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Settle and Metamorphose in Response to Surface-Biofilm Bacteria

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Settle and Metamorphose in Response to Surface-Biofilm Bacteria Vol. 433: 85–96, 2011 MARINE ECOLOGY PROGRESS SERIES Published July 18 doi: 10.3354/meps09192 Mar Ecol Prog Ser Larvae of Pocillopora damicornis (Anthozoa) settle and metamorphose in response to surface-biofilm bacteria Cawa Tran*, Michael G. Hadfield Kewalo Marine Laboratory, University of Hawaii at Manoa, 41 Ahui Street, Honolulu, Hawaii 96813, USA ABSTRACT: Larvae of the scleractinian coral Pocillopora damicornis require a natural cue from sur- face-biofilm bacteria to select a suitable substratum on which to attach, metamorphose, and grow into a benthic polyp. In this study, bacteria were isolated from various reef surfaces, including different species of corals and algae, and glass slides that had been placed in the field for 1 to 2 mo. Settlement assays were conducted on monospecific biofilms of bacteria isolated from the field. Of 52 different isolates, 3 showed strongly inductive capacity, whereas the others were moderately to non-inductive. The isolates were identified by sequencing their 16S rRNA genes, and their phylogenetic relation- ships were then analyzed. There was no correlation between the inductive capacities of individual bacterial species and their phylogenetic relationships nor between their inductive capacities and the surfaces from which they were isolated. Varying the biofilm densities affected settlement only by a strongly inductive bacterial species. Different bacterial species may also affect the inductive capaci- ties of other species when combined. The new data provided here broaden our understanding of the roles of bacteria in the recruitment of coral larvae. KEY WORDS: Larval settlement · Metamorphosis · Biofilm · Marine bacteria · Coral planula · Pocillopora damicornis Resale or republication not permitted without written consent of the publisher INTRODUCTION A common substratum for the settlement of many marine invertebrate larvae is biofilm (Hadfield 2011). The life cycle of most benthic marine invertebrates Biofilms are defined as ‘matrix-enclosed bacterial involves 2 major stages: a planktonic larval stage that populations adherent to each other and/or to surface allows dispersal and habitat selection, and a sessile or interfaces’ (Costerton et al. 1995). Dissolved organic juvenile–adult stage that results from larval settle- molecules form thin layers on newly submerged sur- ment. Settlement involves a change in habitat during faces, followed by the attachment of bacteria as the which larvae enter the juvenile environment and primary colonizers, and a variety of eukaryotic organ- attach to a substratum. This is followed by metamor- isms as secondary colonizers (Zobel & Allen 1935). The phosis — the rapid change in morphology that includes structure of biofilm continues to be highly heteroge- the loss of larval structures and gain of juvenile struc- neous as extracellular polymeric substances (EPS) are tures (Hadfield et al. 2001). Metamorphosis of marine secreted, offering bacteria and other microorganisms invertebrate larvae is governed by a combination of protection and resistance to environmental stress (Wol- biological, physical, and chemical factors (Crisp 1974). faardt et al. 1999). Biofilms provide a stable structure Larvae gain the ability to settle and metamorphose for bacteria to aggregate and function as a community when they become ‘competent,’ which is defined as (Costerton et al. 1995). Previous studies have shown having the capacity to detect and respond to a specific that biofilms provide settlement cues for a diverse environmental cue (Hadfield & Paul 2001, Hadfield et range of invertebrate taxa (Hadfield 2000). Biofilms al. 2001). also function to facilitate adhesion of larvae in the pro- *Email: [email protected] © Inter-Research 2011 · www.int-res.com 86 Mar Ecol Prog Ser 433: 85–96, 2011 cess of settling and of juveniles as they continue to and Porites spp.) (Arnold et al. 2010, Price 2010). develop on a substratum (Zardus et al. 2008). Another species of CCA, Hydrolithon boergesenii, is a This study examines the settlement of the larvae of preferred substratum for A. palmata and A. cervicornis Pocillopora damicornis (Linnaeus, 1758), which is an (Ritson-Williams et al. 2010). Many studies testing the Indo-Pacific coral that is a significant component of settlement of various coral species have led to the con- the reef community in Hawaii. The life cycle of many clusion that CCA play a major role in settlement, with antho zoans involves a planula stage — a dispersal different coral species preferring a different species of phase in which the larva continues to swim in the water CCA. Negri et al. (2001) found that although a steril- column and across substrata until it becomes metamor- ized CCA (Hydrolithon onkodes) could induce settle- phically competent and encounters a suitable substra- ment in the 2 species of Acropora they studied (A. tum on which to settle and metamorphose into a polyp willisae and A. millepora), a particular bacterial strain (Müller & Leitz 2002). The reproductive strategies of isolated from this CCA also induced settlement in the corals vary between broadcast spawning and brooding, absence of CCA. Thus, the authors concluded that and planktonic periods also vary greatly. Miller & CCA might not be the sole inducer of coral settlement Mundy (2003) found that broadcast spawners may set- in these species. Microbial biofilms alone, in the tle as soon as 2 to 3 d after fertilization. However, some absence of CCA, also induced settlement in larvae of broadcast spawners can remain in the plankton for up A. microphthalma (Webster et al. 2004). Golbuu & to 244 d when a suitable substratum is not encountered Richmond (2007) examined 2 species of corals in Guam (Graham et al. 2008). The larvae of brooding corals also and found that one (Goniastrea retiformis) preferen- exhibit a wide range of planktonic periods, with some tially settled on CCA, while the other (Stylaraea punc- settling within 24 h after release (Carlon & Olson 1993). tata) settled on biofilmed carbonate rubble. Thus, set- P. damicornis is a brooder and its larvae can settle at tlement substrata vary greatly among coral species, any time between 2 h and up to 100 d after release and whether the inductive cue originates from CCA or (Harrigan 1972, Richmond 1987). Settlement refers to bacteria is coral-species specific. the descent of the planula from the water column and The larvae of Pocillopora damicornis in Hawaii have its attachment at the aboral end to a substratum. This is been shown not to be very selective and to settle on subsequently followed by metamorphosis, which is any biofilmed surface (Harrigan 1972). The same is characterized by the flattening of the larva in the true for P. damicornis in Australia (Harriott 1983). It has oral–aboral direction, secretion of a calcareous base, been shown that the biofilm bacterial communities can and development of tentacle buds to form the polyp differ vastly among different CCA species (Johnson et (Vandermeulen 1974). Metamorphosis, in the broader al. 1991) as well as among non-biological surfaces at context of most invertebrate larvae, is usually an irre- different depths and times (Webster et al. 2004). versible process (Hadfield 2000). However, in the spe- Therefore, different bacterial species may affect settle- cial case of P. damicornis, reversible metamorphosis ment of coral larvae differently. P. damicornis is a has been observed under conditions of environmental brooder that produces larvae year-round according to stress or energy constraint (Richmond 1985). the lunar cycle (Richmond & Jokiel 1984, Jokiel 1985). Many cnidarian larvae require a natural cue that The planulae remain planktonic in the absence of a indicates an acceptable substratum, and inductive suitable substratum for settlement. However, they will cues range broadly across species. Microbial cues that settle within 24 h in the presence of a biofilmed induce metamorphosis of cnidarian larvae have been surface. The goal of this study is to determine which well studied in hydrozoans (Müller 1973, Freeman & species of bacteria would induce metamorphosis of P. Ridgway 1990, Seipp et al. 2007) and scyphozoans damicornis. The specific questions to be addressed are: (Fleck & Fitt 1999). Anthozoans, particularly corals, (1) Is there specificity in the inductive capacities of utilize a diverse range of cues. Cues can be associated different bacterial species? with crustose coralline algae (CCA) (Morse et al. 1988, (2) Are inductive capacities associated with bacterial 1996, Baird et al. 2003, Baird & Morse 2004, Harrington phylogeny, in which strongly inductive species are et al. 2004, Golbuu & Richmond 2007, Kitamura et al. taxonomically related? 2007, Ritson-Williams et al. 2010, Arnold et al. 2010, (3) Are inductive bacterial species associated with Price 2010) or marine bacteria and biofilms (Negri et al. the particular reef substratum from which they were 2001, Webster et al. 2004). Four species of Acropora isolated? (A. tenuis, A. millepora, A. palmata, and A. cervicornis) (4) Does bacterial density differentially affect larval have been shown to preferentially settle on a particu- settlement? lar species of CCA, Titanoderma prototypum (Harring- (5) Can different bacterial species inhibit or enhance ton et al. 2004, Ritson-Williams et al. 2010), which is each other’s inductive capacities when combined in a also preferred by other hard corals (Pocillopora spp. mixed-species biofilm? Tran & Hadfield: Bacteria affect settlement of coral larvae 87 MATERIALS AND METHODS
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