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Metamorphosis of Broadcast Spawning Corals in Response to Bacteria Isolated from Crustose Algae

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Metamorphosis of Broadcast Spawning Corals in Response to Bacteria Isolated from Crustose Algae MARINE ECOLOGY PROGRESS SERIES Vol. 223: 121–131, 2001 Published November 28 Mar Ecol Prog Ser Metamorphosis of broadcast spawning corals in response to bacteria isolated from crustose algae A. P. Negri1,*, N. S. Webster1, R. T. Hill2, A. J. Heyward1 1Australian Institute of Marine Science, PMB 3, Townsville, Queensland 4810, Australia 2 Center of Marine Biotechnology, University of Maryland Biotechnology Institute, 701 East Pratt St., Baltimore, Maryland 21202, USA ABSTRACT: External chemical signals provide a mechanism for broadcast-spawning scleractinian corals to recognise suitable substrata for larval settlement and metamorphosis. These morphogens can be extracted from crustose coralline algae (CCA) and the skeletons of some coral species, how- ever the precise origin of the chemical inducers has not yet been conclusively demonstrated. Micro- organisms have been reported to induce metamorphosis in various species of echinoderms, molluscs, polychaetes and cnidarians. We report that Strain A3, a species of Pseudoalteromonas isolated from the CCA Hydrolithon onkodes (Heydrich), was able to induce significant levels (up to 51.5% ± 5.8 SE) of metamorphosis of Acropora willisae Veron & Wallace, 1984 and A. millepora (Ehrenberg, 1834) larvae in laboratory assays. This experiment was repeated daily over 4 d, and the spat developed normally into juvenile polyps in flow-through aquaria. Approximately the same number of larvae underwent partial metamorphosis, forming flattened discs that were not attached to the substrata. Larvae underwent full settlement, attachment and metamorphosis only in the presence of Pseudo- alteromonas A3 plus inert chips of the coral skeleton Porites sp., indicating that the calcareous matrix may play a role in the synthesis of inducers from Pseudoalteromonas Strain A3. This discovery pro- vides evidence for a widening range of morphogenic sources and demonstrates the role that micro- organisms may play in fine-scale coral recruitment. In addition, the synthesis of chemical inducers by Pseudoalteromonas Strain A3 may have biotechnological applications for reef re-seeding. KEY WORDS: Coral · Metamorphosis · Settlement · Bacteria Resale or republication not permitted without written consent of the publisher INTRODUCTION seek appropriate substrata upon which to settle, attach and undergo metamorphosis. The larvae of broadcast- Reproduction and recruitment spawning scleractinian corals typically become com- petent to metamorphose into juvenile polyps within a Corals exhibit a range of reproductive strategies, week of the spawning and fertilisation event (e.g. Bab- which include both sexual and asexual propagation. cock & Heyward 1986). At this stage, larvae have Many species of brooding coral exhibit internal fertili- developed cilia for motility and are able to use sensory sation and expel well-developed larvae at various and secretory cells to actively ‘taste’ and subsequently times of the year. However, most species of coral adhere to appropriate surfaces (Heyward 1987). Lar- reproduce during annual spawning events whereby vae at this stage of development have been reported to gametes are ejected into the water column synchro- probe or crawl over available surfaces and are thought nously and fertilisation occurs outside the polyp (Harri- to actively select suitable substrata upon which to son & Wallace 1990). Both strategies result in the attach and metamorphose (Fadlallah 1983, Harrison & development of free-swimming planula larvae that Wallace 1990). The terms settlement and metamorphosis continue *E-mail: [email protected] to be used interchangeably in the literature. In this © Inter-Research 2001 · www.int-res.com 122 Mar Ecol Prog Ser 223: 121–131, 2001 paper we use the term ‘settle’ to describe the point Microbial sources of morphogens where pelagic larvae have become pear-shaped and casually attached to the substrata at the aboral end. The role of microorganisms in the induction of settle- This is a behavioural description. Metamorphosis ment and metamorphosis in marine invertebrates across occurs when larvae undergo physiological and mor- a wide array of phyla is becoming increasingly apparent phological changes that are largely irreversible. Early (see Johnson & Sutton 1994, Leitz 1997, Bryan & Qian metamorphosis in acroporid species often occurs 1998, Unabia & Hadfield 1999). Most studies have ex- within 12 h of settlement, when larvae have developed amined the role of microbial biofilms in preference to into firmly attached disc-shaped structures with pro- specific activity of particular bacterial isolates. Micro- nounced flattening of the oral-aboral axis and typically algal and bacterial biofilms of indeterminate species obvious septal mesenteries radiating from the central composition induced metamorphosis in up to 16% of mouth region (Harrison & Wallace 1990, Heyward & individual agariciid larvae (Morse et al. 1988). In the Negri 1999). Subsequent calcification proceeds rapidly same experiments, CCA induced almost 90% metamor- and the development of tentacles usually occurs within phosis. Larvae of 2 additional brooding corals have been a week. As corals are sessile animals, the choice of an shown to settle and metamorphose in response to appropriate substrata and habitat for settlement of biofilms. The soft coral Heteroxenia fuscenscens under- planula larvae is crucial to survival. In field studies, went 60 and 40% metamorphosis in the presence of 2 larvae have been reported to prefer undersurfaces strains of unknown bacteria isolated from a coral skele- and, in general, favour locations of low light intensity ton (Henning et al. 1991), while the miniature sclerac- and irregular or rough substrata (see Harrison & Wal- tinian coral Stylaraea punctata responded to natural lace 1990, Mundy & Babcock 1998). microbial biofilms in preference to other substrata (Golbuu et al. 1995). This raises the possibility that microbial biofilms, in addition to CCA, may function to Chemical signals for metamorphosis influence metamorphosis in some coral species. Micro- organisms associated with CCA are thought to play a In addition to physical influences, increasing evidence role in triggering metamorphosis of other marine inver- indicates that many corals, such as the brooding agarici- tebrates. For instance, bacterial films associated with ids and the broadcast-spawning acroporid and favid CCA induce metamorphosis in the crown-of-thorns species, require an external chemical signal to trigger starfish (Johnson & Sutton 1994). In fact, the larvae of settlement and metamorphosis (Morse et al. 1988, 1994, many cnidarian species, including hydrozoans and 1996, Heyward & Negri 1999). The best-known source of scyphozoans, undergo settlement and metamorphosis in chemical morphogens for coral larvae are various response to bacteria isolated from natural substrata in- species of non-geniculate calcareous red algae (CCA). cluding CCA (see comprehensive review by Leitz 1997). Larvae of agariciid (Morse et al. 1988) and acroporid Electron microscopy techniques have been used to corals (Morse et al. 1996, Heyward & Negri 1999) do not visualise high densities of bacteria on the surface of require continuous contact with the water-insoluble various CCA species (Galbary & Veltkamp 1980, Gar- cue(s) throughout metamorphosis, but are able to land et al. 1985, Lewis et al. 1985, Johnson et al. proceed to other substrata for permanent attachment. 1991a,b). It is possible that bacteria associated with In addition, such coral species may have evolved CCA may be involved in the synthesis of inducers for chemosensory receptors in order to recognise the clean, metamorphosis of scleractinian corals. In this study, we high-current habitats often colonised by CCA and most isolated various species of heterotrophic bacteria from suitable for successful survival of the adult colonies. The the surface of CCA and examined their potential to identity of these CCA-associated chemical cues has been induce the settlement and metamorphosis of larvae reported as cell-wall-bound, high molecular mass poly- from 2 broadcast-spawning scleractinian corals from saccharides that can only be released following decalci- the Great Barrier Reef. fication (Morse et al. 1994, 1996). Chemical inducers for the metamorphosis of Acropora millepora larvae were later found to be readily extractable without decalcifi- MATERIALS AND METHODS cation from various species of CCA using methanol (Heyward & Negri 1999). Inducers for metamorphosis Experiments were conducted with widespread plate- were also discovered in the skeleton of the massive coral forming acroporid species from 2 mass spawnings, Goneastrea sp. and coral rubble (Heyward and Negri the first at Lizard Island on the Great Barrier Reef 1999). These observations indicate that either multiple (14° 40’ S, 145° 26’ E) on November 18, 1997, and the inducers for metamorphosis exist or specific inducers second at Nelly Bay, Magnetic Island (19° 10’ S, may originate from a variety of sources. 146° 51’ E), on November 27, 1999. Negri et al.: Bacterium-induced coral metamorphosis 123 Spawning, gamete collection and larval cultivation. Expt 2: Similar substrata were prepared in 1999 Expt 1 was conducted at the Lizard Island Research using the CCA Lithophyllum sp. collected from Mag- Station. Eight live colonies of the reef-building coral netic Island. The negative controls used in this experi- Acropora millepora (Ehrenberg, 1834), each measur- ment were also chips produced from fragments of ter- ing approximately
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