Genetic testing reveals some mislabeling but general compliance with a ban on herbivorous fish harvesting in Belize

Overfishing of herbivorous fishes is one of the primary causes of Caribbean coral reef decline. In Belize, herbivorous fishes comprised 28% of the catch from 2005 to 2008. In 2009, the Belize Fisheries Department implemented a national ban on herbivorous fish harvesting to mitigate high-macroalgal cover on much of the Belize Barrier Reef. However, compliance with this approach has not been evaluated. We assessed the proportion of herbivorous fish in local markets by genetically identifying fish fillets sold in five major towns in Belize from 2009 to 2011. We found that 5-7% of 111 fillets were identified as herbivorous fish and 32-51% were mislabeled. A 5-7% proportion of parrotfish in local markets suggests some ongoing parrotfish harvesting. However, our results suggest that the ban has reduced herbivorous fish harvesting and has the potential to help facilitate the restoration of 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

Differential disease incidence and mortality of inner and outer reef corals of the upper Florida Keys in association with a white syndrome outbreak

The Florida Keys Reef Tract has suffered extraordinary losses in live coral cover over the past four decades and is now battling an unprecedented coral disease outbreak. Here, colonies of Siderastrea siderea (Ellis and Solander, 1786) and Pseudodiploria strigosa (Dana, 1846) were tracked over 3 yrs (2015-2017) across two pairs of inner and outer reef sites in the upper keys, offering a unique perspective into the distribution of disease throughout the reef tract. We found that outer reef colonies of both coral species exhibited greater disease incidence and mortality associated with this ongoing epidemic, while inner patch reef colonies remained largely unaffected. These findings suggest that ecological or biological factors that differentiate coral populations across these reef zones may play an important role in susceptibility to disease

Apparent timing of density banding in the Caribbean coral Siderastrea siderea suggests complex role of key physiological variables

Skeletal growth bands in massive reef-building corals are increasingly used as proxies for environmental records despite an incomplete understanding of their formation. While the bands are known to arise from seasonal changes in light and temperature, conflicting reports about the timing of constituent high- and low-density growth bands have complicated the dating and interpretation of environmental signals recorded in corals’ growth histories. Here, we analyze 35 Siderastrea siderea cores extracted from inshore and offshore reef zones along the Florida Keys Reef Tract to investigate potential drivers of banding variability in this species. A previously proposed model of banding variation is applied to assess its potential to explain band timing in S. siderea. Colony growth characteristics and the timing of band deposition were obtained from the cores via computed tomography and were coupled with tissue thickness measurements and gender identification. Apparent time difference, or the perceived lag in coral growth response to changes in environmental conditions, was quantified for each coral core. Results suggest that linear extension, tissue thickness, and gender together do not fully explain the timing of band formation in S. siderea and therefore do not fully resolve the density patterns observed within this species. This finding suggests that other factors yet to be identified are partially determining the formation and appearance of density bands in S. siderea. The continued characterization of banding variability on scales ranging from the individual colony to entire reef systems will enrich our understanding of both coral growth and the environmental conditions to which corals are exposed

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

Microfiber abundance associated with coral tissue varies geographically on the Belize Mesoamerican Barrier Reef System

Ocean plastic pollution is a global problem that causes ecosystem degradation. Crucial knowledge gaps exist concerning patterns in microfiber abundance across regions and ecosystems, as well as the role of these pollutants within the environment. Here, we quantified the abundance of microfibers in coral samples collected from the Belize Mesoamerican Barrier Reef System (MBRS) using a polarized light microscope and identified a subsample of these to the polymer level using an Attenuated Total Reflectance Fourier Transform Infrared Spectroscopy microscope. Microfibers were found in all coral samples with rayon being identified as the most common microfiber, comprising 85% of quantified pollutants. We found a greater average abundance of microfibers in coral samples from the Sapodilla Cayes (296 ± SE 89) than in samples from the Drowned Cayes (75 ± SE 14), indicating spatial variation in microfiber abundance within coral tissue along the MBRS. These results demonstrate that corals on the Belize MBRS interact with microfibers and that microfiber abundance on reefs varies spatially due to point sources of pollution and local oceanography. As rayon from clothing typically enters the ocean through wastewater effluent, alterations to waste water infrastructure may prove useful in decreasing rayon pollution in coastal waters

Patterns of environmental variability influence coral-associated bacterial and algal communities on the Mesoamerican Barrier Reef

A coral's capacity to alter its microbial symbionts may enhance its fitness in the face of climate change. Recent work predicts exposure to high environmental variability may increase coral resilience and adaptability to future climate conditions. However, how this heightened environmental variability impacts coral-associated microbial communities remains largely unexplored. Here, we examined the bacterial and algal symbionts associated with two coral species of the genus Siderastrea with distinct life history strategies from three reef sites on the Belize Mesoamerican Barrier Reef System with low or high environmental variability. Our results reveal bacterial community structure, as well as alpha- and beta-diversity patterns, vary by host species. Differences in bacterial communities between host species were partially explained by high abundance of Deltaproteobacteria and Rhodospirillales and high bacterial diversity in Siderastrea radians. Our findings also suggest Siderastrea spp. have dynamic core bacterial communities that likely drive differences observed in the entire bacterial community, which may play a critical role in rapid acclimatization to environmental change. Unlike the bacterial community, Symbiodiniaceae composition was only distinct between host species at high thermal variability sites, suggesting that different factors shape bacterial versus algal communities within the coral holobiont. Our findings shed light on how domain-specific shifts in dynamic microbiomes may allow for unique methods of enhanced host fitness

Two offshore coral species show greater acclimatization capacity to environmental variation than nearshore counterparts in southern Belize

Coral reefs are enduring decline due to the intensifying impacts of anthropogenic global change. This widespread decline has resulted in increased efforts to identify resilient coral populations and develop novel restoration strategies. Paramount in these efforts is the need to understand how environmental variation and thermal history affect coral physiology and resilience. Here, we assess the acclimatization capacity of Siderastrea siderea and Pseudodiploria strigosa corals via a 17-month reciprocal transplant experiment between nearshore and offshore reefs on the Belize Mesoamerican Barrier Reef System. These nearshore reefs are more turbid, eutrophic, warm, and thermally variable than offshore reefs. All corals exhibited some evidence of acclimatization after transplantation. Corals transplanted from nearshore to offshore calcified slower than in their native habitat, especially S. siderea corals which exhibited 60% mortality and little to no net growth over the duration of the 17-month study. Corals transplanted from offshore to nearshore calcified faster than in their native habitat with 96% survival. Higher host tissue δ15N in nearshore corals indicated that increased heterotrophic opportunity or nitrogen sources between nearshore and offshore reefs likely promoted elevated calcification rates nearshore and may facilitate adaptation in nearshore populations to such conditions over time. These results demonstrate that offshore populations of S. siderea and P. strigosa possess the acclimatization capacity to survive in warmer and more turbid nearshore conditions, but that local adaptation to native nearshore conditions may hinder the plasticity of nearshore populations, thereby limiting their utility in coral restoration activities outside of their native habitat in the short term

Impacts of seawater saturation state (ΩA = 0.4–4.6) and temperature (10, 25 °C) on the dissolution kinetics of whole-shell biogenic carbonates

Anthropogenic increase of atmospheric pCO2 since the Industrial Revolution has caused seawater pH to decrease and seawater temperatures to increase—trends that are expected to continue into the foreseeable future. Myriad experimental studies have investigated the impacts of ocean acidification and warming on marine calcifiers’ ability to build protective shells and skeletons. No studies, however, have investigated the combined impacts of ocean acidification and warming on the whole-shell dissolution kinetics of biogenic carbonates. Here, we present the results of experiments designed to investigate the effects of seawater saturation state (ΩA = 0.4–4.6) and temperature (10, 25 °C) on gross rates of whole-shell dissolution for ten species of benthic marine calcifiers: the oyster Crassostrea virginica, the ivory barnacle Balanus eburneus, the blue mussel Mytilus edulis, the conch Strombus alatus, the tropical coral Siderastrea siderea, the temperate coral Oculina arbuscula, the hard clam Mercenaria mercenaria, the soft clam Mya arenaria, the branching bryozoan Schizoporella errata, and the coralline red alga Neogoniolithon sp. These experiments confirm that dissolution rates of whole-shell biogenic carbonates decrease with calcium carbonate (CaCO3) saturation state, increase with temperature, and vary predictably with respect to the relative solubility of the calcifiers’ polymorph mineralogy [high-Mg calcite (mol% Mg > 4) ≥ aragonite > low-Mg calcite (mol% Mg < 4)], consistent with prior studies on sedimentary and inorganic carbonates. Furthermore, the severity of the temperature effects on gross dissolution rates also varied with respect to carbonate polymorph solubility, with warming (10–25 °C) exerting the greatest effect on biogenic high-Mg calcite, an intermediate effect on biogenic aragonite, and the least effect on biogenic low-Mg calcite. These results indicate that both ocean acidification and warming will lead to increased dissolution of biogenic carbonates in future oceans, with shells/skeletons composed of the more soluble polymorphs of CaCO3 being the most vulnerable to these stressors. The effects of saturation state and temperature on gross shell dissolution rate were modeled with an exponential asymptotic function (y=B0–B2·eB1Ω) that appeals to the general Arrhenius-derived rate equation for mineral dissolution [r=(C·e-Ea/RT)(1 − Ω)n]. Although the dissolution curves for the investigated biogenic CaCO3 exhibited exponential asymptotic trends similar to those of inorganic CaCO3, the observation that gross dissolution of whole-shell biogenic CaCO3 occurred (albeit at lower rates) even in treatments that were oversaturated (Ω > 1) with respect to both aragonite and calcite reveals fundamental differences between the dissolution kinetics of whole-shell biogenic CaCO3 and inorganic CaCO3. Thus, applying stoichiometric solubility products derived for inorganic CaCO3 to model gross dissolution of biogenic carbonates may substantially underestimate the impacts of ocean acidification on net calcification (gross calcification minus gross dissolution) of systems ranging in scale from individual organisms to entire ecosystems (e.g., net ecosystem calcification). Finally, these experiments permit rough estimation of the impact of CO2-induced ocean acidification on the gross calcification rates of various marine calcifiers, calculated as the difference between net calcification rates derived empirically in prior studies and gross dissolution rates derived from the present study. Organisms’ gross calcification responses to acidification were generally less severe than their net calcification response patterns, with aragonite mollusks (bivalves, gastropods) exhibiting the most negative gross calcification response to acidification, and photosynthesizing organisms, including corals and coralline red algae, exhibiting relative resilience

Mapping coral calcification strategies from in situ boron isotope and trace element measurements of the tropical coral Siderastrea siderea

Boron isotopic and elemental analysis of coral aragonite can give important insights into the calcification strategies employed in coral skeletal construction. Traditional methods of analysis have limited spatial (and thus temporal) resolution, hindering attempts to unravel skeletal heterogeneity. Laser ablation mass spectrometry allows a much more refined view, and here we employ these techniques to explore boron isotope and co-varying elemental ratios in the tropical coral Siderastrea siderea. We generate two-dimensional maps of the carbonate parameters within the calcification medium that deposited the skeleton, which reveal large heterogeneities in carbonate chemistry across the macro-structure of a coral polyp. These differences have the potential to bias proxy interpretations, and indicate that different processes facilitated precipitation of different parts of the coral skeleton: the low-density columella being precipitated from a fluid with a carbonate composition closer to seawater, compared to the high-density inter-polyp walls where aragonite saturation was ~ 5 times that of external seawater. Therefore, the skeleton does not precipitate from a spatially homogeneous fluid and its different parts may thus have varying sensitivity to environmental stress. This offers new insights into the mechanisms behind the response of the S. siderea skeletal phenotype to ocean acidification