Luke Smith

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.

Recovery of an isolated coral reef system following severe disturbance

Reef Repair Coral reefs suffer mass mortality because of coral bleaching, disease, and tropical storms, but we know much more about when, where, and how rapidly these ecosystems have collapsed than we do about their recovery. Gilmour et al. (p. 69; see the Perspective by Polidoro and Carpenter) studied a highly isolated coral reef before and after a climate-induced mass mortality event that killed 70 to 90% of the reef corals. The initial recovery of coral cover involved growth and survival of remnant colonies, which was followed by increases in larval recruitment. Thus, in the absence of chronic disturbance, even isolated reefs can recover from catastrophic disturbance. Isolated reefs with thriving herbivorous fish populations can recover rapidly after major bleaching events. [Also see Perspective by Polidoro and Carpenter] Coral reef recovery from major disturbance is hypothesized to depend on the arrival of propagules from nearby undisturbed reefs. Therefore, reefs isolated by distance or current patterns are thought to be highly vulnerable to catastrophic disturbance. We found that on an isolated reef system in north Western Australia, coral cover increased from 9% to 44% within 12 years of a coral bleaching event, despite a 94% reduction in larval supply for 6 years after the bleaching. The initial increase in coral cover was the result of high rates of growth and survival of remnant colonies, followed by a rapid increase in juvenile recruitment as colonies matured. We show that isolated reefs can recover from major disturbance, and that the benefits of their isolation from chronic anthropogenic pressures can outweigh the costs of limited connectivity.

Multiple scales of genetic connectivity in a brooding coral on isolated reefs following catastrophic bleaching

Understanding the pattern of connectivity among populations is crucial for the development of realistic and spatially explicit population models in marine systems. Here we analysed variation at eight microsatellite loci to assess the genetic structure and to infer patterns of larval dispersal for a brooding coral, Seriatopora hystrix, at an isolated system of reefs in northern Western Australia. Spatial autocorrelation analyses show that populations are locally subdivided, and that the majority of larvae recruit to within 100 m of their natal colony. Further, a combination of F‐ and R‐ statistics showed significant differentiation at larger spatial scales (2–60 km) between sites, and this pattern was clearly not associated with distance. However, Bayesian analysis demonstrated that recruitment has been supplemented by less frequent but recent input of larvae from outside the local area; 2–6% of colonies were excluded from the site at which they were sampled. Individual assignments of these migrants to the most likely populations suggest that the majority of migrants were produced at the only site that was not decimated by a recent and catastrophic coral bleaching event. Furthermore, the only site that recovered to prebleaching levels received most of these immigrants. We conclude that the genetic structure of this brooding coral reflects its highly opportunistic life history, in which prolific, philopatric recruitment is occasionally supplemented by exogenously produced larvae.

Ecologically relevant dispersal of corals on isolated reefs: implications for managing resilience

Coral reefs are in decline worldwide, and marine reserve networks have been advocated as a powerful management tool for maximizing the resilience of coral communities to an increasing variety, number, and severity of disturbances. However, the effective design of reserves must account for the spatial scales of larval dispersal that affect the demography of communities over ecological time frames. Ecologically relevant distances of dispersal were inferred from DNA microsatellite data in a broadcast-spawning (Acropora tenuis) and a brooding (Seriatopora hystrix) coral at isolated reef systems off northwest Australia. Congruent with expectations based on life histories, levels of genetic subdivision among populations were markedly higher in the brooder than in the broadcast spawner. Additionally, significant subdivision for both species between systems (>100 km), and between (>10 km) or within reefs (<10 km) within systems, indicated that many reefs or reef patches are demographically independent. There was also a clear distinction in the scale of genetic structure between the different systems; at the more geographically complex of the systems, a much finer scale structure was detected in both species. This suggested that the hydrodynamics associated with these complex reefs restrict distances regularly traveled by larvae. The primary implication is that short-term recovery of these coral communities after severe disturbance requires the input of larvae from viable communities kilometers to a few tens of kilometers away. Therefore, to be self-sustaining, we suggest that coral reef protected areas need to be large enough to encompass these routine dispersal distances. Further, to facilitate recovery from severe disturbances, protected areas need to be replicated over these spatial scales. However, specific designs also need to account for size, complexity, and isolation of reefs, which will either restrict or enhance dispersal within this range.

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.

Chronic Exposure of Corals to Fine Sediments: Lethal and Sub-Lethal Impacts

Understanding the sedimentation and turbidity thresholds for corals is critical in assessing the potential impacts of dredging projects in tropical marine systems. In this study, we exposed two species of coral sampled from offshore locations to six levels of total suspended solids (TSS) for 16 weeks in the laboratory, including a 4 week recovery period. Dose-response relationships were developed to quantify the lethal and sub-lethal thresholds of sedimentation and turbidity for the corals. The sediment treatments affected the horizontal foliaceous species (Montipora aequituberculata) more than the upright branching species (Acropora millepora). The lowest sediment treatments that caused full colony mortality were 30 mg l−1 TSS (25 mg cm−2 day−1) for M. aequituberculata and 100 mg l−1 TSS (83 mg cm−2 day−1) for A. millepora after 12 weeks. Coral mortality generally took longer than 4 weeks and was closely related to sediment accumulation on the surface of the corals. While measurements of damage to photosystem II in the symbionts and reductions in lipid content and growth indicated sub-lethal responses in surviving corals, the most reliable predictor of coral mortality in this experiment was long-term sediment accumulation on coral tissue.