Karl D. Castillo

Declining coral skeletal extension for forereef colonies of Siderastrea siderea on the Mesoamerican Barrier Reef System, Southern Belize.

Background Natural and anthropogenic stressors are predicted to have increasingly negative impacts on coral reefs. Understanding how these environmental stressors have impacted coral skeletal growth should improve our ability to predict how they may affect coral reefs in the future. We investigated century-scale variations in skeletal extension for the slow-growing massive scleractinian coral Siderastrea siderea inhabiting the forereef, backreef, and nearshore reefs of the Mesoamerican Barrier Reef System (MBRS) in the western Caribbean Sea. Methodology/Principal Findings Thirteen S. siderea cores were extracted, slabbed, and X-rayed. Annual skeletal extension was estimated from adjacent low- and high-density growth bands. Since the early 1900s, forereef S. siderea colonies have shifted from exhibiting the fastest to the slowest average annual skeletal extension, while values for backreef and nearshore colonies have remained relatively constant. The rates of change in annual skeletal extension were −0.020±0.005, 0.011±0.006, and −0.008±0.006 mm yr−1 per year [mean±SE] for forereef, backreef, and nearshore colonies respectively. These values for forereef and nearshore S. siderea were significantly lower by 0.031±0.008 and by 0.019±0.009 mm yr−1 per year, respectively, than for backreef colonies. However, only forereef S. siderea exhibited a statistically significant decline in annual skeletal extension over the last century. Conclusions/Significance Our results suggest that forereef S. siderea colonies are more susceptible to environmental stress than backreef and nearshore counterparts, which may have historically been exposed to higher natural baseline stressors. Alternatively, sediment plumes, nutrients, and pollution originating from watersheds of Guatemala and Honduras may disproportionately impact the forereef environment of the MBRS. We are presently reconstructing the history of environmental stressors that have impacted the MBRS to constrain the cause(s) of the observed reductions in coral skeletal growth. This should improve our ability to predict and potentially mitigate the effects of future environmental stressors on coral reef ecosystems.

Thermal and pCO2 Stress Elicit Divergent Transcriptomic Responses in a Resilient Coral

The oceans are becoming warmer and more acidic as a result of rising atmospheric pCO2. Transcriptome plasticity may facilitate marine organisms’ acclimation to thermal and acidification stress by tailoring gene expression to mitigate the impacts of these stressors. Here, we produce the first transcriptome of the abundant, ubiquitous, and resilient Caribbean reef-building coral Siderastrea siderea, and investigate this corals’ transcriptomic response to 95 days of thermal (T = 25, 28, 32°C) and CO2-induced acidification (324, 477, 604, 2553 µatm) stress. The S. siderea transcriptome was assembled using RNAseq and then Weighted Gene Correlation Network Analysis was employed to obtain systems-level insights into the coral’s stress response. Exposure of the coral to both elevated temperature and acidification elicited strong but divergent transcriptomic responses. Gene Ontology analysis suggests that long-term thermal stress disrupts homeostasis by increasing transcription of protein-coding genes associated with protein catabolism and suppressing transcription of genes involved in responding to environmental stimuli. Both next century (604 µatm) and extreme-high (2553 µatm) pCO2 stress increased transcription of genes associated with respiration, highlighting the potentially greater energetic requirements of maintaining calcification under high-pCO2 conditions. Under extreme-high-pCO2, increased transcription of H+-transporter genes was observed, consistent with the proposed role of proton transport in facilitating coral calcification under elevated pCO2. These results suggest that 95 days of exposure to 32°C seawater elicits a more adverse transcriptomic response (i.e., broad scale reductions in gene expression) than exposure to extreme-high acidification (2553 µatm; i.e., increased expression of genes associated with ion transport) within S. siderea—with the response to extreme warming suggesting cellular shutdown and the response to extreme acidification indicating capacity for acclimation. These results are consistent with the observation that rates of net calcification for the investigated corals were more negatively affected by the prescribed thermal stress than by the prescribed acidification stress. This study demonstrates how transcriptome plasticity may promote coral acclimation to these global change stressors, but that there are limits to the efficacy of this plasticity.

Population structure and connectivity of the mountainous star coral, Orbicella faveolata , throughout the wider Caribbean region

Abstract As coral reefs continue to decline worldwide, it becomes ever more necessary to understand the connectivity between coral populations to develop efficient management strategies facilitating survival and adaptation of coral reefs in the future. Orbicella faveolata is one of the most important reef‐building corals in the Caribbean and has recently experienced severe population reductions. Here, we utilize a panel of nine microsatellite loci to evaluate the genetic structure of O. faveolata and to infer connectivity across ten sites spanning the wider Caribbean region. Populations are generally well‐mixed throughout the basin (FST = 0.038), although notable patterns of substructure arise at local and regional scales. Eastern and western populations appear segregated with a genetic break around the Mona Passage in the north, as has been shown previously in other species; however, we find evidence for significant connectivity between Curaçao and Mexico, suggesting that the southern margin of this barrier is permeable to dispersal. Our results also identify a strong genetic break within the Mesoamerican Barrier Reef System associated with complex oceanographic patterns that promote larval retention in southern Belize. Additionally, the diverse genetic signature at Flower Garden Banks suggests its possible function as a downstream genetic sink. The findings reported here are relevant to the ongoing conservation efforts for this important and threatened species, and contribute to the growing understanding of large‐scale coral reef connectivity throughout the wider Caribbean.

Temperature Regimes Impact Coral Assemblages along Environmental Gradients on Lagoonal Reefs in Belize.

Coral reefs are increasingly threatened by global and local anthropogenic stressors such as rising seawater temperature, nutrient enrichment, sedimentation, and overfishing. Although many studies have investigated the impacts of local and global stressors on coral reefs, we still do not fully understand how these stressors influence coral community structure, particularly across environmental gradients on a reef system. Here, we investigate coral community composition across three different temperature and productivity regimes along a nearshore-offshore gradient on lagoonal reefs of the Belize Mesoamerican Barrier Reef System (MBRS). A novel metric was developed using ultra-high-resolution satellite-derived estimates of sea surface temperatures (SST) to classify reefs as exposed to low (lowTP), moderate (modTP), or high (highTP) temperature parameters over 10 years (2003 to 2012). Coral species richness, abundance, diversity, density, and percent cover were lower at highTP sites relative to lowTP and modTP sites, but these coral community traits did not differ significantly between lowTP and modTP sites. Analysis of coral life history strategies revealed that highTP sites were dominated by hardy stress-tolerant and fast-growing weedy coral species, while lowTP and modTP sites consisted of competitive, generalist, weedy, and stress-tolerant coral species. Satellite-derived estimates of Chlorophyll-a (chl-a) were obtained for 13-years (2003–2015) as a proxy for primary production. Chl-a concentrations were highest at highTP sites, medial at modTP sites, and lowest at lowTP sites. Notably, thermal parameters correlated better with coral community traits between site types than productivity, suggesting that temperature (specifically number of days above the thermal bleaching threshold) played a greater role in defining coral community structure than productivity on the MBRS. Dominance of weedy and stress-tolerant genera at highTP sites suggests that corals utilizing these two life history strategies may be better suited to cope with warmer oceans and thus may warrant protective status under climate change.

Next-century ocean acidification and warming both reduce calcification rate, but only acidification alters skeletal morphology of reef-building coral Siderastrea siderea

Atmospheric pCO2 is predicted to rise from 400 to 900 ppm by year 2100, causing seawater temperature to increase by 1–4 °C and pH to decrease by 0.1–0.3. Sixty-day experiments were conducted to investigate the independent and combined impacts of acidification (pCO2 = 424–426, 888–940 ppm-v) and warming (T = 28, 32 °C) on calcification rate and skeletal morphology of the abundant and widespread Caribbean reef-building scleractinian coral Siderastrea siderea. Hierarchical linear mixed-effects modelling reveals that coral calcification rate was negatively impacted by both warming and acidification, with their combined effects yielding the most deleterious impact. Negative effects of warming (32 °C/424 ppm-v) and high-temperature acidification (32 °C/940 ppm-v) on calcification rate were apparent across both 30-day intervals of the experiment, while effects of low-temperature acidification (28 °C/888 ppm-v) were not apparent until the second 30-day interval—indicating delayed onset of acidification effects at lower temperatures. Notably, two measures of coral skeletal morphology–corallite height and corallite infilling–were negatively impacted by next-century acidification, but not by next-century warming. Therefore, while next-century ocean acidification and warming will reduce the rate at which corals build their skeletons, next-century acidification will also modify the morphology and, potentially, function of coral skeletons.

Intrareef variations in Li/Mg and Sr/Ca sea surface temperature proxies in the Caribbean reef‐building coral Siderastrea siderea

Caribbean sea surface temperatures (SSTs) have increased at a rate of 0.2°C per decade since 1971, a rate double that of the mean global change. Recent investigations of the coral Siderastrea siderea on the Belize Mesoamerican Barrier Reef System (MBRS) have demonstrated that warming over the last 30 years has had a detrimental impact on calcification. Instrumental temperature records in this region are sparse, making it necessary to reconstruct longer SST records indirectly through geochemical temperature proxies. Here we investigate the skeletal Sr/Ca and Li/Mg ratios of S. siderea from two distinct reef zones (forereef and backreef) of the MBRS. Our field calibrations of S. siderea show that Li/Mg and Sr/Ca ratios are well correlated with temperature, although both ratios are 3 times more sensitive to temperature change in the forereef than in the backreef. These differences suggest that a secondary parameter also influences these SST proxies, highlighting the importance for site- and species-specific SST calibrations. Application of these paleothermometers to downcore samples reveals highly uncertain reconstructed temperatures in backreef coral, but well-matched reconstructed temperatures in forereef coral, both between Sr/Ca-SSTs and Li/Mg-SSTs, and in comparison to the Hadley Centre Sea Ice and Sea Surface Temperature record. Reconstructions generated from a combined Sr/Ca and Li/Mg multiproxy calibration improve the precision of these SST reconstructions. This result confirms that there are circumstances in which both Li/Mg and Sr/Ca are reliable as stand-alone and combined proxies of sea surface temperature. However, the results also highlight that high-precision, site-specific calibrations remain critical for reconstructing accurate SSTs from coral-based elemental proxies.

Heterotrophy mitigates the response of the temperate coral Oculina arbuscula to temperature stress

Abstract Anthropogenic increases in atmospheric carbon dioxide concentration have caused global average sea surface temperature (SST) to increase by approximately 0.11°C per decade between 1971 and 2010 – a trend that is projected to continue through the 21st century. A multitude of research studies have demonstrated that increased SSTs compromise the coral holobiont (cnidarian host and its symbiotic algae) by reducing both host calcification and symbiont density, among other variables. However, we still do not fully understand the role of heterotrophy in the response of the coral holobiont to elevated temperature, particularly for temperate corals. Here, we conducted a pair of independent experiments to investigate the influence of heterotrophy on the response of the temperate scleractinian coral Oculina arbuscula to thermal stress. Colonies of O. arbuscula from Radio Island, North Carolina, were exposed to four feeding treatments (zero, low, moderate, and high concentrations of newly hatched Artemia sp. nauplii) across two independent temperature experiments (average annual SST (20°C) and average summer temperature (28°C) for the interval 2005–2012) to quantify the effects of heterotrophy on coral skeletal growth and symbiont density. Results suggest that heterotrophy mitigated both reduced skeletal growth and decreased symbiont density observed for unfed corals reared at 28°C. This study highlights the importance of heterotrophy in maintaining coral holobiont fitness under thermal stress and has important implications for the interpretation of coral response to climate change.

Coral Symbiodinium Community Composition Across the Belize Mesoamerican Barrier Reef System is Influenced by Host Species and Thermal Variability

Reef-building corals maintain a symbiotic relationship with dinoflagellate algae of the genus Symbiodinium, and this symbiosis is vital for the survival of the coral holobiont. Symbiodinium community composition within the coral host has been shown to influence a coral’s ability to resist and recover from stress. A multitude of stressors including ocean warming, ocean acidification, and eutrophication have been linked to global scale decline in coral health and cover in recent decades. Three distinct thermal regimes (highTP, modTP, and lowTP) following an inshore-offshore gradient of declining average temperatures and thermal variation were identified on the Belize Mesoamerican Barrier Reef System (MBRS). Quantitative metabarcoding of the ITS-2 locus was employed to investigate differences and similarities in Symbiodinium genetic diversity of the Caribbean corals Siderastrea siderea, S. radians, and Pseudodiploria strigosa between the three thermal regimes. A total of ten Symbiodinium lineages were identified across the three coral host species. S. siderea was associated with distinct Symbiodinium communities; however, Symbiodinium communities of its congener, S. radians and P. strigosa, were more similar to one another. Thermal regime played a role in defining Symbiodinium communities in S. siderea but not S. radians or P. strigosa. Against expectations, Symbiodinium trenchii, a symbiont known to confer thermal tolerance, was dominant only in S. siderea at one sampled offshore site and was rare inshore, suggesting that coral thermal tolerance in more thermally variable inshore habitats is achieved through alternative mechanisms. Overall, thermal parameters alone were likely not the only primary drivers of Symbiodinium community composition, suggesting that environmental variables unrelated to temperature (i.e., light availability or nutrients) may play key roles in structuring coral-algal communities in Belize and that the relative importance of these environmental variables may vary by coral host species.

Nearshore corals on the Mesoamerican Barrier Reef System on pace to cease growing as soon as year 2110

Anthropogenic global change and local anthropogenic stressors are decreasing coral growth and survival globally, thus altering the structure and function of coral reef ecosystems. We show that skeletal extension rates of nearshore colonies of Siderastrea siderea and Pseudodiploria strigosa across the Belize Mesoamerican Barrier Reef System (MBRS) have declined at average rates of 0.01 and 0.08 mm/yr, respectively, over approximately the past century, while offshore conspecifics exhibited no significant trend in extension with time. This caused extension rates of nearshore colonies to converge with their historically slower-growing offshore conspecifics. Bleaching events negatively impacted extension rates in S. siderea but not in P. strigosa. The more negative trend in linear extension for nearshore versus offshore colonies may arise from ocean warming combined with stronger land-based anthropogenic stressors within nearshore environments. Extrapolating these trends in linear extension into the future suggests that nearshore P. strigosa and S. siderea will cease growing by years 2110 and 2370, respectively.

Historical trends in pH and carbonate biogeochemistry on the Belize Mesoamerican Barrier Reef System

Coral reefs are important ecosystems that are increasingly negatively impacted by human activities. Understanding which anthropogenic stressors play the most significant role in their decline is vital for the accurate prediction of future trends in coral reef health and for effective mitigation of these threats. Here we present annually resolved boron and carbon isotope measurements of two cores capturing the past 90 years of growth of the tropical reef‐building coral Siderastrea siderea from the Belize Mesoamerican Barrier Reef System. The pairing of these two isotope systems allows us to parse the reconstructed pH change into relative changes in net ecosystem productivity and net ecosystem calcification between the two locations. This approach reveals that the relationship between seawater pH and coral calcification, at both a colony and ecosystem level, is complex and cannot simply be modeled as linear or even positive. This study also underscores both the utility of coupled δ11B‐δ13C measurements in tracing past biogeochemical cycling in coral reefs and the complexity of this cycling relative to the open ocean. Plain Language Summary Coral reefs world‐wide are in decline due to multiple anthropogenic stressors (e.g. ocean warming and acidification in response to anthropogenic CO2 release). Here we explore a new way to examine the relationship between these anthropogenic stressors and critical ecosystem‐scale processes using paired annual‐resolution boron and carbon isotope measurements of coral cores spanning the past century. This isotopic pairing allowed us to compare changes in seawater pH, net ecosystem productivity, and net ecosystem calcification between forereef and backreef locations of the southern Belize Mesoamerican Barrier Reef System. We specifically show that the forereef colony, which exhibits declining growth over the past century, recorded unexpectedly steady pH over the same interval. The backreef colony, in contrast, exhibited accelerating growth over this interval, while recording surprisingly rapid ocean acidification. This apparent contradiction is explained with carbon isotope data from the cores showing that increasing primary production on the forereef has offset anthropogenic acidification. Likewise, the increasing rate of coral calcification in the backreef (which generates acidity) has exacerbated anthropogenic acidification of backreef waters. Thus, although ocean acidification and warming influence calcification and primary production within reef systems, the resulting changes can drive biogeochemical feedbacks capable of eliminating or amplifying the anthropogenic CO2 signal.