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.     

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'.     

Hosts of the Plio-Pleistocene past reflect modern-day coral vulnerability

The risk of global extinction of reef-building coral species is increasing. We evaluated extinction risk using a biological trait-based resiliency index that was compared with Caribbean extinction during the Plio-Pleistocene, and with extinction risk determined by the International Union for Conservation of Nature (IUCN). Through the Plio-Pleistocene, the Caribbean supported more diverse coral assemblages than today and shared considerable overlap with contemporary Indo-Pacific reefs. A clear association was found between extant Plio-Pleistocene coral genera and our positive resilience scores. Regional extinction in the past and vulnerability in the present suggests that Pocillopora, Stylophora and foliose Pavona are among the most susceptible taxa to local and regional isolation. These same taxa were among the most abundant corals in the Caribbean Pliocene. Therefore, a widespread distribution did not equate with immunity to regional extinction. The strong relationship between past and present vulnerability suggests that regional extinction events are trait-based and not merely random episodes. We found several inconsistencies between our data and the IUCN scores, which suggest a need to critically re-examine what constitutes coral vulnerability.     

Cyanobacteria associated with coral black band disease in Caribbean and Indo-Pacific Reefs

For 30 years it has been assumed that a single species of cyanobacteria, Phormidium corallyticum, is the volumetrically dominant component of all cases of black band disease (BBD) in coral. Cyanobacterium-specific 16S rRNA gene primers and terminal restriction fragment length polymorphism analyses were used to determine the phylogenetic diversity of these BBD cyanobacteria on coral reefs in the Caribbean and Indo-Pacific Seas. These analyses indicate that the cyanobacteria that inhabit BBD bacterial mats collected from the Caribbean and Indo-Pacific Seas belong to at least three different taxa, despite the fact that the corals in each case exhibit similar signs and patterns of BBD mat development.     

Cyanobacteria Associated with Coral Black Band Disease in Caribbean and Indo-Pacific Reefs

For 30 years it has been assumed that a single species of cyanobacteria, Phormidium corallyticum, is the volumetrically dominant component of all cases of black band disease (BBD) in coral. Cyanobacterium-specific 16S rRNA gene primers and terminal restriction fragment length polymorphism analyses were used to determine the phylogenetic diversity of these BBD cyanobacteria on coral reefs in the Caribbean and Indo-Pacific Seas. These analyses indicate that the cyanobacteria that inhabit BBD bacterial mats collected from the Caribbean and Indo-Pacific Seas belong to at least three different taxa, despite the fact that the corals in each case exhibit similar signs and patterns of BBD mat development.     

Algae as Reservoirs for Coral Pathogens

Benthic algae are associated with coral death in the form of stress and disease. It''s been proposed that they release exudates, which facilitate invasion of potentially pathogenic microbes at the coral-algal interface, resulting in coral disease. However, the original source of these pathogens remains unknown. This study examined the ability of benthic algae to act as reservoirs of coral pathogens by characterizing surface associated microbes associated with major Caribbean and Indo-Pacific algal species/types and by comparing them to potential pathogens of two dominant coral diseases: White Syndrome (WS) in the Indo-Pacific and Yellow Band Disease (YBD) in the Caribbean. Coral and algal sampling was conducted simultaneously at the same sites to avoid spatial effects. Potential pathogens were defined as those absent or rare in healthy corals, increasing in abundance in healthy tissues adjacent to a disease lesion, and dominant in disease lesions. Potentially pathogenic bacteria were detected in both WS and YBD and were also present within the majority of algal species/types (54 and 100% for WS and YBD respectively). Pathogenic ciliates were associated only with WS and not YBD lesions and these were also present in 36% of the Indo-Pacific algal species. Although potential pathogens were associated with many algal species, their presence was inconsistent among replicate algal samples and detection rates were relatively low, suggestive of low density and occurrence. At the community level, coral-associated microbes irrespective of the health of their host differed from algal-associated microbes, supporting that algae and corals have distinctive microbial communities associated with their tissue. We conclude that benthic algae are common reservoirs for a variety of different potential coral pathogens. However, algal-associated microbes alone are unlikely to cause coral death. Initial damage or stress to the coral via other competitive mechanisms is most likely a prerequisite to potential transmission of these pathogens.     

The Vibrio core group induces yellow band disease in Caribbean and Indo-Pacific reef-building corals

Aims: To determine the relationship between yellow band disease (YBD)-associated pathogenic bacteria found in both Caribbean and Indo-Pacific reefs, and the virulence of these pathogens. YBD is one of the most significant coral diseases of the tropics. Materials and Results: The consortium of four Vibrio species was isolated from YBD tissue on Indo-Pacific corals: Vibrio rotiferianus, Vibrio harveyi, Vibrio alginolyticus and Vibrio proteolyticus. This consortium affects Symbiodinium (zooxanthellae) in hospite causing symbiotic algal cell dysfunction and disorganization of algal thylakoid membrane-bound compartment from corals in both field and laboratory. Infected corals have decreased zooxanthella cell division compared with the healthy corals. Vibrios isolated from diseased Diploastrea heliopora, Fungia spp. and Herpolitha spp. of reef-building corals display pale yellow lesions, which are similar to those found on Caribbean Montastraea spp. with YBD. Conclusions: The Vibrio consortium found in YBD-infected corals in the Caribbean are close genetic relatives to those in the Indo-Pacific. The consortium directly attacks Symbiodinium spp. (zooxanthellae) within gastrodermal tissues, causing degenerated and deformed organelles, and depleted photosynthetic pigments in vitro and in situ. Infected Fungia spp. have decreased cell division compared with the healthy zooxanthellae: 4·9%vs 1·9%, (P ≥ 0·0024), and in D. heliopora from 4·7% to 0·7% (P ≥ 0·002). Significance and Impact of the Study: Pathogen virulence has major impacts on the survival of these important reef-building corals around the tropics.     

Biogeography of azooxanthellate corals in the Caribbean and surrounding areas

Biogeographic patterns for azooxanthellate corals are not as well known as those of zooxanthellate (primarily reef-building) corals. I analyzed occurrences of 129 species of azooxanthellate corals in 19 geopolitical regions in the Caribbean and surrounding areas. I performed an unweighted pair-group method with arithmetic averages (UPGMA) cluster analysis using Bray-Curtis' similarity measure on the complete data set and shallow- and deep-water subsets of the data. The results indicate two provinces, each with a widespread (tropical and subtropical distributions) component to its fauna. One province has a tropical and primarily insular component to it, while the other has a subtropical and primarily continental component. By contrast, zooxanthellate corals have a uniform faunal composition throughout the Caribbean. Moreover, zooxanthellate corals have half as many species in the Caribbean as the azooxanthellate corals even though their global diversities are equal. These differences in diversity and geographic distribution patterns should be considered when developing conservation strategies.     

Towards a knowledge of marine boundaries using ascidians as indicators: characterising transition zones for species distribution along Atlantic-Mediterranean shores

Two methodological approaches are compared with regard to their usefulness for providing explanations of observed faunal differences along Atlantic-Mediterranean coasts. A set of distribution data of ascidians containing 519 species and 80 genera was used for this purpose. Similarity methods were applied to establish the faunal affinities between distribution areas, and the measurement of β diversity and ecological distances along unidimensional gradients by non-lineal rescaling (using Detrended Correspondence Analysis) was undertaken for determining the steepness of ecotones existing along spatial gradients; these were analysed to detect the principal faunal changes, as well as their concordance with the commonly accepted limits for the classical biogeographical areas. There are fewer widely distributed species of shallow-water ascidians than in the Indo-Pacific region. Marked environmental changes within the Atlantic Ocean translate into significant differences in the composition of ascidian assemblages both in a latitudinal range and between the western and eastern sides. Few species show an amphi-Adantic range and most of these correspond with typically cosmopolitan species which are in general associated with shipping traffic or other forms of man-made transport. Three main endemism areas can be distinguished for Adantic-Mediterranean ascidian fauna involving genera and species: Caribbean, Mediterranean and south-west African. The rest of the shallow-water regions act as transitional or buffer zones where the genetic flows are generally maintained, although an increase in the number of certain species is found in some areas. This transitional role is mosdy found in the European Adantic coasts from the British Isles towards the Senegalian subregion, where gradual changes in ascidian populations occur: cold-water and tropical species at their southern and northern boundaries are substituted by temperate and subtropical species at the entrance of the Mediterranean.     

Folliculinid ciliates: a new threat to Caribbean corals?

This is the first report of a putative pathogenic ciliate protozoan that has been associated with Caribbean corals. Previously, only 2 species of the phylum Ciliophora had been linked to coral diseases, and they were exclusive to the Indo-Pacific region. In this study, a ciliate of the genus Halofolliculina was found on 10 hard coral species at the National Parks of Los Roques and Morrocoy, Venezuela. The general morphology of this ciliate is very similar to that of Halofolliculina corallasia from the Indo-Pacific, which is known to cause skeletal eroding band. None of the other 31 genera in the family Folliculinidae are known to cause diseases in corals or in any other animal species. The presence of this ciliate, which shows a prevalence comparable to that of other epizootics in the Caribbean, suggests it could be a new threat to the coral reefs of this region.     

Coral growth and reef growth: a brief review

The growth potential of modern zooxanthellate corals from the major reef provinces is reviewed with respect to Holocene reef growth. Both coral growth and reef growth is enhanced globally at the beginning of the Holocene and is maintained regionally in the Caribbean Sea up to the present in contrast to reefs of the Indo-Pacific Ocean. This regional difference is mainly caused by the siphoning effect of the tropical Atlantic, which is characterised still by a rising sea level in contrast to global ocean. Hence, Indo-Pacific reefs exhibit a well-cemented reef crest and reef roof barren of living corals. The evaluation of reef growth rates throughout the Phanerozoic shows reduced growth rates of more than one order of magnitude in comparison to their modern counterparts. This is a result of compaction and diagenesis but also strongly biased by uncertainties in absolute dating. Point counting of individual framebuilders with known growth rate may result in more comparative figures for growth rates of fossil reefs with respect to modern ones.     

Comparisons of sexual reproduction in Carijoa riisei (Cnidaria,Alcyonacea) in South Atlantic,Caribbean, and Pacific areas

Soft corals show a wide variety of reproductive strategies, including both asexual and sexual reproduction which can influence macro-evolutionary processes. The octocoral Carijoa riisei has an ample geographical distribution in Pacific and southern Atlantic and also in Caribbean region. This species was considered invasive in Hawaii, and its capacity for rapid proliferation is recognized, but recent studies, however, have indicated that it appears to be native to the Indo-Pacific region. The present study examined the reproductive biology of C. riisei in the Atlantic basin. The results were then compared to previous studies of the same species from the Pacific (Hawaii) and Caribbean (Puerto Rico) regions to examine the hypothesis that the reproductive patterns of C. riisei populations are the same throughout its geographical distribution, independent of its native or non-native status. Samples were collected on a monthly basis from May/2007 to April/2008 at Porto de Galinhas (Pernambuco State, Brazil). This species was found to have similar reproduction patterns in Brazil, the Caribbean, and in Hawaii (a gonochoric reproductive pattern and continuous and asynchronous gamete release). The similarities of their traits contribute to its rapid proliferation and occupation of spaces left by other species, independent of its native or non-native status.     

Global disparity in the resilience of coral reefs

The great sensitivity of coral reefs to climate change has raised concern over their resilience. An emerging body of resilience theory stems largely from research carried out in a single biogeographic region; the Caribbean. Such geographic bias raises the question of transferability of concepts among regions. In this article, we identify factors that might predispose the Caribbean to its low resilience, including faster rates of macroalgal growth, higher rates of algal recruitment, basin-wide iron-enrichment of algal growth from aeolian dust, a lack of acroporid corals, lower herbivore biomass and missing groups of herbivores. Although mechanisms of resilience are likely to be ubiquitous, our analysis suggests that Indo-Pacific reefs would have to be heavily degraded to exhibit bistability or undergo coral-macroalgal phase shifts.     

Distribution of a nematocyst-bearing sponge in relation to potential coral donors

Haliclona sp. 628 (Demospongiae, Haplosclerida, Chalinidae), a sponge found on the reef slope below 5 m depth on the Great Barrier Reef, has two unusual characteristics. It contains a symbiotic dinoflagellate, Symbiodinium sp., similar in structure to the dinoflagellate found within Acropora nobilis (S. microadriaticum), and it contains coral nematocysts randomly distributed between the ectosome and endosome and usually undischarged in intact sponge tissue. Given the unusual occurrence of nematocysts in Haliclona sp. 628, the focus of this study was to determine the distribution of this species of sponge on the reef slope at Heron Island Reef in relation to the distribution of potential coral donors. A combination of line and belt transects was used to estimate the abundance of Haliclona sp. 628 and a co-occurring congener, Haliclona sp. 1031, which does not contain nematocysts, at three widely separated sites on the reef slope at Heron Island Reef. The abundance of different types of substratum (sand, sand-covered coral rubble, dead A. nobilis, live A. nobilis, other live coral, and other dead coral) along the transects and the substratum to which each sponge colony was attached were also recorded. Despite the predominance of live A. nobilis and sand-covered rubble at all sites, between 30 and 55% of Haliclona sp. 628 colonies were attached to dead A. nobilis which comprised less than 8% of the available substratum along any transect. In contrast, Haliclona sp. 1031 was found significantly more frequently on other dead corals and less frequently on live A. nobilis than would be expected based on the availability of the different substrata in the sites. Potential explanations to account for the distribution of Haliclona sp. 628 in relation to potential coral donors are discussed.     

A preliminary assessment of the invasiveness of the Indo-Pacific sponge Chalinula nematifera on coral communities from the tropical Eastern Pacific

This is the first report of a sponge that overgrows live corals in the tropical Eastern Pacific ocean. Chalinula nematifera, native from the Indo-Pacific region, is an invasive sponge recorded for the first time in 2003 on coral communities from the Isla Isabel National Park (Mexican Pacific Ocean). Later, in 2006, it was found also on coral reefs from the Cabo Pulmo National Park; 217 nautical miles far away. It has been suggested that C. nematifera was introduced as fouling on ship hulls that have arrived at Isla Isabel from the Indo-Pacific. In this paper we examined the habitat specificity and the distribution and abundance through time of C. nematifera. While there were no significant variations in abundance through time, this species showed a very high specificity for living on live corals of the genus Pocillopora (94% vs. 6% on rocks). One of the environmental parameters that may explain this specificity for ramified corals is the low light intensity inside the coral colony, which was 96% lower than outside it. Coral reefs are currently struggling with a multitude of impacts that have weakened their resilience and pushed them away from equilibrium. As a result, more attention on ecology of corals is necessary. Although the abundance of C. nematifera seems to be stable, long-term monitoring programs (including studies of growth rates and recruitment) are needed to determine if this species could represent a threat to the Mexican coral ecosystem in the future.     

Geographic patterns of coral bioerosion: A productivity hypothesis

The numbers of boring bivalves in corals in large museum collections were used to indicate relative bioerosional damage to the corals. The proportion of corals from different locations that contain boring bivalves is highly correlated with global patterns of plankton primary productivity. The densities of five other, non-boring, groups of plantivores associated with the same corals are similarly correlated with productivity.The proportion of corals containing boring bivalves and the number of boring bivalves per coral head can be ranked by region as follows: eastern Pacific > western Atlantic > Indian Ocean > western Pacific. This ranking also corresponds to primary productivity differences.Measurements of the basal, margin of live tissue, and maximum circumstances of the coral heads indicate that western Atlantic massive corals have more of their skeletal surface exposed to borers, i.e. not covered by live tissue, than do Indo-Pacific corals. Consequently, the former also have weaker basal attachments which suggests that they are more likely to be dislodged during storms. The reason why massive corals in the western Atlantic tend to have less of their skeleton covered by live tissue than corals in the rest of the world is unknown.     

Sea surface temperature and the growth of the West Atlantic reef-building coral Montastraea annularis

Relationships were analyzed between sea surface temperature (SST) and annual growth characteristics (density, extension rate and calcification rate) of the Caribbean reef-building coral Montastraea annularis. Colonies were collected from 12 localities in the Gulf of Mexico and the Caribbean Sea. Two well-separated relationships were found, one for the Gulf of Mexico and the other for the Caribbean Sea. Calcification rate and skeletal density increased with increasing SST in both regions, while extension rate tended to decrease. Calcification rate increased ∼0.57 g cm⁻² year⁻¹ for each 1 °C increase in SST. Zero calcification was projected to occur at 23.7 °C in corals from the Gulf of Mexico and at 25.5 °C in corals from the Caribbean Sea. The 24 °C annual average SST isotherm marks the northern limit of distribution of M. annularis. Montastraea annularis populations of the Gulf of Mexico are isolated from those of the Caribbean Sea, and results indicate that corals from the Gulf of Mexico are adapted to growth at lower minimum and average annual SST. Corals from both the Gulf of Mexico and the Caribbean Sea, growing at lower SSTs and having lower calcification rates, extend their skeletons the same or more than those growing at higher SSTs. They achieve this by putting more of their calcification resources into extension and less into thickening, i.e., by sacrificing density.     

Development of gene expression markers of acute heat-light stress in reef-building corals of the genus Porites

Coral reefs are declining worldwide due to increased incidence of climate-induced coral bleaching, which will have widespread biodiversity and economic impacts. A simple method to measure the sub-bleaching level of heat-light stress experienced by corals would greatly inform reef management practices by making it possible to assess the distribution of bleaching risks among individual reef sites. Gene expression analysis based on quantitative PCR (qPCR) can be used as a diagnostic tool to determine coral condition in situ. We evaluated the expression of 13 candidate genes during heat-light stress in a common Caribbean coral Porites astreoides, and observed strong and consistent changes in gene expression in two independent experiments. Furthermore, we found that the apparent return to baseline expression levels during a recovery phase was rapid, despite visible signs of colony bleaching. We show that the response to acute heat-light stress in P. astreoides can be monitored by measuring the difference in expression of only two genes: Hsp16 and actin. We demonstrate that this assay discriminates between corals sampled from two field sites experiencing different temperatures. We also show that the assay is applicable to an Indo-Pacific congener, P. lobata, and therefore could potentially be used to diagnose acute heat-light stress on coral reefs worldwide.     

First report of folliculinid ciliates affecting Caribbean scleractinian corals

This is the first report of a ciliate of the genus Halofolliculina infecting hard coral species of six families (Acroporidae, Agaricidae, Astrocoeniidae, Faviidae, Meandrinidae and Poritidae) and milleporids in the Caribbean. Surveys conducted during 2004–2005 in Venezuela, Panama and México confirmed that this ciliate affects up to 25 scleractinian species. The prevalence of this ciliate at the coral community level was variable across sites, being most commonly found at Los Roques, Venezuela, and at Bocas del Toro, Panama (prevalence 0.2–2.5%), but rarely observed in the Mexican Caribbean. Ciliates were more prevalent within populations of acroporids (Acropora palmata, Acropora cervicornis and Acropora prolifera) in Los Roques. Recent observations also corroborate the presence of these ciliates in Curacao and Puerto Rico. Our observations indicate that ciliates affecting corals have a wider distribution than previously thought, and are no longer exclusively found in the Indo-Pacific and Red Sea.