Epilithic Cyanobacterial Communities of a Marine Tropical Beach Rock (Heron Island, Great Barrier Reef): Diversity and Diazotrophy

The diversity and nitrogenase activity of epilithic marine microbes in a Holocene beach rock (Heron Island, Great Barrier Reef, Australia) with a proposed biological calcification “microbialite” origin were examined. Partial 16S rRNA gene sequences from the dominant mat (a coherent and layered pink-pigmented community spread over the beach rock) and biofilms (nonstratified, differently pigmented microbial communities of small shallow depressions) were retrieved using denaturing gradient gel electrophoresis (DGGE), and a clone library was retrieved from the dominant mat. The 16S rRNA gene sequences and morphological analyses revealed heterogeneity in the cyanobacterial distribution patterns. The nonheterocystous filamentous genus Blennothrix sp., phylogenetically related to Lyngbya, dominated the mat together with unidentified nonheterocystous filaments of members of the Pseudanabaenaceae and the unicellular genus Chroococcidiopsis. The dominance and three-dimensional intertwined distribution of these organisms were confirmed by nonintrusive scanning microscopy. In contrast, the less pronounced biofilms were dominated by the heterocystous cyanobacterial genus Calothrix, two unicellular Entophysalis morphotypes, Lyngbya spp., and members of the Pseudanabaenaceae family. Cytophaga-Flavobacterium-Bacteroides and Alphaproteobacteria phylotypes were also retrieved from the beach rock. The microbial diversity of the dominant mat was accompanied by high nocturnal nitrogenase activities (as determined by in situ acetylene reduction assays). A new DGGE nifH gene optimization approach for cyanobacterial nitrogen fixers showed that the sequences retrieved from the dominant mat were related to nonheterocystous uncultured cyanobacterial phylotypes, only distantly related to sequences of nitrogen-fixing cultured cyanobacteria. These data stress the occurrence and importance of nonheterocystous epilithic cyanobacteria, and it is hypothesized that such epilithic cyanobacteria are the principal nitrogen fixers of the Heron Island beach rock.     

The behaviour of Abudefduf zonatus (Pisces,pomacentridae) at Heron Island,Great Barrier Reef

Social organization and reproductive behaviour of Abudefduf zonatus were studied at Heron Island, Great Barrier Reef. This species is closely associated with the sand and coral substrate of the inner reef flat zone. Territorial, clustering, nest-digging, breeding and parental care behaviours are described. Mature males maintain territories for several weeks or longer around empty clam shells in which periodic spawning occurs. Females and sub-adult males hold territories interspersed among those of adult males. No pair bonds are formed, and eggs are guarded only by males. Breeding is roughly synchronized among fish of one area. Clustering behaviour may contribute to breeding syndrony in local populations.     

Spatiotemporal patterns of coral disease prevalence on Heron Island,Great Barrier Reef,Australia

Despite increasing research effort on coral diseases, little is known about factors driving disease dynamics on the Great Barrier Reef (GBR). This is the first study to investigate the temporal patterns of coral disease prevalence and potential drivers of disease around Heron Island, in the southern Capricorn Bunker sector of the GBR. Surveys were conducted in two austral summers and three winters between November 2007 and August 2009 on six sites around the island. Six diseases were detected: brown band syndrome (BrB), growth anomalies (GA), ulcerative white spots (UWS), white syndrome (WS), skeletal eroding band disease (SEB) and black band disease (BBD). The lowest overall mean disease prevalence was 1.87 ± 0.75% (mean ± SE) in November 2007 and the highest 4.22 ± 1.72% in August 2008. There was evidence of seasonality for two diseases: BrB and UWS. This is the first study to report a higher prevalence of BrB in the winter. BrB had a prevalence of 3.29 ± 0.58% in August 2008 and 1.53 ± 0.28% in August 2009, while UWS was the most common syndrome in the summer with a prevalence of 1.12 ± 0.31% in November 2007 and 2.67 ± 0.52% prevalence in January 2008. The prevalence of GAs and SEB did not depend on the season, although the prevalence of GAs increased throughout the study period. WS had a slightly higher prevalence in the summer, but its overall prevalence was low (<0.5%). Sites with high abundance of staghorn Acropora and Montipora were characterised by the highest disease prevalence (12% of Acropora and 3.3% of Montipora species were diseased respectively). These results highlight the correlations between coral disease prevalence, seasonally varying environmental parameters and coral community composition. Given that diseases are likely to reduce the resilience of corals, seasonal patterns in disease prevalence deserve further research.     

Soundscape diversity in the Great Barrier Reef: Lizard Island,a case study

Passive acoustic monitoring can provide valuable information on coral reefs, and examining the acoustic attributes of these ecosystems has the potential to provide an insight into their status and condition. From 2014 to 2016, a series of underwater recordings were taken at field sites around Lizard Island in the Great Barrier Reef, Australia. Six individual fish choruses were identified where each chorus displayed distinct acoustic characteristics. Choruses exhibited diurnal activity and some field sites displayed consistently higher diversity of choruses and levels than others, suggesting that particular locations are important aggregation areas for soniferous fish species. During peak activity, choruses were a prominent component of reef soundscapes, where received levels of a chorus reached upwards of 120 dB re 1μPa rms over the 450–650 Hz band, equating to a 40 dB increase above ambient noise levels of ≈80 dB re 1μPa rms. Three out of the six detected choruses exhibited spectral and temporal characteristics similar to choruses previously documented at these sites and elsewhere, produced by planktivorous fish species. Three of these choruses appear to be undocumented and could hold information on the presence, abundance and dispersal patterns of important fish species, which may have potential long-term management applications. Future research should focus on extricating the temporal patterns associated with bioacoustic activity and determining the potential environmental drivers of biological choruses. Additionally, developing appropriate techniques for direct identification of vocalizing species would strongly increase the management applicability of passive acoustic monitoring.     

Variability in benthic diazotrophy and cyanobacterial diversity in a tropical intertidal lagoon

Benthic nitrogen fixation has been estimated to contribute 15 Tg N year(-1) to the marine nitrogen budget. With benthic marine nitrogen fixation being largely overlooked in more recent surveys, a refocus on benthic diazotrophy was considered important. Variations in nitrogenase activity (acetylene reduction-gas chromatography) in a tropical lagoon in the western Indian Ocean (Zanzibar, Tanzania) were monitored over a 3-year period (2003-2005) and related to cyanobacterial and diazotrophic microbial diversity using a polyphasic approach. Different nitrogenase activity patterns were discerned, with the predominant pattern being high daytime activities combined with low nighttime activities. Analyses of the morphological and 16S rRNA gene diversity among cyanobacteria revealed filamentous nonheterocystous (Oscillatoriales) and unicellular (Chroococcales) representatives to be predominant. Analyses of the nifH gene diversity showed that the major phylotypes belonged to noncyanobacterial prokaryotes. However, as shown by cyanobacterial selective nifH-denaturing gradient gel electrophoresis analysis, cyanobacterial nifH gene sequences were present at all sites. Several nifH and 16S rRNA gene phylotypes were related to uncultured cyanobacteria or bacteria of geographically distant habitats, stressing the widespread occurrence of still poorly characterized microorganisms in tropical benthic marine communities.     

Actinosporeans (Myxozoa) from marine oligochaetes of the Great Barrier Reef

Four species of actinosporeans are described from marine oligochaetes (all Tubificidae) from the Great Barrier Reef, Queensland, Australia. They developed in the coelom of the oligochaete and produced spores in groups of eight in the pansporocysts. The new genus Endocapsa is proposed within the family Sphaeractinomyxidae Janiszewska, 1957 on the basis that mature spores have small valve cell processes and non-protruding polar capsules. The type-species, Endocapsa rosulata n. sp., has three valve cell processes, which resemble a rosette, and submerged polar capsules. It infected Heterodrilus cf. keenani from Heron Island and morphologically similar parasites occurred in Thalassodrilides cf. gurwitschi and Heronidrilus sp. from Lizard Island. E. stepheni n. sp. has asymmetrical valve cell processes and submerged polar capsules. It was found in H. cf. keenani and H. queenslandicus from Heron Island. Sphaeractinomyxon leptocapsula n. sp. has thin widely spaced polar capsules and is described from Heronidrilus sp. from Lizard Island. S. ersei Hallett, O'Donoghue & Lester, 1998 infected Tubificidae gen. sp. from Heron Island and S. cf. ersei occurred in Bathydrilus sp., Thalassodrilides cf. gurwitschi and Limnodriloides lateroporus from Lizard Island.     

Effect of colony size and surrounding substrate on corals experiencing a mild bleaching event on Heron Island reef flat (southern Great Barrier Reef,Australia)

In January–May 2006, Heron Island in the Great Barrier Reef experienced a mild bleaching event. The effect of colony size, morphology and surrounding substrate on the extent of bleaching was explored. In contrast with previous studies, colony size did not influence bleaching sensitivity, suggesting that there may be a threshold of light and temperature stress beyond which size plays a role. Also contrasting with previous studies, massive corals were more affected by bleaching than branching corals. Massive corals surrounded by sand were more affected than the ones surrounded by rubble or dead coral. It is hypothesized that light reflectance from sand increases stress levels experienced by the colonies. This effect is maximized in massive corals as opposed to branching corals that form dense thickets on Heron Island. These results emphasize the importance of the ecological dynamics of coral communities experiencing low, moderate and high levels of bleaching for the understanding of how coral communities may change under the stress of climate change.     

Microbial diversity in marine biofilms along a water quality gradient on the Great Barrier Reef

Microbial communities are potential indicators for water quality as they respond rapidly to environmental changes. In the Whitsunday Islands, Australia, microbial biofilm communities from two offshore islands were compared to those from two inshore islands subjected to poor water quality. Biofilm community composition was characterized using three culture-independent molecular techniques. The clone libraries indicated high genetic diversity, with somewhat higher scores in the offshore sites (57%) compared to the inshore sites (41%). The majority of microbes in the biofilms were related to Alphaproteobacteria (39.8%), Gammaproteobacteria (14.1%), Bacteroidetes (13.2%), diatoms (8.3%) and Cyanobacteria (3.9%). Redundancy analysis (RDA) for the CARD-FISH data showed distinct microbial assemblages between offshore and inshore communities. Additionally, 5 out of 13 water quality parameters (DIN, Chla, POP, TSS and POC) explained a significant amount of variation in the microbial communities and high values of these were associated with inshore communities. Analysis of variance (ANOVA) indicated that Cyanobacteria (p = 0.01), Bacteroidetes (p = 0.04) and to some extent Alphaproteobacteria (p = 0.07), were significantly more abundant in the offshore biofilm communities. Principal Component Analysis (PCA) of DGGE data showed clear grouping of cyanobacterial communities into inshore and offshore communities. Reasons for community shifts in the bacterial lineages are currently not resolved. One possible causative factor may be that autotrophic primary producers are more dominant in offshore sites due to the higher light availability as well as the limitation by DIN. The trends found in this study are the bases for more detailed research on microbial indicator species for changes in water quality.     

Overstreetia olsoni n. sp. (Digenea: Zoogonidae) from the Capricorn silverside Atherinomorus capricornensis (Woodland) (Atherinidae) off Heron Island, southern Great Barrier Reef

A new species, Overstreetia olsoni, is described from Atherinomorus capricornensis off Heron Island on the Great Barrier Reef off Queensland, Australia. It differs from its only known congener in that the enlarged spines of the circum-oral rows are smaller ( ≤ 4.5 × 3.5 vs ≤ 21.5 × 10.5μm), the sucker-ratio is smaller (1: 0.97–1.01 vs 1:1.8) and the eggs are larger (40–45 × 22–28 vs 34–37 × 17–22μm).     

Hemiuridae (Digenea) from marine fishes of the Great Barrier Reef,Queensland, Australia

The following species are described, figured and/or recorded from the Great Barrier Reef at Heron Island or Lizard Island, Queensland, with comparative material reported from other areas of the ocean around Australia or New Guinea: Dinurus longisinus (new synonym: D. hippuri) from Seriola lalandi, Heron Island and Coryphaena hippurus, Papua New Guinea; Ectenurus trachuri from Caranx sexfasciatus, Diploprion bifasciatus, Pterocaesio marri, Seriola lalandi and Atherinomorus capricorniensis, Heron Island; Erilepturus hamati (with 25 new synonyms) from Lutjanus carponotatus, Lizard Island, Platycephalus bassensis, Coff's Harbour, NSW, P. fuscus, Coff's Harbour, NSW and Moreton Bay, Queensland, P. endrachtensis, Sillago analis, S. maculata, S. ciliata, Pseudorhombus arsius and Polydactylus sp. from Moreton Bay, Queensland and Lates calcarifer, Darwin, Northern Territory; Tubulovesicula angusticauda from Echeneis naucrates and Lethrinus miniatus, Heron Island and Anguilla reinhardtii, Moreton Bay and Bribie Island, Queensland; Elytrophalloides humerus from Trachinotus botla and T. coppingeri, Heron Island; Lecithochirium kawakawa from Euthynnus affinis Heron Island and Lizard Island: Lecithochirium cirrhiti (new synonyms: L. sammarae, L. nohu) from Sargocentron rubrum, Heron Island; Lecithochirium caesionis from Pterocaesio marri, heron Island; Plerurus digitatus (new synonyms: P. cynoglossi, P. atulis, P. scomberomori) from Plectropomus leopardus, Heron Island, Lutjanus erythropterus, Variola louti, Scomberomorus semifasciatus, Grammatorcynus bicarinatus and Carangoides embureyi, C. gymnostethoides, Lizard Island, Scomberomorus commerson, Heron Island, Lizard Island, New Britain, Papua New Guinea, Point Lookout, Queensland and Moreton Bay, Queensland, Euthynnus affinis Heron Island, Lizard Island and New Britain, Papua New Guinea, Sphyraena barracuda, Heron Island and Lizard Island, Scomberomorus munroi, S. queenslandicus and Saurida undosquamis, Moreton Bay, Queensland and Chirocentrus dorab, Bundaberg, Queensland. The Lecithochirium species-group Cirrhiti is considered indistiguishable from the species-group Lotellae.     

The dynamics of benthic microbial communities at Davies Reef,central Great Barrier Reef

The dynamics of benthic microbial communities were examined within different functional zones (reef crest, reef flat, lagoon) of Davies Reef, central Great Barrier Reef, in winter. Bacterial numbers did not change significantly across the reef with a mean abundance of 1.3 (±0.6) x 10⁹ cells g^-1 DW of sediment. Bacterial production, measured as thymidine incorporation into DNA, ranged from 1.2 (±0.2) to 11.6 (±1.5) mg C m^-2h^-1 across the reef and was significantly lower in a reef crest basin than in the other zones. Bacterial growth rates () across the reef (0.05 to 0.33 g^-1) correlated only with sediment organic carbon and nitrogen. Protozoan and meiofaunal densities varied by an order of magnitude across the reef and correlated with one or more sediment variables but not with bacterial numbers or growth rates. Nutrient flux rates were similar to those found at other reefs in the central and southern Great Barrier Reef and are significantly lower than rates measured in temperate sand communities. In the front lagoon, bioturbation and feeding acitivity by thalassinid shrimps (Callianassa spp.) negatively influenced microbial and meiofaunal communities with a net import of organic matter necessary to support the estimated rates of bacterial productivity. In lagoonal areas not colonized by shrimps, primary productivity (400–1100 mg C m^-2d^-1) from algal mats was sufficient to support bacterial growth. It is suggested that deposit-feeding macrobenthos such as thalassinid crustaceans play a major role in the tructuring and functioning of lower trophic groups (bacteria, microalgae, protozoa, meiofauna) in coral reef sedments, particularly in laggons.     

Sand and nest temperatures and an estimate of hatchling sex ratio from the Heron Island green turtle (Chelonia mydas) rookery, Southern Great Barrier Reef

Sand and nest temperatures were monitored during the 2002–2003 nesting season of the green turtle, Chelonia mydas, at Heron Island, Great Barrier Reef, Australia. Sand temperatures increased from ∼ 24°C early in the season to 27–29°C in the middle, before decreasing again. Beach orientation affected sand temperature at nest depth throughout the season; the north facing beach remained 0.7°C warmer than the east, which was 0.9°C warmer than the south, but monitored nest temperatures were similar across all beaches. Sand temperature at 100 cm depth was cooler than at 40 cm early in the season, but this reversed at the end. Nest temperatures increased 2–4°C above sand temperatures during the later half of incubation due to metabolic heating. Hatchling sex ratio inferred from nest temperature profiles indicated a strong female bias.     

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).     

The cercaria of Galactosomum bearupi Pearson, 1973 (Trematoda: Heterophyidae) at Heron and Masthead Islands,Great Barrier Reef,Australia

Magnacercous cercariae, all morphologically identical but with different coloured tails, were found naturally infecting the intertidal prosobranch gastropod Clypeomorus batillariaeformis Habe & Kosuge (Cerithiidae) at Heron and Masthead Islands. Several species of coral-dwelling fishes were exposed to magnacercous cercariae. Active ingestion by the fish, followed by the complete development of the metacercaria in the optic lobes, occurred in Pomacentrus molluccensis Bleeker, but not in Dascyllus aruanus (L.), where development stopped short after encystment. All cercariae turned out to belong to the same species, Galactosomum bearupi Pearson, 1973. Natural infections of G. bearupi metacercariae were found in eight species of fish at Heron Island: Pomacentrus molluccensis, P. wardi Whitley, P. bankanensis Bleeker, P. flavicauda Whitley, Stegastes cf. fasciolatus (Ogilby), Sillago maculata Quoy & Gaimard, S. cf. ciliata Cuvier and Crenimugil crenilabris (Forsskål). This represents the fourth account of the cercaria of a species of Galactosomum.     

Population dynamics of two snail species,Planaxis sulcatus and Cerithium moniliferum,and their trematode species at Heron Island,Great Barrier Reef

Summary The population dynamics of the prosobranch snail Planaxis sulcatus and its trematode parasites on 600 m of beachrock on the southern side of Heron Island, Great Barrier Reef, were studied. Populations of Planaxis show little mixing, due to lack of long-distance movements. From March 1973 to June 1975, an increase in the numbers of small and medium-sized snails occurred, but the biomass (dry tissue weight) of the snail population did not change. Snails were infected with one species of Aspidogastrea and six species of cerariae. Infections with cercariae did not significantly affect the relative weight of the snails. Multiple infections were random, i.e. neither negative nor positive interactions between trematode species could be demonstrated. Proportions of uninfected snails and snails infected with various trematode species remained more or less constant from July 1973 to February 1975.The population dynamics of the prosobranch snail Cerithium moniliferum and its 11 species of cercariae and one species of Aspidogastrea in a small area at Heron Island were studied. Numbers of large snails decreased and numbers of small snails increased from August 1973 to June 1975. The biomass of the Cerithium population increased only slightly. Prevalence of infection changed significantly only in large snails.Infections of Cerithium moniliferum and Peristernia australiensis with an aspidogastrid species decreased strongly from January 1971 to March/April 1972 and had not recovered by mid 1975.Seasonal fluctuations could not be demonstrated for any of the snails or parasites.The data for Planaxis suggest equilibrium conditions and saturation of the habitat.     

Reproductive development and timing of tropical sponges (Order Haplosclerida) from the Great Barrier Reef,Australia

Reproductive development of three species of the Haplosclerida, Haliclona amboinensis (Lévi 1961), Haliclona cymiformis (Esper 1794) and Niphates nitida Fromont (1993), was monitored for three years on a fringing reef in the central section of the Great Barrier Reef, Australia. All species are viviparous, and gonochoric. Haliclona amboinensis and N. nitida incubated eggs, embryos and larvae in brood chambers. The branching sponge. H. cymiformis, incubated eggs, embryos, and larvae along the central axis of branches. In all species, sperm cysts in high densities are evenly distributed throughout the mesohyl. Mature larvae of all species are creamy white, oval, parenchymella, with a dark coloured ring at the posterior pole. Eggs, embryos and larvae are present contemporaneously for periods of two consecutive months in individuals of H. cymiformis and seven months in H. amboinensis and N. nitida. The first observation of female reproductive products in H. amboinensis and N. nitida coincided with an increase in water temperature, while cessation of reproductive activity was associated with decreasing water temperature. Onset of reproduction in H. cymiformis coincided with peak sexual and vegetative reproductive activity of its algal symbiont, Ceratodictyon spongiosum.     

Holocene evolution of the granite based Lizard Island and MacGillivray Reef systems, Northern Great Barrier Reef

Radiocarbon dating of seven drill cores from both the windward Lizard Island fringing reef and the windward and leeward margins of MacGillivray platform reef, Northern Great Barrier Reef Province, reveal the Holocene evolution of these two mid shelf coral reefs. The windward margin at Lizard Island started growing approximately 6,700 calendar years before present (cal yr BP) directly on an assumed granite basement and approached present day sea level approximately 4,000 cal yr BP. Growth of the windward margin at MacGillivray Reef was initiated by 7,600 cal yr BP and approached present day sea level by approximately 5,600 cal yr BP. The leeward margin at MacGillivray was initiated by 8,200 cal yr BP also directly on an assumed granite basement, but only approached sea level relatively recently, between 260 and 80 cal yr BP. None of the cores penetrated the Holocene-Pleistocene unconformity. The absence of Pleistocene reefal deposits, at 15 m depth in the cores from MacGillivray Reef, raises the possibility that the shelf in this region has subsided relative to modern day sea level by at least 15 m since the last interglacial [125,000 years ago (ka)].     

Uncovering cryptic diversity of Lyngbya: the new tropical marine cyanobacterial genus Dapis (Oscillatoriales)

Cyanobacteria comprise an extraordinarily diverse group of microorganisms and, as revealed by increasing molecular information, this biodiversity is even more extensive than previously estimated. In this sense, the cyanobacterial genus Lyngbya is a highly polyphyletic group composed of many unrelated taxa with morphological similarities. In this study, the new genus Dapis was erected from the genus Lyngbya, based on a combined molecular, chemical, and morphological approach. Herein, two new species of cyanobacteria are described: D. pleousa and D. pnigousa. Our analyses found these species to be widely distributed and abundant in tropical and subtropical marine habitats. Seasonally, both species have the ability to form extensive algal blooms in marine habitats: D. pleousa in shallow‐water, soft bottom habitats and D. pnigousa on coral reefs below depths of 10 m. Electron microscopy showed that D. pleousa contains gas vesicles, a character not previously reported in Lyngbya. These gas vesicles, in conjunction with a mesh‐like network of filaments that trap oxygen released from photosynthesis, provide this species with an unusual mechanism to disperse in coastal marine waters, allowing D. pleousa to be present in both benthic and planktonic forms. In addition, both D. pleousa and D. pnigousa contained nitrogen‐fixing genes as well as bioactive secondary metabolites. Several specimens of D. pnigousa biosynthesized the secondary metabolite lyngbic acid, a molecule that has also been isolated from many other marine cyanobacteria. Dapis pleousa consistently produced the secondary metabolite malyngolide, which may provide a promising chemotaxonomic marker for this species.