Ephemeral hypoxia reduces oxygen consumption in the Caribbean coral Orbicella faveolata

Coral Reefs - Oxygen concentrations in coastal waters have declined globally by 10% since the mid-twentieth century, and ocean warming will further reduce the solubility of oxygen in coastal...     

Genetic differentiation in the mountainous star coral Orbicella faveolata around Cuba

Coral Reefs - Caribbean coral reefs are biodiversity-rich habitats which provide numerous ecosystem services with both ecological and economical values, but nowadays they are severely degraded. In...     

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

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 (F_ST = 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.     

Ocean acidification partially mitigates the negative effects of warming on the recruitment of the coral,Orbicella faveolata

Coral Reefs - Ocean acidification and ocean warming constitute major threats to many calcifying reef organisms, including scleractinian corals. The combined effects of these two environmental...     

Increasing coral calcification in Orbicella faveolata and Pseudodiploria strigosa at Flower Garden Banks,Gulf of Mexico

Coral Reefs - Coral reefs are globally in decline and western Atlantic reefs have experienced the greatest losses in live coral cover of any region. The Flower Garden Banks (FGB) in the Gulf of...     

Variation in Symbiodinium ITS2 sequence assemblages among coral colonies

Endosymbiotic dinoflagellates in the genus Symbiodinium are fundamentally important to the biology of scleractinian corals, as well as to a variety of other marine organisms. The genus Symbiodinium is genetically and functionally diverse and the taxonomic nature of the union between Symbiodinium and corals is implicated as a key trait determining the environmental tolerance of the symbiosis. Surprisingly, the question of how Symbiodinium diversity partitions within a species across spatial scales of meters to kilometers has received little attention, but is important to understanding the intrinsic biological scope of a given coral population and adaptations to the local environment. Here we address this gap by describing the Symbiodinium ITS2 sequence assemblages recovered from colonies of the reef building coral Montipora capitata sampled across Kāne'ohe Bay, Hawai'i. A total of 52 corals were sampled in a nested design of Coral Colony(Site(Region)) reflecting spatial scales of meters to kilometers. A diversity of Symbiodinium ITS2 sequences was recovered with the majority of variance partitioning at the level of the Coral Colony. To confirm this result, the Symbiodinium ITS2 sequence diversity in six M. capitata colonies were analyzed in much greater depth with 35 to 55 clones per colony. The ITS2 sequences and quantitative composition recovered from these colonies varied significantly, indicating that each coral hosted a different assemblage of Symbiodinium. The diversity of Symbiodinium ITS2 sequence assemblages retrieved from individual colonies of M. capitata here highlights the problems inherent in interpreting multi-copy and intra-genomically variable molecular markers, and serves as a context for discussing the utility and biological relevance of assigning species names based on Symbiodinium ITS2 genotyping.     

Hyperspectral Sensing of Disease Stress in the Caribbean Reef-Building Coral,Orbicella faveolata - Perspectives for the Field of Coral Disease Monitoring

The effectiveness of management plans developed for responding to coral disease outbreaks is limited due to the lack of rapid methods of disease diagnosis. In order to fulfill current management guidelines for responding to coral disease outbreaks, alternative methods that significantly reduce response time must be developed. Hyperspectral sensing has been used by various groups to characterize the spectral signatures unique to asymptomatic and bleached corals. The 2010 combined bleaching and Caribbean yellow band disease outbreak in Puerto Rico provided a unique opportunity to investigate the spectral signatures associated with bleached and Caribbean yellow band-diseased colonies of Orbicella faveolata for the first time. Using derivative and cluster analyses of hyperspectral reflectance data, the present study demonstrates the proof of concept that spectral signatures can be used to differentiate between coral disease states. This method enhanced predominant visual methods of diagnosis by distinguishing between different asymptomatic conditions that are identical in field observations and photographic records. The ability to identify disease-affected tissue before lesions become visible could greatly reduce response times to coral disease outbreaks in monitoring efforts. Finally, spectral signatures associated with the poorly understood Caribbean yellow band disease are presented to guide future research on the role of pigments in the etiology.     

Sexual reproduction of the reef-building coral Diploria labyrinthiformis (Scleractinia: Faviidae), in the Colombian Caribbean

Sexual reproduction of the coral Diploria labyrinthiformis was studied for the first time. Monthly histological analyses at the Corales del Rosario National Park (Colombian Caribbean) from May 1997 to April 1998 show that D. labyrinthiformis is a hermaphroditic broadcasting species. It presents an annual gametogenic cycle with a 10-11 month period for gonad investment, in which oogenesis begins in August and ends in May-June. Spermiogenesis is short because sperm cysts were only observed in May tissue samples. In histological collected in May, an average of four mature eggs and six spermatic cysts per fertile mesentery were found. The mean diameter of mature eggs was 297 microm (+/- 97 SD) and 90 microm (+/- 33) for spermatic cysts. Rapid maturation of eggs from stage II to stage III coincides with increases in air temperature, high number of solar hours per month, decreases in wind velocity and absence of rainfall. Reproductive effort for D. labyrinthiformis (14.07 mm3/cm2/year) was similar to other Faviidae species. Although gamete release was not observed in the field, the absence of gonads in histological samples in June suggests spawning between May 25 (five days after full moon) and June 24. This event coincides with high air temperature, low number of solar hours per month, low wind velocity, and initiation of the rainy season. The earlier spawning time of this species differs from other species of the same family known for the Caribbean region.     

Embryogenesis in the reef-building coral Acropora spp

Embryogenesis in the reef building corals Acropora intermedia, A. solitaryensis, A. hyacinthus, A. digitifera, and A. tenuis was studied in detail at the morphological level, and the relationships among the animal pole, blastopore, and mouth were investigated for the first time in corals. These species showed essentially the same sequence of development. The embryo undergoes spiral-like holoblastic cleavage despite the presence of a dense isolecithal yolk. After the morula stage, the embryo enters the "prawn-chip" stage, which consists of an irregularly shaped cellular bilayer. The embryo begins to roll inward to form the bowl stage; the round shape observed during this stage suggests that it may be the beginning of gastrulation. However, the blastopore closes and the stomodeum (mouth and pharynx) is formed via invagination at a site near the closed blastopore. During the planula stage, a concavity forms in the aboral region in conjunction with numerous spirocysts, suggesting that spirocysts are used to attach to the substrate before the onset of metamorphosis.     

Role of host genetics and heat‐tolerant algal symbionts in sustaining populations of the endangered coral Orbicella faveolata in the Florida Keys with ocean warming

Identifying which factors lead to coral bleaching resistance is a priority given the global decline of coral reefs with ocean warming. During the second year of back‐to‐back bleaching events in the Florida Keys in 2014 and 2015, we characterized key environmental and biological factors associated with bleaching resilience in the threatened reef‐building coral Orbicella faveolata. Ten reefs (five inshore, five offshore, 179 corals total) were sampled during bleaching (September 2015) and recovery (May 2016). Corals were genotyped with 2bRAD and profiled for algal symbiont abundance and type. O. faveolata at the inshore sites, despite higher temperatures, demonstrated significantly higher bleaching resistance and better recovery compared to offshore. The thermotolerant Durusdinium trenchii (formerly Symbiondinium trenchii) was the dominant endosymbiont type region‐wide during initial (78.0% of corals sampled) and final (77.2%) sampling; >90% of the nonbleached corals were dominated by D. trenchii. 2bRAD host genotyping found no genetic structure among reefs, but inshore sites showed a high level of clonality. While none of the measured environmental parameters were correlated with bleaching, 71% of variation in bleaching resistance and 73% of variation in the proportion of D. trenchii was attributable to differences between genets, highlighting the leading role of genetics in shaping natural bleaching patterns. Notably, D. trenchii was rarely dominant in O. faveolata from the Florida Keys in previous studies, even during bleaching. The region‐wide high abundance of D. trenchii was likely driven by repeated bleaching associated with the two warmest years on record for the Florida Keys (2014 and 2015). On inshore reefs in the Upper Florida Keys, O. faveolata was most abundant, had the highest bleaching resistance, and contained the most corals dominated by D. trenchii, illustrating a causal link between heat tolerance and ecosystem resilience with global change.     

Range-wide population genetic structure of Symbiodinium associated with the Caribbean Sea fan coral, Gorgonia ventalina

Numerous marine invertebrates form endosymbiotic relationships with dinoflagellates of the genus Symbiodinium, yet few studies have examined the population structure of these symbionts. Here, we elucidate the population genetic structure of Symbiodinium harboured by the Caribbean octocoral Gorgonia ventalina throughout the entire range of the host. We used ten microsatellite loci to survey 35 localities spanning 3124 km across the Caribbean and Western Atlantic. Diversity of Symbiodinium haplotypes was low within colonies of G. ventalina but high among colonies. Despite high haplotypic diversity, significant evidence of clonal reproduction in Symbiodinium was detected, and most clones occurred within localities, not among them. Pairwise measures of F(ST) illustrated significant differentiation in 98% of comparisons between localities, suggesting low levels of gene flow. Clustering analyses identified six genetic groups whose distribution delimited four broad biogeographic regions. There was evidence of some connectivity among regions, corresponding with known geographic and oceanographic features. Fine-scale spatial surveys of G. ventalina colonies failed to detect differentiation among Symbiodinium at the metre scale. However, significant differentiation was observed among Symbiodinium hosted by sympatric G. ventalina colonies of different size/age classes. This cohort effect suggests that Symbiodinium may have an epidemic population structure, whereby G. ventalina recruits are infected by the locally predominant symbiont strain(s), which change over time.     

Genetic structure of a reef-building coral from thermally distinct environments on the Great Barrier Reef

Adaptation to localised thermal regimes is facilitated by restricted gene flow, ultimately leading to genetic divergence among populations and differences in their physiological tolerances. Allozyme analysis of six polymorphic loci was used to assess genetic differentiation between nine populations of the reef-building coral Acropora millepora over a latitudinal temperature gradient on the inshore regions of the Great Barrier Reef (GBR). Small but significant genetic differentiation indicative of moderate levels of gene flow (pairwise F _ST 0.023 to 0.077) was found between southern populations of A. millepora in cooler regions of the GBR and the warmer, central or northern GBR populations. Patterns of genetic differentiation at these putatively neutral allozyme loci broadly matched experimental variation in thermal tolerance and were consistent with local thermal regimes (warmest monthly-averages) for the A. millepora populations examined. It is therefore hypothesized that natural selection has influenced the thermal tolerance of the A. millepora populations examined and greater genetic divergence is likely to be revealed by examination of genetic markers under the direct effects of natural selection.     

Evolutionary origins of germline segregation in Metazoa: evidence for a germ stem cell lineage in the coral Orbicella faveolata (Cnidaria,Anthozoa)

The ability to segregate a committed germ stem cell (GSC) lineage distinct from somatic cell lineages is a characteristic of bilaterian Metazoans. However, the occurrence of GSC lineage specification in basally branching Metazoan phyla, such as Cnidaria, is uncertain. Without an independently segregated GSC lineage, germ cells and their precursors must be specified throughout adulthood from continuously dividing somatic stem cells, generating the risk of propagating somatic mutations within the individual and its gametes. To address the potential for existence of a GSC lineage in Anthozoa, the sister-group to all remaining Cnidaria, we identified moderate- to high-frequency somatic mutations and their potential for gametic transfer in the long-lived coral Orbicella faveolata (Anthozoa, Cnidaria) using a 2b-RAD sequencing approach. Our results demonstrate that somatic mutations can drift to high frequencies (up to 50%) and can also generate substantial intracolonial genetic diversity. However, these somatic mutations are not transferable to gametes, signifying the potential for an independently segregated GSC lineage in O. faveolata. In conjunction with previous research on germ cell development in other basally branching Metazoan species, our results suggest that the GSC system may be a Eumetazoan characteristic that evolved in association with the emergence of greater complexity in animal body plan organization and greater specificity of stem cell functions.     

The coral symbiont Candidatus Aquarickettsia is variably abundant in threatened Caribbean acroporids and transmitted horizontally

The symbiont “Candidatus Aquarickettsia rohweri” infects a diversity of aquatic hosts. In the threatened Caribbean coral, Acropora cervicornis, Aquarickettsia proliferates in response to increased nutrient exposure, resulting in suppressed growth and increased disease susceptibility and mortality of coral. This study evaluated the extent, as well as the ecology and evolution of Aquarickettsia infecting threatened corals, Ac. cervicornis, and Ac. palmata and their hybrid (“Ac. prolifera”). Aquarickettsia was found in all acroporids, with coral host and geographic location impacting the infection magnitude. Phylogenomic and genome-wide single-nucleotide variant analysis of Aquarickettsia found phylogenetic clustering by geographic region, not by coral taxon. Analysis of Aquarickettsia fixation indices suggests multiple sequential infections of the same coral colony are unlikely. Furthermore, relative to other Rickettsiales species, Aquarickettsia is undergoing positive selection, with Florida populations experiencing greater positive selection relative to other Caribbean locations. This may be due in part to Aquarickettsia proliferating in response to greater nutrient stress in Florida, as indicated by greater in situ replication rates in these corals. Aquarickettsia was not found to significantly codiversify with either the coral animal or the coral’s algal symbiont (Symbiodinium “fitti”). Quantitative PCR analysis showed that gametes, larvae, recruits, and juveniles from susceptible, captive-reared coral genets were not infected with Aquarickettsia. Thus, horizontal transmission of Aquarickettsia via coral mucocytes or an unidentified host is more likely. The prevalence of Aquarickettsia in Ac. cervicornis and its high abundance in the Florida coral population suggests that coral disease mitigation efforts focus on preventing early infection via horizontal transmission.Subject terms: Population genetics, Phylogenetics