Andrew Heyward

Natural inducers for coral larval metamorphosis

Abstract Coral gametes from Acropora millepora (Ehrenberg, 1834) and from multi-species spawning slicks provided larvae for use in metamorphosis assays with a selection of naturally occurring inducer chemicals. Four species of crustose coralline algae, one non-coralline crustose alga and two branching coralline algae induced larval metamorphosis. However, one additional species of branching coralline algae did not produce a larval response. Metamorphosis was also observed when larvae were exposed to skeleton from the massive coral Goniastrea retiformis (Lamarck, 1816) and to calcified reef rubble, demonstrating metamorphosis is possible in the absence of encrusting algae. Chemical extracts from these algae and the coral skeleton, obtained using either decalcification or simple methanol extraction procedures, also contained active inducers. These results extend the number of crustose algal species known to induce coral metamorphosis, suggest that some inducers may not necessarily be strongly associated with the calcified algal cell walls, and indicate that inducer sources in reef habitats may be more diverse than previously reported.

Metamorphosis of a Scleractinian Coral in Response to Microbial Biofilms

ABSTRACT Microorganisms have been reported to induce settlement and metamorphosis in a wide range of marine invertebrate species. However, the primary cue reported for metamorphosis of coral larvae is calcareous coralline algae (CCA). Herein we report the community structure of developing coral reef biofilms and the potential role they play in triggering the metamorphosis of a scleractinian coral. Two-week-old biofilms induced metamorphosis in less than 10% of larvae, whereas metamorphosis increased significantly on older biofilms, with a maximum of 41% occurring on 8-week-old microbial films. There was a significant influence of depth in 4- and 8-week biofilms, with greater levels of metamorphosis occurring in response to shallow-water communities. Importantly, larvae were found to settle and metamorphose in response to microbial biofilms lacking CCA from both shallow and deep treatments, indicating that microorganisms not associated with CCA may play a significant role in coral metamorphosis. A polyphasic approach consisting of scanning electron microscopy, fluorescence in situ hybridization (FISH), and denaturing gradient gel electrophoresis (DGGE) revealed that coral reef biofilms were comprised of complex bacterial and microalgal communities which were distinct at each depth and time. Principal-component analysis of FISH data showed that the Alphaproteobacteria, Betaproteobacteria, Gammaproteobacteria, and Cytophaga-Flavobacterium of Bacteroidetes had the largest influence on overall community composition. A low abundance of Archaea was detected in almost all biofilms, providing the first report of Archaea associated with coral reef biofilms. No differences in the relative densities of each subdivision of Proteobacteria were observed between slides that induced larval metamorphosis and those that did not. Comparative cluster analysis of bacterial DGGE patterns also revealed that there were clear age and depth distinctions in biofilm community structure; however, no difference was detected in banding profiles between biofilms which induced larval metamorphosis and those where no metamorphosis occurred. This investigation demonstrates that complex microbial communities can induce coral metamorphosis in the absence of CCA.

Monitoring of Benthic Reference Sites: Using an Autonomous Underwater Vehicle

We have established an Australia-wide observation program that exhibits recent developments in autonomous underwater vehicle (AUV) systems to deliver precisely navigated time series benthic imagery at selected reference stations on Australias continental shelf. These observations are designed to help characterize changes in benthic assemblage composition and cover derived from precisely registered maps collected at regular intervals. This information will provide researchers with the baseline ecological data necessary to make quantitative inferences about the long-term effects of climate change and human activities on the benthos. Incorporating a suite of observations that capitalize on the unique capabilities of AUVs into Australias integrated marine observation system (IMOS) [1] is providing a critical link between oceanographic and benthic processes. IMOS is a nationally coordinated program designed to establish and maintain the research infrastructure required to support Australias marine science research. It has, and will maintain, a strategic focus on the impact of major boundary currents on continental shelf environments, ecosystems, and biodiversity. The IMOS AUV facility observation program is designed to generate physical and biological observations of benthic variables that cannot be cost effectively obtained by other means.

Inhibition of fertilization and larval metamorphosis of the coral Acropora millepora (Ehrenberg, 1834) by petroleum products

Accidental oil spills from ships or rigs and inputs of effluent such as production formation water (PFW) are key perceived threats to tropical biota from industry activities. Scleractinian corals are an important functional component of tropical reefs and the abundance, diversity and resilience of coral communities can be used as an indicator of ecosystem health. In this paper, we report the effects of petroleum products, including water accommodated fractions (WAF) of crude oil, PFW and dispersant (Corexit 9527), on fertilization and larval metamorphosis of the widespread scleractinian coral, Acropora millepora (Ehrenberg, 1834) in laboratory-based assays. At 20% v/v PFW fertilization was inhibited by 25%. This concentration was equivalent 0.0721 mg l−1 total hydrocarbon (THC). In contrast, larval metamorphosis was more sensitive to this effluent, with 98% metamorphosis inhibited at the same concentration. Crude oil WAF did not inhibit fertilization of gametes until dispersant was introduced. Dispersed oil was slightly more toxic to fertilization than dispersant alone, suggesting toxicity to that event may be additive. The minimum concentration of dispersed oil which inhibited fertilization was 0.0325 mg l−1 THC. Larval metamorphosis was more sensitive than fertilization to crude oil. Although crude oil and dispersant inhibited larval metamorphosis individually, this toxicity was magnified when larvae were exposed to combinations of both. Crude oil inhibited metamorphosis at 0.0824 mg l−1 THC and at 0.0325 mg l−1 THC when dispersed in 10% v/v (dispersant/oil). Management of petroleum-related risks to spawning corals should consider not only the occurrence of the annual coral spawning event, but also the subsequent 1–3-week period during which most larval metamorphosis and recruitment occur.

Differing effects of thermal stress on coral fertilization and early embryogenesis in four Indo Pacific species

Coral reefs are expected to be severely impacted by rising seawater temperatures associated with climate change. The fertilization and early embryogenesis of four reef-building coral species representing three Indo-Pacific families were examined in a series of laboratory experiments where temperatures were increased up to 5–6°C at ambient. High levels of fertilization and normal embryogenesis were observed for Favites abdita, Favites chinensis and Mycedium elephantotus at temperatures to 32°C (+5°C) and embryos developed normally until the 5th cell cleavage. Acropora millepora was the only species to be affected by higher temperatures, exhibiting significantly reduced fertilization and a higher frequency of embryonic abnormalities at 32°C (+4°C), and fertilization ceased altogether at 34°C (+6°C). Early cell cleavage rates increased with temperature up to 32°C for all species.

Understanding ship-grounding impacts on a coral reef: potential effects of anti-foulant paint contamination on coral recruitment.

The 184 m cargo ship Bunga Teratai Satu collided with Sudbury Reef, part of the Great Barrier Reef and remained grounded for 12 days. The ship was re-floated only 3 days prior to the November 2000 mass coral spawning. No cargo or fuel was lost but the impact resulted in significant contamination of the reef with anti-foulant paint containing tributyltin (TBT), copper (Cu) and zinc (Zn). Larvae of the reef-building scleractinian coral Acropora microphthalma were exposed to various concentrations of sediment collected from the grounding site in replicated laboratory experiments. Two experiments were performed, both of which used varying ratios of contaminated and control site sediment in seawater as treatments. In the first experiment, the influence of contaminated sediment on larval competency was examined using metamorphosis bioassays. In the second, the effect of contaminated sediment upon larval recruitment on pre-conditioned terracotta tiles was assessed. In both experiments, sediment containing 8.0 mg kg(-1) TBT, 72 mg kg(-1) Cu and 92 mg kg(-1) Zn significantly inhibited larval settlement and metamorphosis. At this level of contamination larvae survived but contracted to a spherical shape and swimming and searching behaviour ceased. At higher contamination levels, 100% mortality was recorded. These results indicate that the contamination of sediment by anti-fouling paint at Sudbury Reef has the potential to significantly reduce coral recruitment in the immediate vicinity of the site and that this contamination may threaten the recovery of the resident coral community unless the paint is removed.

Resilience of coral communities on an isolated system of reefs following catastrophic mass-bleaching

As a result of climate change, sea-water temperatures around the world are expected to increase, potentially causing more frequent and severe episodes of coral bleaching. In this study, the impact of elevated water temperatures at an isolated system of reefs was assessed by quantifying the changes in benthic communities over almost 10 years. Mass-coral bleaching in 1998 dramatically altered the community structure of the reefs, including a >80% relative decrease in the cover of hard and soft corals and a twofold increase in the cover of algae, but which did not include macroalgae. The magnitude of the impact varied among the different sites according to their initial cover and community structure, largely due to the differing susceptibilities of the dominant groups of hard corals. Subsequent increase in the cover of these groups varied according to their life history traits, such as modes of reproduction and rates of growth. Additionally, the increase in cover was strongly correlated with the magnitude of the impact at the different sites, suggesting that recovery was driven by processes acting over local scales. Six years after the bleaching, the hard corals had returned to approximately 40% of their pre-bleaching cover, but there was little change in the cover of soft corals, and the structure of most hard coral communities remained very different to that prior to the bleaching. These data provides insights into the degree to which coral communities are resilient to catastrophic disturbances, when they are isolated from other reef systems but not exposed to some of the chronic stressors affecting many reefs around the world.

Niche specialization of reef-building corals in the mesophotic zone: metabolic trade-offs between divergent Symbiodinium types

The photobiology of two reef corals and the distribution of associated symbiont types were investigated over a depth gradient of 0–60 m at Scott Reef, Western Australia. Pachyseris speciosa hosted mainly the same Symbiodinium C type similar to C3 irrespective of sampling depth. By contrast, Seriatopora hystrix hosted predominantly Symbiodinium type D1a or D1a-like at shallow depths while those in deeper water were dominated by a Symbiodinium C type closely related to C1. The photosynthesis/respiration (P/R) ratio increased consistently with depth at the two sampling times (November 2008 and April 2009) for P. speciosa and in November 2008 only for S. hystrix, suggesting a reduction in metabolic energy expended for every unit of energy obtained from photosynthesis. However, in April 2009, shallow colonies of S. hystrix exhibited decreased P/R ratios down to depths of approximately 23 m, below which the ratio increased towards the maximum depth sampled. This pattern was mirrored by changes in tissue biomass determined as total protein content. The depth of change in the direction of the P/R ratio correlated with a shift from Symbiodinium D to C-dominated colonies. We conclude that while photobiological flexibility is vital for persistence in contrasting light regimes, a shift in Symbiodinium type may also confer a functional advantage albeit at a metabolic cost with increased depth.

Habitat specialization in tropical continental shelf demersal fish assemblages

The implications of shallow water impacts such as fishing and climate change on fish assemblages are generally considered in isolation from the distribution and abundance of these fish assemblages in adjacent deeper waters. We investigate the abundance and length of demersal fish assemblages across a section of tropical continental shelf at Ningaloo Reef, Western Australia, to identify fish and fish habitat relationships across steep gradients in depth and in different benthic habitat types. The assemblage composition of demersal fish were assessed from baited remote underwater stereo-video samples (n = 304) collected from 16 depth and habitat combinations. Samples were collected across a depth range poorly represented in the literature from the fringing reef lagoon (1–10 m depth), down the fore reef slope to the reef base (10–30 m depth) then across the adjacent continental shelf (30–110 m depth). Multivariate analyses showed that there were distinctive fish assemblages and different sized fish were associated with each habitat/depth category. Species richness, MaxN and diversity declined with depth, while average length and trophic level increased. The assemblage structure, diversity, size and trophic structure of demersal fishes changes from shallow inshore habitats to deeper water habitats. More habitat specialists (unique species per habitat/depth category) were associated with the reef slope and reef base than other habitats, but offshore sponge-dominated habitats and inshore coral-dominated reef also supported unique species. This suggests that marine protected areas in shallow coral-dominated reef habitats may not adequately protect those species whose depth distribution extends beyond shallow habitats, or other significant elements of demersal fish biodiversity. The ontogenetic habitat partitioning which is characteristic of many species, suggests that to maintain entire species life histories it is necessary to protect corridors of connected habitats through which fish can migrate.

Multi-species spawning of corals in north-western Philippines

The Philippines has more than 30,000 km of reef area and hosts some of the world’s most diverse and endangered coral communities, however there is little information on patterns of coral reproduction (Bermas et al. 1992) and to date there are no published accounts of direct spawning observations. Sampling to determine the reproductive state of Acropora species and in situ observations of coral spawning was conducted in 2006 and 2007 at sites close to the Bolinao Marine Laboratory (BML) in northwestern Luzon, (16 22¢N 119 54¢E). Prior to the full moon in March 2006, 22 sampled Acropora species (67% of colonies, n = 208) contained white or pigmented oocytes large enough to be visible in branches that were fractured artificially underwater (for methods see Baird et al. 2002) suggesting a seasonal peak in reproduction from March to May. Night dives were carried out during the week following the full moons of 15 March and 14 April 2006; and 2 April, 2 May and 1 June 2007. Multi-species coral spawning was observed during all of the months of observation except in April 2007. Across all months of observation, a total of at least 36 scleractinian species belonging to 14 genera and 7 families (Acroporidae, Mussidae, Agariciidae, Faviidae, Oculinidae, Merulinidae and Poritidae) broadcast spawned (Fig. 1), with a maximum of 13 species observed on the fifth night after full moon in May 2007. Further studies are required to establish the extent of spawning at other times of the year and the reproductive patterns of corals elsewhere in the Philippines.