Coral Reefs (2010) 29:761–770 DOI 10.1007/s00338-010-0622-5
REPORT
A novel reef coral symbiosis O. Pantos • J. C. Bythell
Received: 1 February 2010 / Accepted: 5 April 2010 / Published online: 20 April 2010 Ó Springer-Verlag 2010
Abstract Reef building corals form close associations with unicellular microalgae, fungi, bacteria and archaea, some of which are symbiotic and which together form the coral holobiont. Associations with multicellular eukaryotes such as polychaete worms, bivalves and sponges are not generally considered to be symbiotic as the host responds to their presence by forming physical barriers with an active growth edge in the exoskeleton isolating the invader and, at a subcellular level, activating innate immune responses such as melanin deposition. This study describes a novel symbiosis between a newly described hydrozoan (Zanclea margaritae sp. nov.) and the reef building coral Acropora muricata (=A. formosa), with the hydrozoan hydrorhiza ramifying throughout the coral tissues with no evidence of isolation or activation of the immune systems of the host. The hydrorhiza lacks a perisarc, which is typical of symbiotic species of this and related genera, including species that associate with other cnidarians such as octocorals. The symbiosis was observed at all sites investigated from two distant locations on the Great Barrier Reef, Australia, and appears to be host species specific, being found only in A. muricata and in none of 30 other
Communicated by Biology Editor Dr. Andrew Baird
Electronic supplementary material The online version of this article (doi:10.1007/s00338-010-0622-5) contains supplementary material, which is available to authorized users. O. Pantos (&) Global Change Institute, University of Queensland, St. Lucia, QLD 4072, Australia e-mail:
[email protected];
[email protected] J. C. Bythell School of Biology, Newcastle University, Newcastle upon Tyne NE1 7RU, UK
species investigated at these sites. Not all colonies of A. muricata host the hydrozoans and both the prevalence within the coral population (mean = 66%) and density of emergent hydrozoan hydranths on the surface of the coral (mean = 4.3 cm-2, but up to 52 cm-2) vary between sites. The form of the symbiosis in terms of the mutualism– parasitism continuum is not known, although the hydrozoan possesses large stenotele nematocysts, which may be important for defence from predators and protozoan pathogens. This finding expands the known A. muricata holobiont and the association must be taken into account in future when determining the corals’ abilities to defend against predators and withstand stress. Keywords Coral reef Holobiont Hydrozoan endosymbiont Scleractinia
Introduction Scleractinian corals form close associations with a broad spectrum of both unicellular and multicellular organisms. Their relationship with microbial associates such as the unicellular endosymbiotic microalga Symbiodinium sp. benefits both parties, with the algae responsible for acquiring a significant proportion of the metabolic and nitrogen requirements of the symbiosis (Muscatine et al. 1981; Edmunds and Davies 1986; Bythell 1988, 1990). More recently, bacteria and archaea have also been shown to form specific associations with corals and may benefit the host through a variety of different mechanisms including nitrogen fixation (Rohwer et al. 2002; Lesser et al. 2004); and antibiotic production (Ritchie 2006). This multi-organismal association is referred to as the coral holobiont (Rohwer et al. 2002). These associations with
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microbial partners have been found to be integral to the health and disease susceptibility of corals, and their vulnerability to environmental stress events (Ritchie 2006). Corals also live in association with other eukaryotes, for example, bivalves, boring sponges and polychaete worms, but unlike the very close association with microbes these multicellular partners are isolated from the coral tissues through the formation of an actively growing edge formed by the host’s calcium carbonate exoskeleton, and therefore the relationship is not considered a symbiosis as there is a physical separation of tissues. Similar responses are also sometimes seen when non-clonal coral colonies grow together but do not trigger aggressive defences like sweeper tentacles and mesenterial filament extrusion (Lang and Chornesky 1990). Although few hydroid species are found living in association with other members of the Cnidaria, the symbiotic relationship between hydroids and members of the soft corals (Octocorallia) is well documented (Puce et al. 2008a). However, to date only anecdotal evidence exists to suggest that hydroids also form close associations with members of the reef building Scleractinia (Hexacorallia) (Millard and Bouillon 1973; Boero et al. 2000), with no clear description or identification of the host coral species and limited description of the characteristics of the association. Although most hydroids are considered to be substrate generalists, some species have very strict substrate preferences, including those few species that are only found on members of the Anthozoa. The degree of symbiotic association with anthozoans can range from simple epibiosis, for example Hydrichthella epigorgia, where the hydroid grows over the surface of the soft coral Siphonogorgia sp., separated from direct contact by a chitinous perisarc; to epibiotic associations such as Zanclea timida that lives on the surface of the octocoral, Paratelesto sp. in direct contact with no protective perisarc (Puce et al. 2008a). More closely integrated endobiotic associations also exist between hydroids and Bryozoa such as Z. divergens that lives below the skeleton of the brown encrusting bryozoan Celleporaria sibogae and lacks a perisarc, which has become superfluous as the host provides physical protection (Boero et al. 2000). As well as varying degrees of physical association, the level of mutual benefit or harm resulting from the symbiosis also varies. Some associations tend more towards a parasitic relationship such as that of Halocoryne epizoica which has been found to feed on the lophophoral tentacles of its bryozoan host at a sublethal level (Piraino et al. 1992). In other associations, the hydrozoan symbionts significantly enhance the defensive and competitive abilities of their bryozoan hosts by discouraging attacks from turbellarian and nudibranch predators (Osman and Haugsness 1981). However, the overall net benefit versus harm (mutualism to
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parasitism) of these symbioses, throughout the life of the host and symbiont, has yet to be determined. This paper describes a previously unreported close association between the reef building coral Acropora muricata (formerly A. formosa) (see Wallace 1999; Veron 2000, for discussion) and a newly described hydroid species, Zanclea margaritae sp. nov., on the Great Barrier Reef, Australia.
Methods In June 2009, branch tips (3–4 cm) were collected from A. muricata colonies from forereef (9–12 m) and reef flat (0.5–3 m) sites at Heron Island, Great Barrier Reef, Australia (23.48S; 151.98E). The population density of hydrozoan gastrozooids was surveyed in the distal 2 cm of the coral branch tips on one side of the branch using an Olympus SZX7 binocular microscope and an Olympus LG-PS2 fibre-optic light source. Due to the highly retractile nature of the dactylozooids, they were not included in the counts. In December 2009, sampling was repeated at the same sites and at three other forereef sites on Heron Island and adjacent Wistari reef. In November 2009, a similar survey was conducted at Pioneer Bay, Orpheus Island, GBR (18.68S; 146.58E), approximately 775 km to the northwest. Still and video images were captured from representative samples using a QImaging Micropublisher 3.3 camera and Q-Capture v6 imaging software. Material for histological analysis was initially fixed in 2% glutaraldehyde in artificial seawater and further fixation and embedding was carried out using a microwave-assisted method in 2% glutaraldehyde in 0.1 M cacodylate buffer and post-fixed in 1% osmium tetroxide in cacodylate buffer. Tissues were dehydrated through an ascending ethanol series and embedded in LR White histological resin, sectioned (200 nm) using a Leica Ultracut UCT (type 706201) microtome, stained with toluidine blue and observed using an Olympus BX41 compound microscope. Images were captured using an Olympus DP70 camera and Olympus DP Controller software. Hydranths could clearly be seen in situ with the aid of a hand-held magnifying glass. The presence of the hydroids associated with other scleractinian species was determined across all six sites by carefully surveying 175 colonies from 30 species using a hand-held magnifying glass underwater. Samples also included those from an additional site within Wistari lagoon, where no A. muricata colonies were found. Type specimens have been deposited with the Australian Museum, Sydney (AMS) [accession numbers G.17701-2, G.17704-6].
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A. muricata collected from the forereef site at Wistari reef, December 2009.
Systematics and description of the hydrozoan Diagnosis Order CAPITATA Ku¨hn, 1913 Family ZANCLEIDAE Russell, 1953 Genus Zanclea Gegenbaur, 1857 Zanclea margaritae sp. nov. (Figs. 1, 2, 3) Type material Holotype: [G.17701] gastrozooids growing in association with A. muricata collected from 9 m depth at Coral Gardens forereef site, Heron Island, Australia, May 2009, by OP. Paratypes: [G.17702] medusa collected on release from parent colony associated with A. muricata on Heron Island reef flat, December 2009; [G.17704] gastrogonozooids growing in association with A. muricata collected from Heron Island reef flat, December 2009; [G.17705] gastrozooids collected from Orpheus Island, November 2009; [G.17706] dactylozooids growing in association with
Fig. 1 Micrographs of the hydrozoan symbiont, showing examples of the different hydranth forms in the polymorphic colony. a Gastrozooid emerging from the rim of an axial corallite. Arrow indicates the host coral tentacle; b gastrozooid with a recently ingested food item within the coelenteron, indicated by arrow; c gastrogonozooid
Polymorphic Zanclea species with emergent hydranths (gastrozooids and dactylozooids) living in the staghorn coral Acropora muricata. Perisarc absent, with stolonal hydrorhiza ramifying through the coral tissue and skeleton. When reproductive, gastrozooids develop 1 or 2 medusal buds at the base of the polyp and the tentacles are reduced and may eventually be lost altogether, forming a gonozooid, prior to release. Newly released medusa small, ca. 0.5 mm diameter. Nematocyst complement consists of two sizes of stenotele and microbasic mastigophores (both in the hydranths and medusa); basitrichous isorhizas in the hydranths; and macrobasic apotrichous euryteles in the cnidophores of the tentacles of the medusa. Description Polymorphic, colonial hydroid consisting of retractile gastrozooids and dactylozooids (Fig. 1). Gastrozooid
emerging from the rim of an axial corallite. The medusal bud which has formed at the base of the gastrozooid is indicated by the arrow; and d a gastrozooid and extended dactylozooid emerging from the same corallite. Arrow indicates nematocyst containing head of the dactylozooid. Scale bars represent 500 lm
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Fig. 2 Hydroid gonozooids at different developmental stages. a Gonogastrozooid with a recently formed medusal bud. b An immature medusa attached to the parent colony via a stalk (s) which has recently liberated a second mature medusa; c an immature medusa with a dense accumulation of brown material in the manubrium. By this stage, the bell opening has developed and bell movement can be observed; d an immature medusa with a pink accumulation within the manubrium. The tentacular bulbs (tb) can be seen as two white areas
at the rim of the developing bell; e a mature medusa immediately before release from the parent colony. The conical manubrium (m) and its white oral opening (oo) extends through the bell opening, becoming exposed as the bell pulsates and retracts back; f the vestigal stalk (arrow) that remains following release of the medusae resulting from the original gonozooid. Adjacent to the stalk is another gonogastrozooid. Scale bars represent 500 lm
Fig. 3 Fully developed medusa a medusa still attached to the hydroid colony via a stalk immediately before release showing the bell opening and the two tentacular bulbs (tb) and attached tentacles, inverted back within the bell cavity. The marginal bulbs (mb) can also be seen at the bell edge, as well as the elongate exumbrellar nematocyst pouches (np); b a medusa which has been detached from
the parent colony and placed under a glass coverslip showing the tentacular bulbs and coiled tentacles (t) with cnidophores, one still within the bell cavity, and the other extruded. The point of colony attachment (ca) can be seen adjacent to the manubrium (m) which has become distorted during sample preparation. Scale bars represent 250 lm
hydranths 0.5–1.04 mm long and 0.1–0.17 mm wide (Fig. 1a) responsive to touch but non-retractile, with 5–6 tentacles on the hypostome surrounding the mouth, which appears white in colour, and 5–17 aboral tentacles arranged in rows (up to 6) covering the rest of the body. Tentacles solid, without a coelenteric cavity, and with a terminal enlargement or capitulum. Oral tentacles facilitate the capture and ingestion of food particles (Supplementary Video S1) through the mouth and into the coelenteron
(Fig. 1b). Highly retractile dactylozooids (Fig. 1d), ca. 1.2 mm when fully extended, are hollow with an apical knob (ca. 135 lm in diameter) containing nematocysts (Fig. 4) and glandular cells. When disturbed, the dactylozooids can retract completely into the host tissues leaving only the surface of the apical knob visible within a raised collar of host coral tissue. A reticular hydrorhiza, devoid of a perisarc interconnects the emergent hydranths below the host tissues (Fig. 5). A hydrocaulus, connecting the
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Fig. 4 Nematocysts of the medusal and polyp morphs of Zanclea margaritae sp. nov. growing symbiotically with Acropora muricata on Heron Island reef. a Undischarged stenoteles of two sizes found in the capitate tentacles of a gastrozooids; b bean-shaped macrobasic apotrichous euryteles present medusal tentacles; c discharged
stenoteles of the medusal exumbrella; d discharged and undischarged microbasic mastigophores from the exumbrella with yellow–brown microalgal cells; e discharged basitrichous isorhizas and stenoteles from a gastrogonozooid; and f an undischarged coral host mastigophore. Scale bars represent 10 lm
hydranths (emergent polyps) to the net-like hydrorhiza, extends through pores in the coral tissue surface (Fig. 5a, c). In surveys conducted in May (Autumn), no medusae or medusal buds were observed, but these were commonly seen during December surveys at Heron Island. Medusal buds form at the base of the gastrozooid, forming a gastrogonozooid (Fig. 2a). The buds remain attached to the colony, either as a gastrogonozooid or on a stalk after the modification of a gastrozooid through the reduction and loss of tentacles (Fig. 2b–d). One to two medusal buds evolve from a single gastrozooid. The manubrium of the developing medusae appears pink or may appear brown due to an accumulation of brown material, possibly food particles, which extend down through the coelenteron of either the stalk or gastrogonozooid (Fig. 2c). As the tentacular bulbs develop, they form dense white tissue masses
near the edge of the bell (Fig. 2d). As the medusa nears maturity, the manubrium becomes more conical in shape with a white oral region and can extend to the full length of the umbrella. The bell begins to pulsate whilst still attached to the parent colony (Fig. 2e; Supplementary Video S2) and cnidophore-covered tentacles remain inverted inside the bell (Fig. 3a) until after release. Once mature, the connection to the parent colony at the apex of the umbrella is broken and the medusa is released, leaving a vestigial stalk on the host (Fig. 2b, f). Newly released medusae (0.4–0.6 mm dia.) are near-spherical with four perradial exumbrellar nematocyst pouches extending the length of the bell, and four marginal bulbs at the base of the nematocyst pouches. Two large white tentacular bulbs with tentacles covered in cnidophores, on opposite sides of the bell, extend after release (Fig. 3). Medusae were not kept to maturity and were only observed for 3–4 h post-release.
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Fig. 5 Histological examination of the interaction between coral host and hydrozoan symbiont. a Longitudinal section through a gastrozooid emerging from the coral tissues through a collar of host coral tissues. On entry to the coral, the hydroid hydranth tissues are adjacent to coral oral epidermal tissues, and then become in contact with the calicoblastic ectoderm. b Close-up of the interface between the hydroid and coral tissues as the hydranth emerges from the coral colony surface. Tissues are directly adjacent to one another with no obvious sign of a physical barrier or perisarc. The mesoglea separating the diploblastic tissues is visible in both organisms. c Longitudinal section through the corallite showing hydrorhiza
(transverse section) passing through the centre of the corallite. d Close-up transverse section of the hydrorhiza deep within the coral tissues (shown in c). The hydroid hydrorhiza lies adjacent to and between the coral skeleton and the calicoblastic ectoderm of the coral. ct capitate tentacle; h hydrorhiza; hg hydrozoan gastrovascular cavity; cg coral gastrovascular cavity; hd hydrozoan gastrodermis; ce coral endodermis; cp coral epidermis; hp hydroid epidermis; cm coral mesoglea; hm hydroid mesoglea; coral calicoblastic tissue; z zooxanthellae; cn coral nematocysts; cs coral skeleton; m coral mesentarial filament. Scale bars represent: a and c = 200 lm; b and d = 20 lm
Microalgal cells were found in the gastrovascular cavity of the medusae (Fig. 4d) and the gastrogonozooids. Both medusae with pink manubria and those that appeared brown due to an accumulation of material contained yellow–brown microalgae; however, the pink medusae contained the most microalgal cells. The source of these microalgae (Fig. 4d) is not yet known; they appear morphologically similar to the coral host’s symbiotic algae but they do not apparently enter the tissues of the hydroid and may be digested within the coelenteron. Cnidome: Polyp and medusa possess distinct nematocyst complements (Fig. 4). Polyp possesses two sizes of stenoteles (undischarged ca. 7 9 7 lm and 10 9 10 lm) and microbasic mastigophores (undischarged ca. 5 9 20 lm) in the capitulum of the tentacles (Fig. 4a). Basitrichous isorhizas (discharged ca. 4 9 18 lm) were also found in the hydranth of a gastrogonozooid from which the medusa had been removed (Fig. 4d). Newly released medusae possess stenoteles of two sizes and microbasic mastigophores in the exumbrella, similar to
those seen in the hydranths. Bean-shaped macrobasic apotrichous euryteles (undischarged ca. 5 9 8 lm) are present in the cnidophores of the tentacles (Fig. 4b).
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Etymology The species epithet margaritae is derived from Margaret, after OPs mother Margaret Pantos, in recognition of the support of her parents over the years. Remarks Several morphological characteristics clearly place this hydrozoan in the genus Zanclea Gegenbaur 1856, including capitate tentacles in a whorl around the mouth and aboral capitate tentacles in whorls below the mouth down the length of the gastrozooid, mastigophores in the nematocyst complement and medusa with flask-shaped manubria, exumbrellar chambers and tentacles with cnidophores, (Petersen 1990; Boero et al. 2000). The first hydroid
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reported living in coral tissues (host species not specified), also a Zanclea sp. (Millard and Bouillon 1973; Millard 1975), was monomorphic and did not contain euryteles, and therefore cannot be referred to as the species described here. The closest described species based on morphology is Zanclea gilii (Boero et al. 2000), reported living within the tissues of an unidentified, non-acroporid coral in Papua New Guinea. Z. margaritae sp. nov. has a similar perisarcfree, polymorphic colony to Z. gilii but appears to be specific to the host Acropora muricata. Additionally, its nematocyst complement includes microbasic mastigophores and basitrichous isorhizas, which are absent from Z. gilii. There are also some morphological differences in the newly liberated medusae, including the bell diameter which is approximately half that of Z. gilii and the medusae possess mastigophores, also unlike Z. gilii. Boero et al. (2000) did not report a reduction of the gastrozooid and loss of tentacles to form a gonozooid as shown here.
magnifying glass (Table 2), including 20 other acroporid species, found no evidence of hydroid symbionts being associated with any coral species other than A. muricata. Not all colonies of A. muricata possessed the hydroid symbionts. The prevalence rate varied between sites, ranging from 20 to 29% of colonies on the reef flat to 100% of those examined on the forereef at Coral Gardens, Heron Island. The hydranths (emergent polyps) of the hydroid colony were predominantly located on the rim and outer wall of the coral polyps (Fig. 1), including the apical polyp, but were also found in the valleys between polyps. Individual coral polyps often hosted multiple hydranths, with up to 9 being observed on a single polyp. The density of hydranths varied between sites and between branch tips within a coral colony, with as many as 52 cm-2 being recorded on the distal 2 cm of the branch tip, but with a mean of 4.3 ± 3.8 cm-2 (±SD)(Table 1).
Interaction with the host
Discussion
A raised collar of tissue surrounds the base of the hydranth (Fig. 5a) derived from the host coral tissue. Histological sections showed no evidence of an inflammatory response or any deposition products in the tissues (Fig. 5); and no abnormal growth or thickening of the underlying skeleton could be seen at the macro-scale (Fig. 6). The whole hydrozoan stolonal system including the hydrocaulus and hydrorhiza lacks a perisarc. At the point at which the hydrocaulus passes into the host colony and joins the hydrorhizal system, the hydrozoan tissues are in very close physical contact with those of the host (Fig. 5a, b) and appear to be virtually confluent, with no inflammation or unusual deposits surrounding them. The coral tissues appear to grow around the hydrozoan so that ectoderm is kept in contact with the hydrozoan as it penetrates the tissues down to the skeleton (Fig. 5a, b). Thus, the hydrozoan does not penetrate the mesoglea and does not come into contact with the digestive tissues of the endodermis. The hydrorhiza ramifies through the host colony, extending deep within the skeleton (Fig. 5c), and lies between the coral host skeletal elements and calicoblastic ectoderm (Fig. 5d).
Hydroids are able to establish symbiotic relationships (de Bary 1879) with representatives of most marine phyla and although usually substrate generalists, many species have strict substrate preferences. For example, the hydroid Halocoryne epizoica is strictly associated with a single species of bryozoan (Piraino et al. 1992; Boero et al. 2000). Although relatively few hydroid species live in association with other cnidarians, members of the Anthomedusae suborder Capitata exist symbiotically with cnidarians and other invertebrates, with varying degrees of physical association, and are often host species specific (see Gili and Hughes 1995 for a review). The hydroid described here associated with A. muricata, like Sarsia medelae which lives with a gorgonian host, is a ‘partial endosymbiont’ (Gili et al. 2006) with the hydranths external to the host tissues, and the stolonal system completely embedded within the scleractinian tissues. Most hydroid species associated with anthozoans have a perisarc-covered hydrorhiza isolating the hydrozoan coensarc from the host tissues. The loss of this structure, which increases exposure to the host’s immune defences, is typically associated with symbiotic lifestyles (Puce et al. 2008b). For example, Zanclea species symbiotic with bryozoans are protected by the host’s calcareous skeleton and therefore the perisarc is believed to have been lost as it becomes superfluous in symbiosis (Osman and Haugsness 1981; Ristedt and Schuhmacher 1985; Puce et al. 2002, 2007). The evolutionary influence of the symbiotic condition on the reduction of the perisarc is also highlighted in the genus Eutima, which includes both free-living and symbiotic species. The perisarc of the free-living species is present but has been lost in the symbiotic species (Bouillon et al. 2006). The
Distribution and population densities of hydroid symbionts The association between A. muricata and the hydroid was ubiquitous, being present at all 6 sites from two distant locations investigated on the GBR (Table 1). It appears to be a host species-specific association. A survey of 175 colonies from 30 other coral species using a hand-held
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Fig. 6 Skeletal structure at the site of hydranths. Images of axial corallites with hydranths before (a) and after (b) removal of tissues. Arrows indicate emergence point of hydranths. Close-up micrographs
(c and d) showing no evidence of enhanced calcification or deformation of the skeletal elements at the sites of hydranth emergence. Scale bars represent 500 lm
Table 1 Prevalence rates (per coral colony) and densities of emergent gastrozooids (cm-2) of Zanclea margaritae sp. nov. on 2-cm branch tips of Acropora muricata at various sites and survey dates Site
Sample size (coral colonies)
Hydroid prevalence rate (%)
Mean hydranth density ± SD (range)
Coral gardens forereef
8
100
15 ± 12.8 (0–44)
Coral gardens reef flat
7
29
2 ± 4.3 (0–12)
Heron Island (June 2009)
Heron Island (Dec 2009) Cascades forereef*
6
33
2nd point forereef
5
40
3 ± 5.8 (0–26) 0.2 ± 0.6 (0–3)
Coral gardens forereef
5
100
20 ± 15.5 (2–67)
Coral gardens reef flat
5
20
10 ± 23.9 (0–100)
Wistari forereef
10
90
15 ± 15.7 (0–53)
Orpheus Island (Nov 2009) Reef flat Total
10
80
2 ± 5.6 (0–33)
56
66
8 ± 7.5
*At this site, all (2/6) colonies that had associated hydroid symbionts were diseased (WS)
At this site, one diseased (WS) colony was inspected but it was not associated with hydroids
N = 5 branch tips were surveyed per coral colony. There were no significant differences between sites resurveyed in June and December (2-way ANOVA, F = 2.23, P = 0.15), but highly significant differences between sites in density of emergent gastrozooids (ANOVA, F = 4.9, P = 0.001). Prevalence rates also varied significantly between sites (Chi-square v2 = 23.5, P \ 0.001)
absence of a perisarc and close physical association between the host and symbiont tissues in the case presented here therefore indicate a well-integrated symbiotic association. The absence of an innate immune response at the
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subcellular level (Mydlarz et al. 2008; Palmer et al. 2008), any evidence of a physical barrier of skeletal material isolating the foreign tissue which runs next to the skeleton, or tissue damage even in the absence of a hydroid perisarc,
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Table 2 Coral species and colony number examined for the presence of Zanclea margaritae sp. nov. at sites on Orpheus Island reef, November 2009, and Heron Island and Wistari reef, December 2009 Coral species
Number of colonies
Acropora species A. loripes
5
A. divaricata A. millepora
5 5
A. nobilis
5
A. gemmifera
7
A. cytherea
8
A. abrolhosensis
2
A. horrida
5
A. grandis
1
A. aspera
2
A. humilis
1
A. hyacinthus
4
A. polystoma
3
A. digitifera
11
A. cuneata
5
A. bushyensis
16
A. samoensis A. sarmentosa
14 12
A. anthocercis
17
A. tenuis
3
Other species Seriatopora hystrix
11
Stylophora pistillata
4
Pocillopora damicornis
10
Porites cylindrica
1
Montipora informis
2
M. peltiformis
12
Goniastrea favulus
1
Leptoria phrygia
1
Porites rus
1
Favia favus
1
suggests that a stable and intimate association has coevolved (Puce et al. 2007, 2008b). The extent to which the symbiosis described here is mutually beneficial, commensal or parasitic, and whether it results in novel metabolic capabilities (Douglas 1994) is unknown. However, in similar hydroid–host symbioses, both partners may gain some benefit of protection either through the physical environment of the host skeleton or due to stinging cells (nematocysts) such as is the case for Zanclea gemmosa associated with the bryozoan Schizoporella errata (Osman and Haugsness 1981). In symbiotic hydroid systems, the host may gain protection from predators such as turbellarians and molluscs (Osman and Haugsness 1981; Ristedt
and Schuhmacher 1985) or protection from parasite infestations (Piraino et al. 1994) due to the nematocysts of the hydroid. Although in this case both partners possess nematocysts, the physical structure, toxin complement and size of the nematocysts varies greatly between the Anthozoa and Hydrozoa (Fautin 2009), therefore potentially expanding the spectrum of protective capabilities of the symbiosis by providing additional types of nematocysts that may be effective against a wider range of predators. The difference in scale of feeding structures may also aid the cleansing of the coral surface, removing detritus and potential protozoan pathogens (Coma et al. 1999; Cerrano et al. 2000). Symbiotic hydroids have also been found to provide their host with protection by actively feeding on grazers, even orders of magnitude larger than themselves (Cerrano et al. 2000). In addition to gaining physical protection from their host, the hydroids may exploit changes in water flow at the coral surface for food particle capture (Boero 1981) and gain protection from the coral surface mucus layer (Brown and Bythell 2005). Close physical contact between hydrozoan and host tissues associated with the lack of a perisarc may allow the movement of metabolites between the symbiotic partners. Thus, there are many ways in which potential benefits may accrue to each partner from the association. Alternatively, it is possible that the relationship is parasitic. Preliminary observations of corals held under stressful conditions in aquaria for 24 h showed that only those samples that possessed reproductive hydranths with medusae bleached. Similarly, at one site, the only two diseased (white syndrome) corals observed were also the only two that possessed hydrozoan symbionts. This pattern was not repeated elsewhere, however, and further studies are required to determine the net benefit or cost of the symbiosis. The identification of hydroids on A. muricata colonies at all sites investigated, and at locations separated by several hundred kilometres, suggests that this apparently hostspecific association is widespread throughout the Great Barrier Reef. Although similar associations were not identified in other coral species in this study, reports of Zanclea species living as partial endosymbionts in unidentified corals in Papua New Guinea and the Indian Ocean (Boero et al. 2000) suggest that similar associations may occur between other scleractinian coral species and capitate hydroids, similar to the several known associations with gorgonians (Gili et al. 2006; Puce et al. 2008a). Given the ecological importance of hydrozoan symbioses in other animal groups (Osman and Haugsness 1981), the role of Z. margaritae sp. nov. in the A. muricata holobiont needs urgent further investigation. It should also be considered in future when investigating physiological and ecological performance of A. muricata in, for example, studies of resilience to environmental stress and disease.
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770 Acknowledgments This work was supported by a grant from the Natural Environment Research Council, UK (NE/E006949/1) and travel support from the GEF-World Bank Bleaching Working (BWG). We would like to thank BWG members for comments on the original manuscript, particularly Ove Hoegh-Guldberg, Bill Fitt and Rob van Woesik. We thank Clay Winterford of the Joint University of Queensland, Queensland Institute of Medical Research Histotechnology Facility and Robyn Webb of the Centre for Microscopy and Microanalysis at the University of Queensland for their help with preparing and sectioning tissue for histological examination.
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