Biodiversity, host specificity, and dominance by eusocial species among sponge-dwelling alpheid shrimp on the Belize Barrier Reef

Alpheid shrimp represent an abundant and diverse, but poorly characterized, component of the cryptic biodiversity of coral reefs worldwide. Sponge‐inhabiting alpheids provide a promising model system for exploring patterns of cryptic reef biodiversity because their habitats (hosts) are discrete and qualitatively distinct units. We tabulated data from 14 years of collections at Carrie Bow Cay, Belize to quantify patterns of diversity, host specificity, and dominance among sponge‐dwelling shrimp (Synalpheus), with special attention to eusocial species. From > 600 sampled sponges of 17 species, we recognized at least 36 Synalpheus shrimp species. Of these, 15 (42%) were new to science. Species accumulation curves suggest that we have sampled most of the Synalpheus diversity at Carrie Bow Cay. Diversity of sponge‐dwelling Synalpheus was slightly higher in shallow water, probably because of greater habitat diversity, than in deep water. Host specificity was surprisingly high, with > 50% of all shrimp species found in only a single sponge species each, although some shrimp species used as many as six hosts. Cohabitation of individual sponges by multiple shrimp species was rarer than expected by chance, supporting previous distributional and behavioural evidence that competition for hosts is strong and moulds patterns of host association. The fauna of most well‐sampled sponge species was dominated, both in numbers of individuals and in frequency of occurrence, by eusocial species. Eusocial shrimp species also inhabited a significantly greater number of sponge species than did non‐social shrimp. Consequently, > 65% of shrimp in our quantitative samples belonged to the four eusocial species, and on a per‐species basis, eusocial species were 17 times as abundant as non‐social species. Our data suggest that the highly diverse sponge‐dwelling shrimp assemblage of the Belize Barrier Reef is structured by competition, and that eusociality has allowed a small number of species to dominate the sponge resource.     

Enhanced particle-feeding capacity of corals on turbid reefs (Great Barrier Reef, Australia)

Reef corals occur across a wide range of habitats, from offshore clear waters to nearshore sediment-laden environments. This study tests the hypothesis that corals from turbid nearshore areas have greater capacity to utilise suspended sediment as a food source than conspecifics from less turbid and midshelf areas. The hypothesis was tested on two common and widespread coral species on the Great Barrier Reef (Pocillopora damicornis and Acropora millepora). The particle clearance rates of samples from more turbid reefs were two-fourfold those of conspecifics from less turbid and midshelf reefs. Rates of sediment ingestion were generally a linear function of sediment load indicating no significant saturation within the concentration range of 1–30 mg dry weight l⁻¹. Estimated assimilation efficiency of particulate ¹⁴C varied between 50 and 80%, and was maximised for midshelf A. millepora at the lowest sediment concentration, suggesting that heterotrophy is more efficient in oligotrophic habitats. Based on feeding-response curves, assimilation efficiencies, and published records of ambient particle concentrations, representatives of these species on turbid inshore reefs are 10–20 times more heterotrophic on suspended sediment than their conspecifics on less turbid and midshelf reefs. Accepted: 7 September 1999     

Large-scale bleaching of corals on the Great Barrier Reef

 The Great Barrier Reef (GBR) experienced its most intensive and extensive coral bleaching event on record in early 1998. Mild bleaching commenced in late January and intensified by late February/early March 1998. Broad-scale aerial surveys conducted of 654 reefs (∼23% of reefs on the GBR) in March and April 1998, showed that 87% of inshore reefs were bleached at least to some extent (>1% of coral cover) compared to 28% of offshore (mid- and outer-shelf) reefs. Of inshore reefs 67% had high levels of bleaching (>10% of coral) and 25% of inshore reefs had extreme levels of bleaching (>60% of coral). Fewer offshore reefs (14%) showed high levels of bleaching while none showed extreme levels of bleaching. Ground-truth surveys of 23 reefs, which experienced bleaching in intensities ranging from none to extreme, showed that the aerial survey data are likely to be underestimates of the true extent and intensity of bleaching on the GBR. The primary cause of this bleaching event is likely to be elevated sea temperature and solar radiation, exacerbated by lowered salinity on inshore and some offshore reefs in the central GBR. Accepted: 30 July 1998     

Genotypic diversity and gene flow in brooding and spawning corals along the Great Barrier Reef, Australia

Marine organisms exhibit great variation in reproductive modes, larval types, and other life-history traits that may have major evolutionary consequences. We measured local and regional patterns of genetic variation in corals along Australia's Great Barrier Reef to determine the relative contributions of sexual and asexual reproduction to recruitment and to infer levels of gene flow both locally (among adjacent sites, < 5 km apart) and regionally (among reefs separated by 500-1,200 km). We selected five common brooding species (Acropora cuneata, A. palifera, Pocillopora damicornis, Seriatopora hystrix, and Stylophora pistillata) and four broadcast spawners (Acropora hyacinthus, A. cytherea, A. millepora, and A. valida), which encompassed a wide range of larval types and potential dispersal capabilities. We found substantial genotypic diversity at local scales in six of the nine species (four brooders, two spawners). For these six, each local population displayed approximately the levels of multilocus genotypic diversity (Go) expected for outcrossed sexual reproduction (mean values of Go:Ge ranged from 0.85 to 1.02), although consistent single-locus heterozygous deficits indicate that inbreeding occurs at the scale of whole reefs. The remaining three species, the brooder S. hystrix and the spawners A. valida and A. millepora displayed significantly less multilocus genotypic diversity (Go) than was expected for outcrossed sexual reproduction (Ge) within each of several sites. Acropora valida and A. millepora showed evidence of extensive localized asexual replication: (1) a small number of multilocus (clonal) genotypes were numerically dominant within some sites (Go:Ge values were as low as 0.17 and 0.20): (2) single-locus genotype frequencies were characterized by both excesses and deficits of heterozygotes (cf. Hardy-Weinberg expectations), and (3) significant linkage disequilibria occurred. For the brooding S. hystrix Go:Ge values were also low within each of four sites (x = 0.48). However, this result most likely reflects the highly restricted dispersal of gametes or larvae, because levels of genetic variation among sites within reefs were extremely high (FSR = 0.28). For all species, we detected considerable genetic subdivision among sites within each reef (high FSR-values), and we infer that larval dispersal is surprisingly limited (i.e., Nem among sites ranging from 0.6 to 3.3 migrants per generation), even in species that have relatively long planktonic durations. Nevertheless, our estimates of allelic variation among reefs (FRT) also imply that for all four broadcast spawning species and three of the brooders, larval dispersal is sufficient to maintain moderate to high levels of gene flow along the entire Great Barrier Reef (i.e., Nem among reefs ranged from 5 to 31). In contrast, widespread populations of S. hystrix and S. pistilata (the two remaining brooders) are relatively weakly connected (Nem among reefs was 1.4 and 2.5, respectively). We conclude that most recruitment by corals is very local, particularly in brooders, but that enough propagules are widely dispersed to ensure that both broadcast spawning and brooding species form vast effectively panmictic populations on the Great Barrier Reef.     

Congruent patterns of connectivity can inform management for broadcast spawning corals on the Great Barrier Reef

Connectivity underpins the persistence and recovery of marine ecosystems. The Great Barrier Reef (GBR) is the world's largest coral reef ecosystem and managed by an extensive network of no‐take zones; however, information about connectivity was not available to optimize the network's configuration. We use multivariate analyses, Bayesian clustering algorithms and assignment tests of the largest population genetic data set for any organism on the GBR to date (Acropora tenuis, >2500 colonies; >50 reefs, genotyped for ten microsatellite loci) to demonstrate highly congruent patterns of connectivity between this common broadcast spawning reef‐building coral and its congener Acropora millepora (~950 colonies; 20 reefs, genotyped for 12 microsatellite loci). For both species, there is a genetic divide at around 19°S latitude, most probably reflecting allopatric differentiation during the Pleistocene. GBR reefs north of 19°S are essentially panmictic whereas southern reefs are genetically distinct with higher levels of genetic diversity and population structure, most notably genetic subdivision between inshore and offshore reefs south of 19°S. These broadly congruent patterns of higher genetic diversities found on southern GBR reefs most likely represent the accumulation of alleles via the southward flowing East Australia Current. In addition, signatures of genetic admixture between the Coral Sea and outer‐shelf reefs in the northern, central and southern GBR provide evidence of recent gene flow. Our connectivity results are consistent with predictions from recently published larval dispersal models for broadcast spawning corals on the GBR, thereby providing robust connectivity information about the dominant reef‐building genus Acropora for coral reef managers.     

Coral-mucus-associated Vibrio integrons in the Great Barrier Reef: genomic hotspots for environmental adaptation

Integron cassette arrays in a dozen cultivars of the most prevalent group of Vibrio isolates obtained from mucus expelled by a scleractinian coral (Pocillopora damicornis) colony living on the Great Barrier Reef were sequenced and compared. Although all cultivars showed >99% identity across recA, pyrH and rpoB genes, no two had more than 10% of their integron-associated gene cassettes in common, and some individuals shared cassettes exclusively with distantly-related members of the genus. Of cassettes shared within the population, a number appear to have been transferred between Vibrio isolates, as assessed by phylogenetic analysis. Prominent among the mucus Vibrio cassettes with potentially inferable functions are acetyltransferases, some with close similarity to known antibiotic-resistance determinants. A subset of these potential resistance cassettes were shared exclusively between the mucus Vibrio cultivars, Vibrio coral pathogens and human pathogens, thus illustrating a direct link between these microbial niches through exchange of integron-associated gene cassettes.     

Ten microsatellite loci for the reef‐building coral Acropora millepora (Cnidaria,Scleractinia) from the Great Barrier Reef,Australia

Here we present nine novel, polymorphic microsatellite loci developed for the scleractinian coral Acropora millepora (Acroporidae) from the Great Barrier Reef. In addition, we have assessed the specificity and polymorphism of five microsatellite loci previously developed for a Caribbean congener and one locus developed for an Indo‐Pacific congener. Only one of the latter six loci produced reliable results, yielding a total of 10 polymorphic microsatellite loci for A. millepora. Variability was tested on 20–23 individuals from a single population, plus another ～10 individuals from each of three different populations, resulting in five to 20 alleles per locus.     

Geographic and habitat partitioning of genetically distinct zooxanthellae (Symbiodinium) in Acropora corals on the Great Barrier Reef

Intra- and intercolony diversity and distribution of zooxanthellae in acroporid corals is largely uncharted. In this study, two molecular methods were applied to determine the distribution of zooxanthellae in the branching corals Acropora tenuis and A. valida at several reef locations in the central section of the Great Barrier Reef. Sun-exposed and shaded parts of all colonies were examined. Single-stranded conformational polymorphism analysis showed that individual colonies of A. tenuis at two locations harbour two strains of Symbiodinium belonging to clade C (C1 and C2), whereas conspecific colonies at two other reefs harboured a single zooxanthella strain. A. valida was found to simultaneously harbour strains belonging to two distinct phylogenetic clades (C and D) at all locations sampled. A novel method with improved sensitivity (quantitative polymerase chain reaction using Taqman fluorogenic probes) was used to map the relative abundance distribution of the two zooxanthella clades. At two of the five sampling locations both coral species were collected. At these two locations, composition of the zooxanthella communities showed the same pattern in both coral species, i.e. correlation with ambient light in Pioneer Bay and an absence thereof in Nelly Bay. The results show that the distribution of genetically distinct zooxanthellae is correlated with light regime and possibly temperature in some (but not all) colonies of A. tenuis and A. valida and at some reef locations, which we interpret as acclimation to local environmental conditions.     

Palaeoecological evidence of a historical collapse of corals at Pelorus Island,inshore Great Barrier Reef,following European settlement

The inshore reefs of the Great Barrier Reef (GBR) have undergone significant declines in water quality following European settlement (approx. 1870 AD). However, direct evidence of impacts on coral assemblages is limited by a lack of historical baselines prior to the onset of modern monitoring programmes in the early 1980s. Through palaeoecological reconstructions, we report a previously undocumented historical collapse of Acropora assemblages at Pelorus Island (central GBR). High-precision U-series dating of dead Acropora fragments indicates that this collapse occurred between 1920 and 1955, with few dates obtained after 1980. Prior to this event, our results indicate remarkable long-term stability in coral community structure over centennial scales. We suggest that chronic increases in sediment flux and nutrient loading following European settlement acted as the ultimate cause for the lack of recovery of Acropora assemblages following a series of acute disturbance events (SST anomalies, cyclones and flood events). Evidence for major degradation in reef condition owing to human impacts prior to modern ecological surveys indicates that current monitoring of inshore reefs on the GBR may be predicated on a significantly shifted baseline.     

Bleaching of corals on the Great Barrier Reef: differential susceptibilities among taxa

Large-scale coral bleaching episodes are potentially major disturbances to coral reef systems, yet a definitive picture of variation in assemblage response and species susceptibilities is still being compiled. Here, we provide a detailed analysis of the bleaching response of 4160 coral colonies, representing 45 genera and 15 families, from two depths at four sites on reefs fringing inshore islands on the Great Barrier Reef. Six weeks after the onset of large-scale bleaching in 1998, between 11 and 83% of colonies along replicate transects were affected by bleaching, and mortality was 1 to 16%. There were significant differences in bleaching response between sites, depths and taxa. Cyphastrea, Turbinaria and Galaxea were relatively unaffected by bleaching, while most acroporids and pocilloporids were highly susceptible. The hydrocorals (Millepora spp.) were the most susceptible taxa, with 85% mortality. Spatial variation in assemblage response was linked to the taxonomic composition of reef sites and their bleaching history. We suggest, therefore, that much of the spatial variation in bleaching response was due to assemblage composition and thermal acclimation. Accepted: 14 January 2000     

Symbiodinium (Dinophyceae) community patterns in invertebrate hosts from inshore marginal reefs of the southern Great Barrier Reef,Australia

The broad range in physiological variation displayed by Symbiodinium spp. has proven imperative during periods of environmental change and contribute to the survival of their coral host. Characterizing how host and Symbiodinium community assemblages differ across environmentally distinct habitats provides useful information to predict how corals will respond to major environmental change. Despite the extensive characterizations of Symbiodinium diversity found amongst reef cnidarians on the Great Barrier Reef (GBR) substantial biogeographic gaps exist, especially across inshore habitats. Here, we investigate Symbiodinium community patterns in invertebrates from inshore and mid‐shelf reefs on the southern GBR, Australia. Dominant Symbiodinium types were characterized using denaturing gradient gel electrophoresis fingerprinting and sequencing of the ITS2 region of the ribosomal DNA. Twenty one genetically distinct Symbiodinium types including four novel types were identified from 321 reef‐invertebrate samples comprising three sub‐generic clades (A, C, and D). A range of host genera harbored C22a, which is normally rare or absent from inshore or low latitude reefs in the GBR. Multivariate analysis showed that host identity and sea surface temperature best explained the variation in symbiont communities across sites. Patterns of changes in Symbiodinium community assemblage over small geographic distances (100s of kilometers or less) indicate the likelihood that shifts in Symbiodinium distributions and associated host populations, may occur in response to future climate change impacting the GBR.     

Scarid Biomass on the Northern Great Barrier Reef: The Influence of Exposure, Depth and Substrata

Here I investigate whether patterns of scarid biomass across the continental shelf of the northern Great Barrier Reef can be explained by species associating with particular characteristics of the reef environment. Despite the widely documented tendency of scarids to graze and browse over exposed calcareous reef surfaces, scarid biomass was not significantly correlated with the availability of feeding substrata for any species investigated. Indeed positive correlations between biomass and substrata variables were rare for the 18 species investigated, indicating that biomass in these taxa was not strongly reliant on the availability of preferred substrata quantified at the spatial scale of sites (1620m²). Rather, species specific biomass was commonly highly variable between sites, suggesting that local aggregation of scarids commonly occurs at this scale. Such spatial patchiness potentially reflects the effects of spatially variable recruitment, fishes associating with unmeasured habitat characteristics or aggregating prior to spawning. Despite variability in the biomass of individual species between replicate sites within exposure regimes, exposure was generally a far more reliable predictor of biomass than the other variables quantified. This study provides little evidence to indicate that adult scarids have strict habitat requirements, rather they appear to be habitat generalists whose biomass is strongly influenced by exposure but weakly related to the cover of particular reef substratum.     

Species richness and community structure of reef-building corals on the nearshore Great Barrier Reef

Species richness, cover and community structure of reef-building corals were assessed at 599 sites on 135 reefs along the Great Barrier Reef (GBR) between 1994 and 2001, with focus on the nearshore area. Communities were described hierarchically, with smaller regional communities forming part of higher level communities at increasing spatial scales. Site richness increased from the coast to the mid-continental shelf, declining on the outer shelf. Richness also increased with depth to 5 m, stabilizing thereafter. An anomaly was present in a 400 km section adjacent to the northern, ‘wet tropics’ coast, where site richness was 67 and 41% lower than the adjacent far northern and central GBR, respectively; this was probably due to the disturbance regime, with an apparent anthropogenic component. Site richness also declined in the Southern GBR, probably due to naturally marginal conditions. All indicator species had highest values in five small Far Northern and Central GBR communities. In the eight depauperate communities no indicator species had high values, indicating that these communities represent degraded, yet potentially transitional forms of the more diverse communities of the Far Northern and Central GBR. The study shows that on the GBR, disturbance results in the local removal of corals rather than a shift to suites of other coral species.     

A new species of Halacarsantia Wolff, 1989 (Crustacea, Isopoda, Asellota, Santiidae) from Wistari Reef, southern Great Barrier Reef, Australia

Halacarsantia acutasp. n. is described from Wistari Reef, Capricorn Group, southern Great Barrier Reef, the first record of the genus from Australia. The new species differs from its congeners in having antenna flagellum composed of 8 articles; epipod apically acute, without setae, broad maxilliped endite and pereopod 1 basis with a short projection. A key to species of the genus is provided.     

The effect of sub-lethal increases in temperature on the growth and population trajectories of three scleractinian corals on the southern Great Barrier Reef

To date, coral death has been the most conspicuous outcome of warming tropical seas, but as temperatures stabilize at higher values, the consequences for the corals remaining will be mediated by their demographic responses to the sub-lethal effects of temperature. To gain insight into the nature of these responses, here I develop a model to test the effect of increased temperature on populations of three pocilloporid corals at One Tree Island, near the southern extreme of the Great Barrier Reef (GBR). Using Seriatopora hystrix, S. caliendrum and Pocillopora damicornis as study species, the effects of temperature on growth were determined empirically, and the dynamics of their populations determined under natural temperatures over a 6-month period between 1999 and 2000 [defined as the study year (SY)]. The two data sets were combined in a demographic test of the possibility that the thermal regime projected for the southern GBR in the next 55–83 years—warmer by 3°C than the study year (the SY+3 regime), which is equivalent to 1.4°C warmer than the recent warm year of 1998—would alter coral population trajectories through the effects on coral growth alone; the analyses first were completed by species, then by family after pooling among species. Laboratory experiments showed that growth rates (i.e., calcification) varied significantly among species and temperatures, and displayed curvilinear thermal responses with growth maxima at ∼27.1°C. Based on these temperature-growth responses, the SY+3 regime is projected to: (1) increase annualized growth rates of all taxa by 24–39%, and defer the timing of peak growth from the summer to the autumn and spring, (2) alter the intrinsic rate of population growth (λ) for S. hystrix (λ decreases 26%) and S. caliendrum (λ increases 5%), but not for P. damicornis, and (3) have a minor effect on λ (a 0.3% increase) for the Pocilloporidae, largely because λ varies more among species than it does between temperatures. Ten-year population projections suggest that the effects of a sub-lethal increase in temperature (i.e., the SY+3 regime) are relatively small compared to the interspecific differences in population dynamics, but nevertheless will alter the population size and increase the relative abundance of large colonies at the expense of smaller colonies for all three species, as well as the Pocilloporidae. These effects may play an important role in determining the nuances of coral population structure as seawater warms, and their significance may intensity if the coral species pool is depleted of thermally sensitive species by bleaching.     

Microbiological assessment of a disease outbreak on corals from Magnetic Island (Great Barrier Reef, Australia)

Unusual disease lesions were observed in Montipora corals on the fringing reef of Magnetic Island (Great Barrier Reef, Australia) following a period of high water temperature in early January 2002. Tissue death in Montipora spp. appeared as a black layer that spread rapidly across the colony surface, though this appeared as the final phase of disease progression (with three previous disease phases now identified, S. Anthony, unpublished). Culture and molecular-based microbial analysis of this layer did not identify a likely microbial pathogen. Despite this, DNA sequencing of microbial 16S rDNA indicated a shift in the bacterial population associated with affected coral tissue. A clone library of the healthy coral sample predominantly contained sequences within the -Proteobacteria. A disease coral sample representing the margin of the black lesion and healthy coral tissue was dominated by sequences, which demonstrated low sequence identity to a range of -Proteobacteria, -Proteobacteria and cyanobacteria. The microbes identified in the diseased Montipora spp. samples are likely to be opportunistic rather than the causative agent of the observed lesion. Studies are in progress to further characterise the ecology of this disease and describe the potential microbial pathogen(s).     

Benthic diatom community composition in three regions of the Great Barrier Reef,Australia

Despite their ecological importance, very little is known about the taxonomy and ecology of benthic diatoms in coral-reef ecosystems. Diatom densities and community compositions were investigated in three distinct regions of the Great Barrier Reef (GBR): (a) Wet Tropics (WT), (b) Princess Charlotte Bay (PCB), and (c) the Outer Shelf (OS). About 209 taxa were observed in the GBR sediments studied, with an average abundance of 2.55 × 10⁶ cells ml⁻¹ in the upper 1 cm of sediment. Total diatom abundances were about twice as high in inshore reefs of PCB and WT compared with OS reefs. A redundancy analysis (RDA) of diatom composition clearly grouped the three regions separately but showed little influence of grain size, nitrogen and organic carbon content of the sediments. The only distinct correlates were inorganic carbon and the distance to the mainland associated with OS communities. Analysis of similarity (ANOSIM) of diatom community composition revealed significant differences between all three regions. Indicator values showed that most highly abundant taxa occurred in all regions. However, several taxa were clearly identified as characteristic of particular regions. It is hypothesised that variations in nutrient and light availability are the most likely explanation for the observed differences in community composition.     

Shifts in coralline algae,macroalgae, and coral juveniles in the Great Barrier Reef associated with present‐day ocean acidification

Seawater acidification from increasing CO₂ is often enhanced in coastal waters due to elevated nutrients and sedimentation. Our understanding of the effects of ocean and coastal acidification on present‐day ecosystems is limited. Here we use data from three independent large‐scale reef monitoring programs to assess coral reef responses associated with changes in mean aragonite saturation state (Ω_ar) in the Great Barrier Reef World Heritage Area (GBR). Spatial declines in mean Ω_ar are associated with monotonic declines in crustose coralline algae (up to 3.1‐fold) and coral juvenile densities (1.3‐fold), while non‐calcifying macroalgae greatly increase (up to 3.2‐fold), additionally to their natural changes across and along the GBR. These three key groups of organisms are important proxies for coral reef health. Our data suggest a tipping point at Ω_ar 3.5–3.6 for these coral reef health indicators. Suspended sediments acted as an additive stressor. The latter suggests that effective water quality management to reduce suspended sediments might locally and temporarily reduce the pressure from ocean acidification on these organisms.     

Dynamics of seasonal outbreaks of black band disease in an assemblage of Montipora species at Pelorus Island (Great Barrier Reef,Australia)

Recurring summer outbreaks of black band disease (BBD) on an inshore reef in the central Great Barrier Reef (GBR) constitute the first recorded BBD epizootic in the region. In a 2.7 year study of 485 colonies of Montipora species, BBD affected up to 10 per cent of colonies in the assemblage. Mean maximum abundance of BBD reached 16±6 colonies per 100 m² (n=3 quadrats, each 100 m²) in summer, and decreased to 0–1 colony per 100 m² in winter. On average, BBD lesions caused 40 per cent tissue loss and 5 per cent of infections led to whole colony mortality. BBD reappearance on previously infected colonies and continuous tissue loss after the BBD signs had disappeared suggest that the disease impacts are of longer duration than indicated by the presence of characteristic signs. Rates of new infections and linear progression of lesions were both positively correlated with seasonal fluctuations in sea water temperatures and light, suggesting that seasonal increases in these environmental parameters promote virulence of the disease. Overall, the impacts of BBD are greater than previously reported on the GBR and likely to escalate with ocean warming.