Anthropogenic mortality on coral reefs in Caribbean Panama predates coral disease and bleaching

Caribbean reef corals have declined precipitously since the 1980s due to regional episodes of bleaching, disease and algal overgrowth, but the extent of earlier degradation due to localised historical disturbances such as land clearing and overfishing remains unresolved. We analysed coral and molluscan fossil assemblages from reefs near Bocas del Toro, Panama to construct a timeline of ecological change from the 19th century-present. We report large changes before 1960 in coastal lagoons coincident with extensive deforestation, and after 1960 on offshore reefs. Striking changes include the demise of previously dominant staghorn coral Acropora cervicornis and oyster Dendrostrea frons that lives attached to gorgonians and staghorn corals. Reductions in bivalve size and simplification of gastropod trophic structure further implicate increasing environmental stress on reefs. Our paleoecological data strongly support the hypothesis, from extensive qualitative data, that Caribbean reef degradation predates coral bleaching and disease outbreaks linked to anthropogenic climate change.     

Natural Disease Resistance in Threatened Staghorn Corals

Disease epidemics have caused extensive damage to tropical coral reefs and to the reef-building corals themselves, yet nothing is known about the abilities of the coral host to resist disease infection. Understanding the potential for natural disease resistance in corals is critically important, especially in the Caribbean where the two ecologically dominant shallow-water corals, Acropora cervicornis and A. palmata, have suffered an unprecedented mass die-off due to White Band Disease (WBD), and are now listed as threatened under the US Threatened Species Act and as critically endangered under the IUCN Red List criteria. Here we examine the potential for natural resistance to WBD in the staghorn coral Acropora cervicornis by combining microsatellite genotype information with in situ transmission assays and field monitoring of WBD on tagged genotypes. We show that six percent of staghorn coral genotypes (3 out of 49) are resistant to WBD. This natural resistance to WBD in staghorn corals represents the first evidence of host disease resistance in scleractinian corals and demonstrates that staghorn corals have an innate ability to resist WBD infection. These resistant staghorn coral genotypes may explain why pockets of Acropora have been able to survive the WBD epidemic. Understanding disease resistance in these corals may be the critical link to restoring populations of these once dominant corals throughout their range.     

Coral reefs of Bocas del Toro, Panamá: IV. Distribution, structure and conservation state of continental reefs of Peninsula Valiente]

This is the fourth and last contribution describing the individual structure, distribution and conservation status of coral reefs in the Province of Bocas del Toro. Here we describe 14 new reefs along 129 km of coast from Peninsula Valiente to Río Calovébora. Average live coral coverage for this region was 17.1% (+/- 3.6%), mainly in the western region of the peninsula (Bahia Bluefield and Ensenada Tobobe). Coral cover increases with depth (> 5 m) for most species at several reefs and the corals Porites furcata and Acropora palmata dominated shallow waters. Acropora palmata was found abundant in 43% of the studied reefs and toward the regions of the Ensenada Tobobe and Punta Valiente. Coral recruitment rates were similar in distribution to those reefs with greater coral coverage, with average densities of 4 recruit/m2 (maximum 9 recruits/m2) and mainly Agaricia spp., Porites astreoides and Siderastrea siderea. The greater diversity of corals and sponges was recorded toward the western side of the peninsula, with a total of 55 coral species in the study area, including two new records for Bocas del Toro (59 species in total), Dichocoenia stellaris and Madracis luciphila and increasing the diversity of corals of Panama to 65 species. We found 24 species of octocorals and Gorgonia mariae, Muriceopsis sulphurea and Muricea laxaoosens, are informed for the first time to the area, increasing in 10% the diversity for Bocas del Toro (32 in total). We recorded 48 sponges, including five new species for the area and representing an increase of 9% in the total number (58). Large populations of Acropora palmata were found in the Ensenada Tobobe, what justifies once again the need for modifying the existing protected area, so that this new region is incorporated within the conservation plans.     

Weak prezygotic isolating mechanisms in threatened Caribbean Acropora corals

The Caribbean corals, Acropora palmata and A. cervicornis, recently have undergone drastic declines primarily as a result of disease. Previous molecular studies have demonstrated that these species form a hybrid (A. prolifera) that varies in abundance throughout the range of the parental distribution. There is variable unidirectional introgression across loci and sites of A. palmata genes flowing into A. cervicornis. Here we examine the efficacy of prezygotic reproductive isolating mechanisms within these corals including spawning times and choice and no-choice fertilization crosses. We show that these species have subtly different mean but overlapping spawning times, suggesting that temporal isolation is likely not an effective barrier to hybridization. We found species-specific differences in gametic incompatibilities. Acropora palmata eggs were relatively resistant to hybridization, especially when conspecific sperm are available to outcompete heterospecific sperm. Acropora cervicornis eggs demonstrated no evidence for gametic incompatibility and no evidence of reduced viability after aging four hours. This asymmetry in compatibility matches previous genetic data on unidirectional introgression.     

Nine novel, polymorphic microsatellite markers for the study of threatened Caribbean acroporid corals

Caribbean reef-building corals in the genus Acropora have been declining dramatically since the 1980s and are now listed as threatened. The study of their complex reproductive system (mixed asexual and sexual) and their population structure requires highly polymorphic nuclear genetic markers. Of eight previously developed microsatellite loci for A. palmata, only five behaved in a Mendelian fashion and only four reliably amplified the sister species, A. cervicornis. Here, nine novel microsatellite markers are presented that dramatically increase the power to distinguish between asexual and sexual reproductive events and may help to refine population boundaries and gene flow across their ranges.     

Genomic patterns in Acropora cervicornis show extensive population structure and variable genetic diversity

Threatened Caribbean coral communities can benefit from high‐resolution genetic data used to inform management and conservation action. We use Genotyping by Sequencing (GBS) to investigate genetic patterns in the threatened coral, Acropora cervicornis, across the Florida Reef Tract (FRT) and the western Caribbean. Results show extensive population structure at regional scales and resolve previously unknown structure within the FRT. Different regions also exhibit up to threefold differences in genetic diversity (He), suggesting targeted management based on the goals and resources of each population is needed. Patterns of genetic diversity have a strong spatial component, and our results show Broward and the Lower Keys are among the most diverse populations in Florida. The genetic diversity of Caribbean staghorn coral is concentrated within populations and within individual reefs (AMOVA), highlighting the complex mosaic of population structure. This variance structure is similar over regional and local scales, which suggests that in situ nurseries are adequately capturing natural patterns of diversity, representing a resource that can replicate the average diversity of wild assemblages, serving to increase intraspecific diversity and potentially leading to improved biodiversity and ecosystem function. Results presented here can be translated into specific goals for the recovery of A. cervicornis, including active focus on low diversity areas, protection of high diversity and connectivity, and practical thresholds for responsible restoration.     

Age and intraspecific diversity of resilient Acropora communities in Belize

Coral Reefs - The corals Acropora palmata and A. cervicornis are important Caribbean reef-builders that have faced significant mortality in recent decades. While many studies have focused on the...     

Capitalizing on an ecological process to aid coral reef ecosystem restoration: Can gastropod trophodynamics enhance coral survival?

Coral Reefs - Coral reefs in the Florida Keys have degraded in recent decades, prompting efforts to re-establish populations of staghorn coral, Acropora cervicornis, to restore structure and...     

Widespread association of a Rickettsiales-like bacterium with reef-building corals

White band disease type I (WBD I) has been a major cause of the dramatic decline of Acroporid coral populations throughout the Caribbean during the last two decades, yet the aetiological agent of this disease is unknown. In this study, the bacterial communities associated with both healthy and diseased Acropora species were compared by 16S rDNA analyses. The bacterial communities of both healthy and diseased Acropora spp. were dominated by a single ribotype with 90% identity to a bacterium in the order Rickettsiales. Screening by nested PCR specific to the coral-associated Rickettsiales 1 (CAR1) bacterium showed that this microbe was widespread in both healthy and diseased A. cervicornis and A. palmata corals from 'healthy' (i.e. low WBD I incidence) and 'stressed' reefs (i.e. high WBD I incidence). These results indicate that there were no dramatic changes in the composition of the microbial community associated with WBD I. CAR1 was also associated with non-Acroporid corals of the Caribbean, as well as with two Acroporid corals native to the Pacific. CAR1 was not present in the water column. This bacterium was also absent from preserved Caribbean Acroporid samples collected between 1937 and 1980 before the outbreak of WBD I. These results suggest CAR1 is a relatively new bacterial associate of Acroporids and that a non-bacterial pathogen might be the cause of WBD I.     

Microbiome signatures in Acropora cervicornis are associated with genotypic resistance to elevated nutrients and heat stress

Coral Reefs - The staghorn coral, Acropora cervicornis, was once abundant in the Caribbean, but now is listed as critically endangered. To recover A. cervicornis populations, restoration efforts...     

Examination of species boundaries in the Acropora cervicornis group (Scleractinia, cnidaria) using nuclear DNA sequence analyses

Although Acropora is the most species-rich genus of the scleractinian (stony) corals, only three species occur in the Caribbean: A. cervicornis, A. palmata and A. prolifera. Based on overall coral morphology, abundance and distribution patterns, it has been suggested that A. prolifera may be a hybrid between A. cervicornis and A. palmata. The species boundaries among these three morphospecies were examined using DNA sequence analyses of the nuclear Pax-C 46/47 intron and the ribosomal DNA Internal Transcribed Spacer (ITS1 and ITS2) and 5.8S regions. Moderate levels of sequence variability were observed in the ITS and 5.8S sequences (up to 5.2% overall sequence difference), but variability within species was as large as between species and all three species carried similar sequences. Since this is unlikely to represent a shared ancestral polymorphism, the data suggest that introgressive hybridization occurs among the three species. For the Pax-C intron, A. cervicornis and A. palmata had very distinct allele frequencies and A. cervicornis carried a unique allele at a frequency of 0.769 (although sequence differences between alleles were small). All A. prolifera colonies examined were heterozygous for the Pax-C intron, whereas heterozygosity was only 0.286 and 0.333 for A. cervicornis and A. palmata, respectively. These data support the hypothesis that A. prolifera is the product of hybridization between two species that have a different allelic composition for the Pax-C intron, i.e. A. cervicornis and A. palmata. We therefore suggest that A. prolifera is a hybrid between A. cervicornis and A. palmata, which backcrosses with the parental species at low frequency.     

A 'fair go' for coral hybridization

Hybridisation between coral species clearly occurs in vitro, but the evolutionary significance of this cross-fertility is still the subject of much debate. Compelling genetic and reproductive evidence support introgressive hybridization amongst Indo-Pacific members of the scleractinian genus Acropora. Although population genetic analyses indicate that interspecific hybridization events are relatively rare, they are likely be important on evolutionary time scales, creating the capacity for adaptive evolution by increasing genomic diversity and heterozygosity. However, in a recent paper based exclusively on the three endemic Caribbean Acropora species, Vollmer and Palumbi (2002) dispute the occurrence of reticulation in corals. Here we use data from both the Vollmer and Palumbi study and our earlier paper on the same species (van Oppen et al., 2000) to show that reticulation has occurred amongst the Caribbean Acropora species. Furthermore, conclusions based on the limited Caribbean Acropora fauna cannot simply be extrapolated to Indo-Pacific corals, and it is inappropriate to view some coral species as 'immortal mules'.     

Human pathogen shown to cause disease in the threatened eklhorn coral Acropora palmata

Coral reefs are in severe decline. Infections by the human pathogen Serratia marcescens have contributed to precipitous losses in the common Caribbean elkhorn coral, Acropora palmata, culminating in its listing under the United States Endangered Species Act. During a 2003 outbreak of this coral disease, called acroporid serratiosis (APS), a unique strain of the pathogen, Serratia marcescens strain PDR60, was identified from diseased A. palmata, human wastewater, the non-host coral Siderastrea siderea and the corallivorous snail Coralliophila abbreviata. In order to examine humans as a source and other marine invertebrates as vectors and/or reservoirs of the APS pathogen, challenge experiments were conducted with A. palmata maintained in closed aquaria to determine infectivity of strain PDR60 from reef and wastewater sources. Strain PDR60 from wastewater and diseased A. palmata caused disease signs in elkhorn coral in as little as four and five days, respectively, demonstrating that wastewater is a definitive source of APS and identifying human strain PDR60 as a coral pathogen through fulfillment of Koch's postulates. A. palmata inoculated with strain PDR60 from C. abbreviata showed limited virulence, with one of three inoculated fragments developing APS signs within 13 days. Strain PDR60 from non-host coral S. siderea showed a delayed pathogenic effect, with disease signs developing within an average of 20 days. These results suggest that C. abbreviata and non-host corals may function as reservoirs or vectors of the APS pathogen. Our results provide the first example of a marine "reverse zoonosis" involving the transmission of a human pathogen (S. marcescens) to a marine invertebrate (A. palmata). These findings underscore the interaction between public health practices and environmental health indices such as coral reef survival.     

Local and regional scale recovery of Diadema promotes recruitment of scleractinian corals

The phase change from coral to macroalgal dominance on many Caribbean reefs was exacerbated by the mortality of the echinoid Diadema antillarum in 1983–1984, and until recently, this sea urchin has remained rare on reefs throughout the western Atlantic. By the late 1990s, Diadema started to reappear in large numbers on some Jamaican reefs, and by 2000, the high densities were correlated with significantly greater abundances of juvenile corals. Here, we show that dense populations of Diadema now occur over a multi-kilometre-wide scale at six locations scattered along a 4100 km arc across the entire Caribbean. In all cases, these dense populations are found in shallow water (< 6 m depth) on outer reef communities and are associated with reduced macroalgal cover and enhanced coral recruitment. We conclude that population recovery of Diadema is occurring at both local and regional scales, and that grazing by this echinoid is creating conditions favouring the recruitment of corals.     

Small-scale mapping of indeterminate arborescent acroporid coral (Acropora cervicornis) patches

Coral Reefs - Western Atlantic populations of the staghorn coral Acropora cervicornis have drastically declined over the past few decades. Hence, interest in its ecology and spatial extent has...     

Coral reefs and residents of the U.S. Virgin Islands: a relationship of knowledge, outdoor activities and stewardship

To test the hypotheses that U.S. Virgin Islanders' knowledge about local coral reefs is correlated with behavior, and that different sociological groups of residents have different patterns of knowledge and behavior, a mixed approach to surveying residents was used: (1) personal interviews were held in public locations and (2) an online version of the survey was administered to residents of the U.S. Virgin Islands. From July-October 2008,462 residents over 18 years old were surveyed. Results indicate that people who engaged in outdoor activities knew significantly more about coral reefs (Spearman p < 0.01, r2 = -0.128). Those more knowledgeable about coral reefs engaged in more positive stewardship activities (e.g. beach clean-ups) (Spearman p < 0.01, r2 = 0.127). Negative behaviors (e.g. anchoring on reef) were not significantly correlated with increased knowledge of coral reefs (Spearman p = -0.911, r2 = -0.000025). Fishers did not have greater ability in identifying Acropora palmata coral than non-fishers (chi2 = 4.138, p = 0.126); however, swimmers, snorkelers and divers (as a class) were more able to identify A. palmata than non-swimmers (chi2 = 9.764, p = 0.002). Most residents identified sea turtle species as endangered (hawksbill turtle, 78.9%) but only 48.2% of the responses included Acropora spp. as threatened. Resident attitudes towards conservation of local resources were overwhelmingly positive.     

Characterization of geographically distinct bacterial communities associated with coral mucus produced by Acropora spp. and Porites spp

Acropora and Porites corals are important reef builders in the Indo-Pacific and Caribbean. Bacteria associated with mucus produced by Porites spp. and Acropora spp. from Caribbean (Punta Maroma, Mexico) and Indo-Pacific (Hoga and Sampela, Indonesia) reefs were determined. Analysis of pyrosequencing libraries showed that bacterial communities from Caribbean corals were significantly more diverse (H', 3.18 to 4.25) than their Indonesian counterparts (H', 2.54 to 3.25). Dominant taxa were Gammaproteobacteria, Alphaproteobacteria, Firmicutes, and Cyanobacteria, which varied in relative abundance between coral genera and region. Distinct coral host-specific communities were also found; for example, Clostridiales were dominant on Acropora spp. (at Hoga and the Mexican Caribbean) compared to Porites spp. and seawater. Within the Gammproteobacteria, Halomonas spp. dominated sequence libraries from Porites spp. (49%) and Acropora spp. (5.6%) from the Mexican Caribbean, compared to the corresponding Indonesian coral libraries (<2%). Interestingly, with the exception of Porites spp. from the Mexican Caribbean, there was also a ubiquity of Psychrobacter spp., which dominated Acropora and Porites libraries from Indonesia and Acropora libraries from the Caribbean. In conclusion, there was a dominance of Halomonas spp. (associated with Acropora and Porites [Mexican Caribbean]), Firmicutes (associated with Acropora [Mexican Caribbean] and with Acropora and Porites [Hoga]), and Cyanobacteria (associated with Acropora and Porites [Hoga] and Porites [Sampela]). This is also the first report describing geographically distinct Psychrobacter spp. associated with coral mucus. In addition, the predominance of Clostridiales associated with Acropora spp. provided additional evidence for coral host-specific microorganisms.     

Atmospheric dimethysulphide production from corals in the Great Barrier Reef and links to solar radiation, climate and coral bleaching

Coral zooxanthellae contain high concentrations of dimethylsulphoniopropionate (DMSP), the precursor of dimethylsulphide (DMS), an aerosol substance that could affect cloud cover, solar radiation and ocean temperatures. Acropora intermedia a dominant staghorn coral in the Indo-Pacific region, contain some of the highest concentrations of DMSP reported in the literature but no studies have shown that corals produce atmospheric DMS in situ and thus could potentially participate in sea surface temperature (SST) regulation over reefs; or how production varies during coral bleaching. We show that A. intermedia from the Great Barrier Reef (GBR) produces significant amounts of atmospheric DMS, in chamber experiments, indicating that coral reefs in this region could contribute to an “ocean thermostat” similar to that described for the western Pacific warm pool, where significantly fewer coral reefs have bleached during the last 25?years because of a cloud-SST feedback. However, when Acropora intermedia was stressed with higher light levels and seawater temperatures DMSP production, an indicator of zooxanthellae expulsion, increased markedly in the chamber, whilst atmospheric DMS emissions almost completely shut down. These results suggest that during increased light levels and seawater temperatures in the GBR coral shut-down atmospheric DMS aerosol production, potentially increasing solar radiation levels over reefs and exacerbating coral bleaching.     

Genetic Diversity and Connectivity in the Threatened Staghorn Coral (Acropora cervicornis) in Florida

Over the past three decades, populations of the dominant shallow water Caribbean corals, Acropora cervicornis and A. palmata, have been devastated by white-band disease (WBD), resulting in the listing of both species as threatened under the U.S. Endangered Species Act. A key to conserving these threatened corals is understanding how their populations are genetically interconnected throughout the greater Caribbean. Genetic research has demonstrated that gene flow is regionally restricted across the Caribbean in both species. Yet, despite being an important site of coral reef research, little genetic data has been available for the Florida Acropora, especially for the staghorn coral, A. cervicornis. In this study, we present new mitochondrial DNA sequence data from 52 A. cervicornis individuals from 22 sites spread across the upper and lower Florida Keys, which suggest that Florida''s A. cervicornis populations are highly genetically interconnected (F_ST = −0.081). Comparison between Florida and existing mtDNA data from six regional Caribbean populations indicates that Florida possesses high levels of standing genetic diversity (h = 0.824) relative to the rest of the greater Caribbean (h = 0.701±0.043). We find that the contemporary level of gene flow across the greater Caribbean, including Florida, is restricted ( = 0.117), but evidence from shared haplotypes suggests the Western Caribbean has historically been a source of genetic variation for Florida. Despite the current patchiness of A. cervicornis in Florida, the relatively high genetic diversity and connectivity within Florida suggest that this population may have sufficient genetic variation to be viable and resilient to environmental perturbation and disease. Limited genetic exchange across regional populations of the greater Caribbean, including Florida, indicates that conservation efforts for A. cervicornis should focus on maintaining and managing populations locally rather than relying on larval inputs from elsewhere.     

Host population genetic structure and zooxanthellae diversity of two reef-building coral species along the Florida Reef Tract and wider Caribbean

In preparation for a large-scale coral restoration project, we surveyed host population genetic structure and symbiont diversity of two reef-building corals in four reef zones along the Florida reef tract (FRT). There was no evidence for coral population subdivision along the FRT in Acropora cervicornis or Montastraea faveolata based on microsatellite markers. However, in A. cervicornis, significant genetic differentiation was apparent when extending the analysis to broader scales (Caribbean). Clade diversity of the zooxanthellae differed along the FRT. A. cervicornis harbored mostly clade A with clade D zooxanthellae being prominent in colonies growing inshore and in the mid-channel zones that experience greater temperature fluctuations and receive significant nutrient and sediment input. M. faveolata harbored a more diverse array of symbionts, and variation in symbiont diversity among four habitat zones was more subtle but still significant. Implications of these results are discussed for ongoing restoration and conservation work.