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      Larval Settlement: The Role of Surface Topography for Sessile Coral Reef Invertebrates

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          Abstract

          For sessile marine invertebrates with complex life cycles, habitat choice is directed by the larval phase. Defining which habitat-linked cues are implicated in sessile invertebrate larval settlement has largely concentrated on chemical cues which are thought to signal optimal habitat. There has been less effort establishing physical settlement cues, including the role of surface microtopography. This laboratory based study tested whether surface microtopography alone (without chemical cues) plays an important contributing role in the settlement of larvae of coral reef sessile invertebrates. We measured settlement to tiles, engineered with surface microtopography (holes) that closely matched the sizes (width) of larvae of a range of corals and sponges, in addition to surfaces with holes that were markedly larger than larvae. Larvae from two species of scleractinian corals ( Acropora millepora and Ctenactis crassa) and three species of coral reef sponges ( Luffariella variabilis, Carteriospongia foliascens and Ircinia sp.,) were used in experiments. L. variabilis, A. millepora and C. crassa showed markedly higher settlement to surface microtopography that closely matched their larval width. C. foliascens and Ircinia sp., showed no specificity to surface microtopography, settling just as often to microtopography as to flat surfaces. The findings of this study question the sole reliance on chemical based larval settlement cues, previously established for some coral and sponge species, and demonstrate that specific physical cues (surface complexity) can also play an important role in larval settlement of coral reef sessile invertebrates.

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          Larval experience and latent effects--metamorphosis is not a new beginning.

          For many years ecologists have documented the remarkable within-species variation inherent in natural systems-for example, variability in juvenile growth rates, mortality rates, fecundities, time to reproductive maturity, the outcomes of competitive interactions, and tolerance to pollutants. Over the past 20 years, it has become increasingly apparent that at least some of this variation may reflect differences in embryonic or larval experiences. Such experiences may include delayed metamorphosis, short term starvation, short term salinity stress, or exposure to sublethal concentrations of pollutants or sublethal levels of ultra violet irradiation. Latent effects-effects that have their origins in early development but that are first exhibited in juveniles or adults-have now been documented among gastropods, bivalves, echinoderms, polychaetes, crustaceans, bryozoans, urochordates, and vertebrates. The extent to which latent effects alter ecological outcomes in natural populations in the field, and the mechanisms through which they are mediated are largely unexplored.
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            Metamorphosis of a scleractinian coral in response to microbial biofilms.

            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.
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              Induction of Larval Metamorphosis of the Coral Acropora millepora by Tetrabromopyrrole Isolated from a Pseudoalteromonas Bacterium

              The induction of larval attachment and metamorphosis of benthic marine invertebrates is widely considered to rely on habitat specific cues. While microbial biofilms on marine hard substrates have received considerable attention as specific signals for a wide and phylogenetically diverse array of marine invertebrates, the presumed chemical settlement signals produced by the bacteria have to date not been characterized. Here we isolated and fully characterized the first chemical signal from bacteria that induced larval metamorphosis of acroporid coral larvae (Acropora millepora). The metamorphic cue was identified as tetrabromopyrrole (TBP) in four bacterial Pseudoalteromonas strains among a culture library of 225 isolates obtained from the crustose coralline algae Neogoniolithon fosliei and Hydrolithon onkodes. Coral planulae transformed into fully developed polyps within 6 h, but only a small proportion of these polyps attached to the substratum. The biofilm cell density of the four bacterial strains had no influence on the ratio of attached vs. non-attached polyps. Larval bioassays with ethanolic extracts of the bacterial isolates, as well as synthetic TBP resulted in consistent responses of coral planulae to various doses of TBP. The lowest bacterial density of one of the Pseudoalteromonas strains which induced metamorphosis was 7,000 cells mm−2 in laboratory assays, which is on the order of 0.1 –1% of the total numbers of bacteria typically found on such surfaces. These results, in which an actual cue from bacteria has been characterized for the first time, contribute significantly towards understanding the complex process of acroporid coral larval settlement mediated through epibiotic microbial biofilms on crustose coralline algae.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                11 February 2015
                2015
                : 10
                : 2
                : e0117675
                Affiliations
                [1 ]Marine Ecology Research Centre, School of Environment, Science and Engineering, Southern Cross University, PO Box 157, Lismore, 2480, New South Wales, Australia
                [2 ]MACRO—the Centre for Macroalgal Resources and Biotechnology, James Cook University, Townsville, 4811, Queensland, Australia
                [3 ]Australian Institute of Marine Science, PMB 3 Townsville, Queensland, 4810, Australia
                [4 ]AIMS@JCU, James Cook University, Townsville, 4811, Queensland, Australia
                [5 ]ARC Centre for Excellence for Coral Reef Studies, James Cook University, Townsville, 4811, Queensland, Australia
                [6 ]College of Public Health, Medical and Veterinary Sciences, Department of Molecular Sciences, James Cook University, Townsville, 4811, Queensland, Australia
                [7 ]CSIRO Manufacturing Flagship, Pigdons Road, Waurn Ponds, 3216, Victoria, Australia
                University of New South Wales, AUSTRALIA
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: SW RdN. Performed the experiments: SW MAW SS. Analyzed the data: SW MAW. Contributed reagents/materials/analysis tools: SW RdN AP. Wrote the paper: SW. Revised the paper: MAW SS AP RdN.

                Article
                PONE-D-14-15075
                10.1371/journal.pone.0117675
                4324781
                25671562
                7b5108f7-97f7-435e-8aa0-d59645ffbfa6
                Copyright @ 2015

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

                History
                : 6 April 2014
                : 16 November 2014
                Page count
                Figures: 6, Tables: 3, Pages: 16
                Funding
                This work was undertaken with funding to SW through the Great Barrier Reef Foundation and under permit G13/36138.1, issued by the Great Barrier Reef Marine Park Authority. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Custom metadata
                Data are available from Dryad under the DOI doi: 10.5061/dryad.7pd40.

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