fosters transparency in methods used would strengthen comparisons among studies that can help inform coral reef management and facilitate conservation strategies to mitigate coral bleaching worldwide.

A global analysis of coral bleaching over the past two decades.

Thermal-stress events associated with climate change cause coral bleaching and mortality that threatens coral reefs globally. Yet coral bleaching patterns vary spatially and temporally. Here we synthesize field observations of coral bleaching at 3351 sites in 81 countries from 1998 to 2017 and use a suite of environmental covariates and temperature metrics to analyze bleaching patterns. Coral bleaching was most common in localities experiencing high intensity and high frequency thermal-stress anomalies. However, coral bleaching was significantly less common in localities with a high variance in sea-surface temperature (SST) anomalies. Geographically, the highest probability of coral bleaching occurred at tropical mid-latitude sites (15-20 degrees north and south of the Equator), despite similar thermal stress levels at equatorial sites. In the last decade, the onset of coral bleaching has occurred at significantly higher SSTs (∼0.5 °C) than in the previous decade, suggesting that thermally susceptible genotypes may have declined and/or adapted such that the remaining coral populations now have a higher thermal threshold for bleaching.

Author Correction: Some coral diseases track climate oscillations in the Caribbean.

A correction to this article has been published and is linked from the HTML and PDF versions of this paper. The error has not been fixed in the paper.

Some coral diseases track climate oscillations in the Caribbean.

Disease outbreaks continue to reduce coral populations worldwide. Understanding coral diseases and their relationships with environmental drivers is necessary to forecast disease outbreaks, and to predict future changes in coral populations. Yet, the temporal dynamics of coral diseases are rarely reported. Here we evaluate trends and periodicities in the records of three common coral diseases (white-band disease, yellow-band disease, and dark-spot syndrome) that were surveyed between 1997 and 2014 at 2082 sites throughout the Caribbean. The relationship between the periodicities of disease prevalence and El Niño Southern Oscillation (ENSO) cycles was examined using cross-wavelet analyses and convergent cross mapping (CCM). The prevalence of the diseases peaked every two to four years, and matched periodicities in ENSO conditions. CCM models suggested that environmental conditions associated with recent ENSO cycles may have influenced the patterns in disease prevalence. We also found no increasing trends in disease prevalence through time. Instead, our work suggests that the prevalence of coral diseases is dynamic and complex. The gradual increase in sea-surface temperature, a consequence of increasing greenhouse gas emissions, progressively raises the modal temperature threshold of each ENSO cycle. These dynamic cycles and the increasing modal temperatures appear to influence the dynamics of coral diseases.

Coral benchmarks in the center of biodiversity.

There is an urgent need to quantify coral reef benchmarks that assess changes and recovery rates through time and serve as goals for management. Yet, few studies have identified benchmarks for hard coral cover and diversity in the center of marine diversity. In this study, we estimated coral cover and generic diversity benchmarks on the Tubbataha reefs, the largest and best-enforced no-take marine protected area in the Philippines. The shallow (2-6m) reef slopes of Tubbataha were monitored annually, from 2012 to 2015, using hierarchical sampling. Mean coral cover was 34% (σ±1.7) and generic diversity was 18 (σ±0.9) per 75m by 25m station. The southeastern leeward slopes supported on average 56% coral cover, whereas the northeastern windward slopes supported 30%, and the western slopes supported 18% coral cover. Generic diversity was more spatially homogeneous than coral cover.

Keep up or drown: adjustment of western Pacific coral reefs to sea-level rise in the 21st century.

Since the Mid-Holocene, some 5000 years ago, coral reefs in the Pacific Ocean have been vertically constrained by sea level. Contemporary sea-level rise is releasing these constraints, providing accommodation space for vertical reef expansion. Here, we show that Porites microatolls, from reef-flat environments in Palau (western Pacific Ocean), are 'keeping up' with contemporary sea-level rise. Measurements of 570 reef-flat Porites microatolls at 10 locations around Palau revealed recent vertical skeletal extension (78±13 mm) over the last 6-8 years, which is consistent with the timing of the recent increase in sea level. We modelled whether microatoll growth rates will potentially 'keep up' with predicted sea-level rise in the near future, based upon average growth, and assuming a decline in growth for every 1°C increase in temperature. We then compared these estimated extension rates with rates of sea-level rise under four Representative Concentration Pathways (RCPs). Our model suggests that under low-mid RCP scenarios, reef-coral growth will keep up with sea-level rise, but if greenhouse gas concentrations exceed 670 ppm atmospheric CO2 levels and with +2.2°C sea-surface temperature by 2100 (RCP 6.0 W m(-2)), our predictions indicate that Porites microatolls will be unable to keep up with projected rates of sea-level rise in the twenty-first century.

Relationships between the history of thermal stress and the relative risk of diseases of Caribbean corals.

The putative increase in coral diseases in the Caribbean has led to extensive declines in coral populations. Coral diseases are a consequence of the complex interactions among the coral hosts, the pathogens, and the environment. Yet, the relative influence that each of these components has on the prevalence of coral diseases is unclear. Also unknown is the extent to which historical thermal-stress events have influenced the prevalence of contemporary coral diseases and the potential adjustment of coral populations to thermal stress. We used a Bayesian approach to test the hypothesis that in 2012 the relative risk of four signs of coral disease (white signs, dark spots, black bands, and yellow signs) differed at reef locations with different thermal histories. We undertook an extensive spatial study of coral diseases at four locations in the Caribbean region (10(3) km), two with and two without a history of frequent thermal anomalies (approximately 4-6 years) over the last 143 years (1870-2012). Locations that historically experienced frequent thermal anomalies had a significantly higher risk of corals displaying white signs, and had a lower risk of corals displaying dark spots, than locations that did not historically experience frequent thermal anomalies. By contrast, there was no relationship between the history of thermal stress and the relative risk of corals displaying black bands and yellow signs, at least at the spatial scale of our observations.

Coral immunology and resistance to disease.

Scleractinian corals (phylum Cnidaria, class Anthozoa) have innate immunological responses against infections. Research has recently suggested that corals also possess an adaptive-like immunological repertoire that recognizes specific pathogens and allografts. While evolutionarily distinct, the corals' innate and adaptive-like immunity systems are not mutually exclusive because the phagocytic cells of the non-specific, innate immune system may activate specific adaptive immunological responses. Warming oceans may immunocompromise coral hosts, making them more susceptible to tropical marine diseases, independent of the virulence of the pathogen. The ability of corals to ward off both primary and opportunistic infections, through adaptive-like mechanisms, may play a critical role in the corals' ability to fight future disease infection. Here we show evidence that corals possess immunological repertoires that extend well beyond simple innate defenses. The extent to which corals have developed such an adaptive-like immune repertoire will determine whether corals will survive climate change and other anthropogenic disturbances.

Calm before the spawn: global coral spawning patterns are explained by regional wind fields.

Most corals in tropical localities broadcast their gametes into the water column, yet we have a poor understanding of what forces reproductive schedules. Moreover, recent studies show considerable geographical variation in the duration of the coral spawning season. For example, on the Great Barrier Reef, corals display tight coupling, while corals in Kenya spawn over seven months. This study reconciles the regional variance by testing the hypothesis that regional wind fields are the corals' ultimate reproductive proxy. Regions with short calm periods should be more tightly coupled than regions with calm periods extending for several months. Regional wind fields were assessed at seven localities, between 1997 and 2006, using the 11 GHz channel radiometer tropical microwave imager (TMI) onboard the tropical rainfall measuring mission (TRMM). There was a direct positive relationship between the duration of regional calm periods and the coupling of mass coral spawning. Ultimate long-term evolutionary advantages of releasing gametes during calm periods ensure fertilization and facilitate larval retention and local recruitment. Coupling mass spawning with seasonally calm periods agrees strongly with recent genetic evidence of local dispersal and high local retention.

Corals escape bleaching in regions that recently and historically experienced frequent thermal stress.

The response of coral-reef ecosystems to contemporary thermal stress may be in part a consequence of recent or historical sea-surface temperature (SST) variability. To test this hypothesis, we examined whether: (i) there was a relationship between the historical frequency of SST variability and stress experienced during the most recent thermal-stress events (in 1998 and 2005-2006) and (ii) coral reefs that historically experienced frequent thermal anomalies were less likely to experience coral bleaching during these recent thermal-stress events. Examination of nine detrended coral delta(18)O and Sr/Ca anomaly records revealed a high- (5.7-year) and low-frequency (>54-year) mode of SST variability. There was a positive relationship between the historical frequency of SST anomalies and recent thermal stress; sites historically dominated by the high-frequency mode experienced greater thermal stress than other sites during both events, and showed extensive coral bleaching in 1998. Nonetheless, in 2005-2006, corals at sites dominated by high-frequency variability showed reduced bleaching, despite experiencing high thermal stress. This bleaching resistance was most likely a consequence of rapid directional selection that followed the extreme thermal event of 1998. However, the benefits of regional resistance could come at the considerable cost of shifts in coral species composition.

Acclimation effect on fatty acids of the coral Montipora digitata and its symbiotic algae.

Lipids play a key role in thermal and photo-acclimation processes, yet they are often neglected in stress studies. We investigated the influence of different light intensities and an increase of temperature on the fatty acid composition of the coral Montipora digitata and its symbiotic algae (i.e., zooxanthellae). Coral branches were subjected to 3 different light intensities (7, 30 and 95% sea surface photosynthetic active radiation) in filtered seawater for 35 days. Fatty acids as methyl esters were determined using gas chromatography (GC) and verified by GC-mass spectrometry. Different light intensities, but only in combination with increased temperature, significantly affected the fatty acid composition of the coral host and zooxanthellae. Temperature and light intensity increases caused reductions in the proportion of polyunsaturated fatty acids in both the host and symbionts. Most changes occurred in the host coral, which suggests that the host is more susceptible to environmental change than the symbiont, or that the host shields the symbionts from environmental change.

Annual cycles of solar insolation predict spawning times of Caribbean corals.

Seasonal increases in sea surface temperature (SST) have long been considered the trigger for mass spawning events in reef corals. We critically examined the relationship between SST and the spawning activity of broadcasting corals in the tropical western Atlantic (Caribbean). This meta-analysis examined 12 species of broadcasting corals at 25 sites spanning 22 degrees of latitude (10 degrees-32 degrees N) from Venezuela to Bermuda in the Atlantic Ocean from 1986 to 2004. Sigmoidal logit regression models were used to examine the relationship between the release of reef-coral gametes and the environmental variables SST and solar insolation defined as (1) the cumulative response 7-10 months prior to spawning (integral); (2) the rate of change at the time of spawning (derivative); and (3) the average for the month of spawning. The Quasi-Newton method was used to estimate the maximum likelihood of the response function. We demonstrate that the recent history and rate of change in temperature correlate poorly with the timing of spawning, while the average temperature during the month of spawning was significant (with all corals releasing gametes 28-30 degrees C, except Montastraea annularis, which released gametes at 27-30 degrees C). In contrast, the rate of change and the cumulative response of solar insolation cycles was a better predictor of gamete release, but solar insolation intensity at the time of spawning was not. These models have important implications for predicting coral reproductive cycles in all oceans, and for examining other marine phototrophic systems beyond corals.

Monokaryotic chloroplast mutation has no effect on non-Mendelian transmission of chloroplast and mitochondrial DNA in Chlamydomonas species.

We studied whether the monokaryotic chloroplast (moc) mutation affects the transmission of chloroplast and mitochondrial DNA in Chlamydomonas species. We used a previously isolated moc mutant from our cell line G33, which had only one large chloroplast nucleus. To obtain zygotes, we crossed the mutant cells with wild-type cells, and mutant cells with receptive mates (females [mt+] with males [mt-]). In these zygotes, we recorded preferential dissolution of mt- parental chloroplast nuclei and fusion of the two cell nuclei. Antibiotic-resistance markers of chloroplast DNA were maternally transmitted in all crosses. PCR analysis of the cytochrome b (cob) gene sequence showed that the mitochondrial DNA was paternally transmitted to offspring. These results suggest that the moc mutation did not affect the organelle DNA transmission.

Symbiotic zooxanthellae provide the host-coral Montipora digitata with polyunsaturated fatty acids.

We compared the fatty acid composition of the host-coral Montipora digitata with the fatty acid composition in the coral's endosymbiotic dinoflagellates (zooxanthellae). Fatty acids as methyl esters were determined using gas chromatography (GC) and verified by GC-mass spectrometry. We found the main difference between the fatty acids in the host and their symbionts were that zooxanthellae supported higher proportions of polyunsaturated fatty acids. The presence of fatty acids specific to dinoflagellates (i.e. 18:4omega3, 22:5omega3 and 22:6omega3) in the host tissue suggests that zooxanthellae provide the coral host not only with saturated fatty acids, but also with diverse polyunsaturated fatty acids.

Strict paternal transmission of mitochondrial DNA of Chlamydomonas species is explained by selection against maternal nucleoids.

The non-Mendelian inheritance of organelle DNA is common in most plants and animals. Here we examined inheritance mechanisms involved in the transfer of mitochondrial DNA. We successively backcrossed (to F(5)) two interfertile strains of the unicellular isogamous haploid algae Chlamydomonas reinhardtii and Chlamydomonas smithii to match nuclear backgrounds and examine transmission patterns of mitochondrial DNA by PCR analysis of cob gene sequences. Mitochondrial DNA was strictly transmitted paternally. To investigate the behavior of parental mitochondrial DNA, we used F(5) progeny to form zygotes and isolated single zygotes. The results showed selective disappearance of maternal mitochondrial nucleoids occurred between 3 and 6 h after zygote formation.

Separation of highly fluorescent proteins by SDS-PAGE in Acroporidae corals.

This study characterized the spectral properties of Acropora tenuis, A. nasuta, A. secale, and A. aspera, all of which showed strong colorful fluorescence under ultraviolet light-A (black light). The emission maxima of fluorescence from the intact corals were 517, 482, 484, and 514 nm in A. tenuis, A. nasuta, A. secale, and A. aspera, respectively. Using a soluble fraction of cell-free extract of the corals, we applied a method of sodium dodecyl sulfate polyacrylamide gel electrophoresis (SDS-PAGE) to separate each fluorescent protein component contained in the corals. Green fluorescent bands were detected in all Acropora examined, although their apparent molecular mass and relative content were different. A. aspera had two orange bands in addition to the green one. The major excitation and emission peaks of the orange fluorescence bands were almost identical (476 and 478 nm), however, they were discernible by their spectral profiles and molecular masses. Some biochemical properties of the highly fluorescent proteins of Acropora are described and implications of the results are discussed.

Spatial and temporal variance of river discharge on Okinawa (Japan): inferring the temporal impact on adjacent coral reefs.

Land-use changes and associated river discharges in coastal tropical regions present a global threat to coral reef environments. This study investigated the temporal variation in biological oxygen demand (BOD5) and suspended particulate matter (SPM) at the mouths of seven rivers on Okinawa Island (Japan) over 20 years. We report strong positive relationships between human population densities within river catchment areas and both average BOD5 concentration (r2 = 0.968; p < 0.001) and SPM (r2 = 0.659; p < 0.003) at the mouths of the rivers. At the reef adjacent to one river (Hija River, 50.2 km2 catchment area) we applied moving window analysis to assess an optimal sampling strategy for elucidating transitional boundaries in coral composition from the river mouth to a point where the effect of river discharge was minimal. The optimal window width for Okinawan rivers was five 1 m2 quadrats spaced over 5 m intervals. This sampling strategy clearly showed dissimilarity spikes in coral community composition up to 400 m from the Hija River mouth, beyond which no significant differences in coral composition were detected using analysis of similarities (ANOSIM). We developed a simple diffusion model linking the rivers' maximum discharge rate, and the average concentration of BOD5 and SPM with the spatial impact on the coral communities. The diffusion model can aid in predicting negative shifts in coral communities expected to result from detrimental land-use changes and is an important tool for monitoring coral reefs.

Photo-acclimation of the hermatypic coral Stylophora pistillata while subjected to either starvation or food provisioning.

This study investigated the photo-acclimation capacity of the coral Stylophora pistillata (Esper). Outer branches of coral colonies, taken from 2 m, were subjected to 90, 20, or 3% of incident surface photosynthetic active radiation (PAR(0)), or kept in total darkness. The corals were maintained either in filtered seawater (i.e., under starvation), or in seawater that had daily additions of zooplankton (rotifers). The experiments were maintained for 31 days. Zooxanthellae population densities and chlorophyll concentrations increased in S. pistillata fragments subjected to 20 and 3% PAR(0). The zooxanthellae densities decreased after 6 days in corals kept in total darkness, although chlorophyll concentrations remained higher. Corals that were fed and subjected to 90% PAR(0) showed lower degrading zooxanthellae frequencies, higher photosynthetic and respiration rates, and higher chlorophyll concentrations than corals in the same light regime under starvation. Complete acclimation to dim (20% PAR(0)) and low (3% PAR(0)) light was only apparent for corals fed with zooplankton. Changes in zooxanthellae population densities occurred through differential rates of zooxanthellae division and degradation.