J. Mar. Biol. Ass. U.K. (2002), 82, 943^954 Printed in the United Kingdom Zanclea (Cnidaria: Hydrozoa) species from Bunaken Marine Park (Sulawesi Sea, Indonesia) S. Puce*, C. CerranoO, M. BoyerP, C. FerrettiO and G. Bavestrello*$ *Istituto di Scienze del Mare, Universita' di Ancona, Via Brecce Bianche, I-60131 Ancona, Italy. ODip.Te.Ris. Universita' di Genova, Corso Europa 26, I-16100 Genova, Italy. P Biodiversity Project, PO Box 1014, Manado, Indonesia. $Corresponding author, e-mail: bavestrello@popcsi.unian.it Three species belonging to the genus Zanclea: Zanclea divergens, Zanclea tipis, sp. nov. and Zanclea exposita, sp. nov. have been described as epizoic of bryozoan from the coral reef of the Bunaken Marine Park (Sulawesi Sea, Indonesia). The record of Z. divergens is the second after its description from Papua New Guinea. Zanclea tipis is characterized by a polymorphic colony and a medusa with very extended exumbrellar pouches. Zanclea exposita shows a naked hydrorhiza creeping on the surface of the bryozoan skeleton. An evolutionary trend among the Zancleidae, from species epibionts of algae and bivalve shells with the hydrorhiza covered by perisarc to species symbiotic with bryozoan with a naked hydrorhiza, is discussed. INTRODUCTION The North Sulawesi peninsula, stretching between the Sulawesi Sea (north-west) and the Maluku Sea (southeast), lies in an area commonly considered the centre of marine biodiversity (Sheppard & Wells, 1988; Muller, 1996; Tomascik et al., 1997; Edinger et al., 1998) due to geographical reasons (it acts as a link between the Indian and the Paci¢c Ocean), and on account of its complex geological history. A dynamic and complex geotectonic history as well as £uctuating sea levels during the Pleistocene glacial periods caused repeated isolation and remixing of faunas throughout the region leading to important speciation phenomena (Lieske & Myers, 1994; Barber et al., 2000). The extinction rate has been lower than elsewhere, due to the marginal e¡ect on low water temperature from the latest glacial episodes. Nowadays a constant current from the Paci¢c Ocean to the Indian Ocean, named the Indonesian through £ow, provides an important passage of colonization for Paci¢c species (Tomascik et al., 1997). The hydroid population present in this area is almost completely unknown. There is no monograph covering the hydroids of the tropical Indo-West Paci¢c, although a number of expedition reports and accounts of collections from speci¢c regions or island groups have been published as the voyages of the ‘Uranie’ (Lamoroux, 1824), ‘Challenger’ (Allman, 1883, 1888) and ‘Siboga’ (Billard, 1913, 1925). Information about hydroids of the eastern Indian Ocean (Ritchie, 1910), and results of expeditions in the Archipelago Malays, in the Indochina Sea and in the Philippines are also available (Pictet, 1893; Bedot, 1909; Hargitt, 1924; Nutting, 1927; Lelup, 1937). The most recent reports are from Papua New Guinea (Bouillon et al., 1986), from the Philippines, Indonesia (Makassar Strait) and New Caledonia (Vervoort, 1993). In the framework of a research project about hydroid biodiversity of the Bunaken Marine Park (Sulawesi Sea) this paper deals with the genus Zanclea and its association with bryozoans. Journal of the Marine Biological Association of the United Kingdom (2002) The symbiosis between hydroids and bryozoans involves several genera including Zanclea Gegenbaur, 1857, Halocoryne Hadzi, 1917, Zanclella Boero & Hewitt, 1992, Perarella Stechow, 1922, Octotiara Kramp, 1953 and Hydranthea Hincks, 1868 (Boero & Hewitt, 1992; Piraino et al., 1992; Boero et al., 2000). The relationship between hydroids and cheilostomatous bryozoans can show di¡erent levels of interdependency. The bryozoans may receive protection from predators such as turbellarians and molluscs, while the hydroid may exploit the water circulation generated by the feeding activity of the bryozoan zooids and at the same time it may be protected by the bryozoan skeleton from nudibranch predation. In some cases the association may shift towards a form of parasitism: the hydroid Halocoryne epizoica Hadzi, 1917 ‘bites’ the lophophoral tentacles of the bryozoan (Piraino et al., 1992) and Perarella schneideri (Motz-Kossowska, 1905) engulfs the tip of lophophoral tentacles and feeds on bryozoan larvae, a¡ecting the life cycle of its host (Bavestrello et al., 2000). MATERIALS AND METHODS The sample collections were gathered by diving at di¡erent sites (Likuan I, Likuan II, Sachiko’s Point, Siladen, Bualo and Alung Banua) of the reef surrounding the Bunaken Island (Figure 1), during the period January^ February 2001. The sites show similar characteristics: vertical winding walls with many cracks, and canyons and caves characterized by strong currents. Only Alung Banua is a very sheltered zone. Among the collected samples of hydroids living with bryozoans, some colonies were ¢xed in 4% formaldehyde after morphological observation by stereomicroscope, while the others were cultured in small bowls, feeding the polyps with Artemia nauplii. When production of medusae occurred, they were kept in small bowls at natural temperature and fed with Artemia nauplii too. The water was changed daily two hours after the feeding session. Each 944 S. Puce et al. Zanclea Gengenbaur from Indonesia Figure 1. Map of Bunaken Island showing the dive sites Likuan I and II (1), Sachiko’s Point (2), Siladen (3), Bualo (4), Alung Banua (5). day several of the reared medusae were ¢xed in 4% formaldehyde. The behavioural observations were carried out by a stereomicroscope. Drawings were made from living material soon after the collection and the colours mentioned in the descriptions are from living material. The nematocysts are measured from ¢xed material. For scanning electron microscopy (SEM) analysis some portions of colonies were ¢xed in 2.5% glutaraldehyde in arti¢cial seawater as a bu¡er (pH¼7.6) for two hours. After rinsing the specimens in the same bu¡er, they were gradually dehydrated in an ethanol gradient. Samples were not exposed to critical-point, but were dehydrated at 608C for 10 min, then mounted on stubs with silver conducting paint, sputter-coated with gold-palladium in Blazer Union Evaporator, and observed with a Philips EM 515 electron microscope. For histological sections, the ¢xed samples were dehydrated in a graded ethanol series and specimens were embedded in Technovit 8100 (Kulzer). Sections 3 mm in thickness were collected on slides, stained with toluidine blue and mounted in resin (Eukitt). Type material of the new species is deposited in the Museo di Storia Naturale, Genova, Italy (MSNG). SYSTEMATICS Zanclea divergens Boero, Bouillon & Gravili, 2000 (Figure 2; Table 1) Zanclea divergens Boero, Bouillon & Gravili, 2000: 100. Journal of the Marine Biological Association of the United Kingdom (2002) Type material IRSNB (Institut Royal des Sciences Naturelles, Bruxelles, Belgique), I.G. 27838 Material examined Bunaken Island (Likuan I, 720 m, Likuan II, 730 m, Sachiko’s Point, 730 m, Siladen, 725 m), January ^ February, 2001. Description of the hydroid The examined specimens of this hydroid live in association with the brown encrusting bryozoan Celleporaria sibogae Winston & Heimberg, 1986 (Figures 2A & 3A) The reticulate hydrorhiza grows under the bryozoan skeleton from which polyps and clusters of nematocysts emerge (Figures 2A, 4 & 5A^ C). The polyp (0.5^1mm high) is sessile, with a cylindrical body and a whitish hypostome surrounded by four oral capitate tentacles. Short aboral capitate tentacles 25^30 are scattered on the body (Figures 2B & 5A). The medusa buds arise from the hydrorhiza. Cnidome: holotrichous macrobasic euryteles (undischarged capsule 45
25 mm, discharged capsule 37.5
17.5 mm, shaft 250 mm) in the hypostome and in the hydrorhiza (Figure 2C); stenoteles of two sizes (undischarged capsule 17.5
12.5 mm, discharged capsule 13
11 mm and undischarged capsule 7.5
5 mm, discharged capsule 5
3 mm) in tentacle capitations. Description of the medusa The young medusa (Figure 2D) is characterized by an almost spherical bell (about 0.8 mm in diameter) and a Zanclea Gengenbaur from Indonesia S. Puce et al. 945 Figure 2. Zanclea divergens. (A) Polyp, medusa bud and clusters of nematocysts protruding from the bryozoan colony; (B) polyp; (C) undischarged and discharged holotrichous macrobasic eurytele from the polyp and the hydrorhiza; (D) newly released medusa; (E) cnidophore containing three undischarged euryteles; (F) undischarged capsule of holotrichous macrobasic eurytele from the cnidophore; (G) undischarged capsule of basitrichous isorhiza from the exumbrella of the medusa. Scale bars: A,B&D, 0.5 mm; C, 50 mm; E, 20 mm; F,G, 10 mm. Journal of the Marine Biological Association of the United Kingdom (2002) 946 S. Puce et al. Zanclea Gengenbaur from Indonesia Figure 3. Photographs of colonies of (A) Zanclea divergens; (B) Zanclea tipis; and (C) Zanclea exposita in situ. Scale bars: A, 0.8 mm; B, 1 cm; C, 1 mm). cylindrical manubrium reaching half-way along the subumbrellar cavity; four exumbrellar nematocyst pouches extending for half of the exumbrella; two opposite perradial tentacular bulbs and two tentacles bearing about 15 cnidophores with the terminal swelling covered by long cilia, containing three nematocysts each (Figure 2E). Cnidome: holotrichous macrobasic euryteles (12.5
7.5 mm) in cnidophores (Figure 2F), basitrichous isorhizae (7.5
7 mm) on exumbrella (Figure 2G), small stenoteles (5
7 mm) in the margin of the manubrium and large stenoteles (17.5
12.5 mm) in the exumbrellar pouches. Journal of the Marine Biological Association of the United Kingdom (2002) Distribution Papua New Guinea (Bismarck Sea), Indonesia (North Sulawesi Sea). Remarks Our specimens di¡er from the holotype description for the whitish coloration of the polyp hypostome and for the presence of only one kind of stenoteles (the larger) in the medusal pouches. The observation of living polyps has shown a particular feeding interaction between the hydroid and the bryozoan. The bryozoan touches the polyps with the lophophoral Zanclea Gengenbaur from Indonesia S. Puce et al. 947 Table 1. Characters of the described species. HYDROID CHARACTERS Zanclea divergens Boero, Bouillon & Gravili, 2000 Zanclea tipis sp. nov. Zanclea exposita sp. nov. Hydrorhiza and substrate reticular, under bryozoan skeleton, with nematocysts clusters absent 4 reticular, under bryozoan skeleton present 5^6 reticular with large plates, on bryozoan skeleton absent 5^6 25^30 absent whitish with an intense white hypostome on hydrorhiza undischarged capsule 45
25 mm; discharged capsule 37.5
17.5 mm; shaft 250 mm 20^25 present transparent-white with an intense white hypostome inferior half of the hydranth undischarged capsule 17
10 mm; discharged capsule 15.5
7.5 mm Position of macrobasic euryteles hypostome and hydrorhiza scattered in hydranths, dactylozooids, hydrorhiza 25^30 absent transparent-white with an intense white hypostome unknown undischarged capsule 30
20 mm; discharged capsule 25
17 mm; shaft 320 mm a dense ring around the hypostome and abundant in the hydrorhiza MEDUSA CHARACTERS Zanclea divergens Boero, Bouillon & Gravili, 2000 Zanclea tipis sp. nov. Zanclea exposita sp. nov. Gonads at release Shape of umbrella at release Tentacles at release absent spherical 2 absent spherical 2 unknown unknown unknown Cnidophores Cnidophoral nematocysts 15 holotrichous macrobasic euryteles (12.5
7.5 mm) 40 macrobasic euryteles (5
2.5 mm) unknown unknown Exumbrellar nematocysts pouches at release Exumbrellar nematocysts at release 4 4 unknown basitrichous isorhizae (7.5
7 mm) none unknown Perisarc Oral tentacles Aboral tentacles Dactylozooids Colour Position of medusa buds Macrobasic euryteles tentacles until they egest a mucous aggregate of particles. Then the lophophores perform a series of rapid contractions fragmenting the mucus into smaller portions on which they feed. In this way the bryozoan may exploit an easily available trophic source and also have the protection of the nematocysts of the hydroid. On the other hand, the hydroid polyps are mechanically protected by the bryozoan: when the polyps contract, they disappear under the calcareous skeleton, leaving exposed only the oral portion of the hypostome defended by its large nematocysts as described by Ostman & Haugsness (1981). Zanclea tipis, sp. nov. (Figure 6; Table 1) Type material Holotype MSNG 50780, one formalin preserved colony on the bryozoan Triphyllozoon cfr. inornatum. Siladen (Bunaken Island, Indonesia) on the reef, depth 20 m; coll: S. Puce (SCUBA), 28 January 2001. Material examined Bunaken Island (Likuan II, 710 m, Sachiko’s Point, 720 m, Siladen, 720 m, Bualo, 720 m), Indonesia (North Sulawesi Sea), January ^ February, 2001. Journal of the Marine Biological Association of the United Kingdom (2002) Description of the hydroid This hydroid lives in association with the reteporiform bryozoan Triphyllozoon cfr. inornatum Harmer, 1934 (Figures 3B & 6A). The reticular hydrorhiza, covered by perisarc, grows inside the bryozoan skeleton (Figure 4) and the polyps arise from it only on the side of the bryozoan in which the lophophores expand. On the opposite side, the polyps are absent and the portions of hydrorhiza growing on this surface are exposed. This species is polymorphic: the colony is composed of thin gastro-gonozooids and dactylozooids (Figure 6A). The gastro-gonozooids (Figure 6B) are cylindrical with a strikingly white-coloured hypostome surrounded by 5^6 oral capitate tentacles. The aboral portion of the polyp presents about 20^25 short capitate tentacles, most reduced to sessile capitations. A short cup of perisarc is present at the base of the polyps (Figures 5D & 6B). The polyps 0.5^0.8 mm high, are not able to contract very strongly. The medusa buds are born in clusters of 4^7 on the inferior half of the polyps that tend to reabsorb the hypostome, reducing to blastostyles (0.2^0.4 mm high), during the progressive maturation of the medusae (Figure 6A&D). Dactylozooids (0.5^1.2 mm) (Figure 6C) are uncommon and present a chordal structure when they are completely extended. They are deprived of tentacles and 948 S. Puce et al. Zanclea Gengenbaur from Indonesia Figure 4. Histological sections of the bryozoan skeleton and the hydrorhiza of Zanclea divergens with its nematocyst clusters, Z. tipis and Z. exposita. In these pictures are showed the zooeciae of the bryozoan (z), the bryozoan surface (bs), the sections of the hydrorhiza (hy), the nematocysts (n), the nematocyst clusters (nc) and the perisarc of the hydrorhiza (p). Scale bar: 50 mm. present an enlarged apex; numerous glandular cells are scattered on their bodies. Cnidome: rare macrobasic euryteles (Figure 6F) (undischarged capsule 17
10 mm, discharged capsule 15.5
7.5 mm; the shaft was never clearly observed) scattered in Journal of the Marine Biological Association of the United Kingdom (2002) the polyp, in the dactylozooids and in the hydrorhiza; stenoteles of two sizes (undischarged capsule 15
12.5 mm, discharged capsule 11
11 mm and undischarged capsule 7.5
5 mm, discharged capsule 5
5 mm) in the tentacle capitations and in the dactylozooids. Zanclea Gengenbaur from Indonesia S. Puce et al. 949 Figure 5. Scanning electron microscopy photographs. (A) Polyp (p) of Zanclea divergens; (B) cluster of nematocysts (n); (C) cluster of nematocysts with nematocysts exposed (n); (D) polyp (p) of Zanclea tipis sp. nov. showing the perisarc cup (arrow); (E) polyp (p) of Zanclea exposita sp. nov.; (F) hydrorhiza (hy) of Zanclea exposita sp. nov. creeping between two zooeciae (z) of the bryozoan. Scale bars: A, 250 mm; B,C&F, 50 mm; D, 200 mm; E, 100 mm. Description of the medusa The newly released medusa (Figure 6G) presents a spherical bell (about 0.5 mm in diameter) with four white very long exumbrellar nematocyst pouches, which may reach over half the umbrella height. The manubrium is short, about one-third of the subumbrellar cavity, and in the upper portion has little whitish spots. Two tentacular bulbs may be observed from which two long tentacles with Journal of the Marine Biological Association of the United Kingdom (2002) about 40 cnidophores without developed cilia, each one containing three nematocysts (Figure 6I). The medusa buds are ciliate, then, when released, the medusa loses the cilia (Figure 6E). Cnidome: macrobasic euryteles (Figure 6H) (15
7.5 mm) and large stenoteles (15
12.5 mm) in the upper portion of the manubrium and little stenoteles (6.5
5 mm) in the lower one; stenoteles of one size only (undischarged 950 S. Puce et al. Zanclea Gengenbaur from Indonesia Figure 6. Zanclea tipis sp. nov. (A) Gastrozooids, gonozooids and dactylozooids protruding from the bryozoan colony; (B) gastrozooid with perisarc cup; (C) dactylozooid; (D) gonozooid with four medusa buds in di¡erent stage of maturation; (E) ciliated medusa bud; (F) undischarged capsule of macrobasic eurytele from the polyps; (G) newly released medusa; (H) undischarged capsule of macrobasic eurytele from the medusa; (I) cnidophore and undischarged capsule of macrobasic eurytele from the cnidophore. Scale bars: A,E&G, 0.2 mm; B^D, 0.1 mm; F,H&I, 10 mm. Journal of the Marine Biological Association of the United Kingdom (2002) Zanclea Gengenbaur from Indonesia S. Puce et al. 951 Figure 7. Zanclea exposita sp. nov. (A) Polyp and hydrorhiza on the bryozoan colony; (B) Polyp; (C) undischarged and discharged capsule of holotrichous macrobasic eurytele from the polyp and the hydrorhiza. Scale bars: A, 0.5 mm; B, 0.2 mm; C, 30 mm. capsule 10
7.5 mm, discharged capsule 7.5
7.5 mm) in the exumbrellar pouches, euryteles macrobasic (Figure 6I) (5
2.5 mm) in cnidophores. Etymology The word ‘tipis’ is Indonesian meaning ‘thin’. This speci¢c name refers to the shape of the polyps. Remarks This species di¡ers in several characteristics from the other polymorphic ones: Z. polymorpha Schuchert, 1996 presents dactylozooids with capitate tentacles, Z. gilii Boero, Bouillon & Gravili, 2000 shows a larger size of macrobasic euryteles in the polyps, a di¡erent shape and number of cnidophores and a di¡erent number of nematocysts in each of these. The last polymorphic species, Z. hirohitoi Boero, Bouillon & Gravili, 2000, produces medusae with short exumbrellar nematocyst pouches containing two sizes of stenoteles, and only 20 cnidophores on each tentacle. The observation of the living colonies allows us to point to a feeding relationship between the hydroid and its host. Journal of the Marine Biological Association of the United Kingdom (2002) The gastro-gonozooids apparently do not perform direct interactions with the lophophores of the bryozoan, while dactylozooids usually bend over lophophores and softly insert their apex between the lophophoral tentacles. They maintain this position for a long time and the lophophores rarely appear disturbed by this behaviour and only sometimes contract, re-extending immediately after. The meaning of this behaviour is not clear, but, in this way, the enlarged apex of dactylozooids may collect microparticles and stick them onto its surface, exploiting the water current produced by the lophophoral tentacles. It is remarkable that the gastro-gonozooids appear not to be able to capture and feed on the Artemia nauplii experimentally administered to the living colonies. Zanclea exposita sp. nov. (Figure 7; Table 1) Type material Holotype MSNG 50779, one colony on Rhynchozoon sp., formalin preserved. Alung Banua (Bunaken Island, 952 S. Puce et al. Zanclea Gengenbaur from Indonesia Figure 8. Evolutionary trend of hydrorhiza and medusa buds position from species epibionts of algae and bivalve shells to Zanclea exposita. Indonesia) on the reef, depth 20 m; coll: S. Puce (SCUBA), 3 February 2001. Material examined Bunaken Island (Alung Banua, 720 m, 727 m), Indonesia (North Sulawesi Sea), January ^ February, 2001. Description of the medusa Never observed. Etymology This speci¢c name refers to the exposed naked hydrorhiza. Description of the hydroid This hydroid lives in association with the pink encrusting bryozoan Rhynchozoon sp. (Ristedt & Schuhmacher, 1985) (Figures 3C & 7A). The hydrorhiza is reticulate and grows on the bryozoan skeleton, forming a dense net that expands sometimes in large plates (Figures 4 & 5F). It is completely deprived of the perisarc, but armoured by large macrobasic euryteles. The polyps (0.2^0.6 mm) (Figures 5E & 7B) are sessile, cylindrical, and transparent-white with an intense white hypostome. They present 5^6 oral capitate tentacles and about 25^30 scattered aboral tentacles, often reduced to sessile capitations. Cnidome: holotrichous macrobasic euryteles with rounded capsule (Figure 7C) (undischarged capsule 30
20 mm, discharged capsule 25
17 mm, shaft 320 mm) forming a dense ring around the hypostome and abundant in the hydrorhiza; stenoteles of two size (20
17.5 mm and 7.5
10 mm) in the tentacle capitations. Journal of the Marine Biological Association of the United Kingdom (2002) Remarks The closer species to Z. exposita is Z. retractilis Boero, Bouillon & Gravili, 2000, which di¡ers from our species in terms of the smaller size of macrobasic euryteles of the polyps, in the structure of the hydrorhiza and in the ability of the polyps to completely retract inside the bryozoan skeleton. Di¡erently from all known Zanclea species living in association with bryozoans, this species shows a naked hydrorhiza growing not under but on the bryozoan skeleton. Usually the hydrorhiza grows among zooeciae, moreover, sometime it enlarges, forming plates that partially cover the zooeciae of the bryozoan. This species was found only on the reef of the dive site Alung Banua, which is a very sheltered site from water movement. In this area it is very abundant, covering large portions of the rock and death coral surface. The rearing of this species was di⁄cult and consequently it Zanclea Gengenbaur from Indonesia was not possible to carry out behavioural observations and the medusal stage description. DISCUSSION All the species belonging to the family Zancleidae Russell, 1953 are known as living in association with other benthic organisms. The species of the genus Zanclea are associated with algae (1 species), with corals (1 species), with ascidians (1 species), with bivalves (2 species), and with bryozoan (10 species). The host of two other species is unknown. The genera Halocoryne and Zanclella live associated with bryozoans. Unfortunately, in almost all the associations with Zanclea, the species of the bryozoan host is unknown. This lack of knowledge represents a limitation for future studies on the speci¢city of these relationships. Describing all the species of the family, Boero et al., (2000) hypothesize a phylogenetic reconstruction of the evolution of the Zancleids showing a transition from nonsymbiotic species with medusa to symbiotic and highly modi¢ed hydroids with more or less reduced or modi¢ed medusae and a behavioural integration with the host. In our opinion the characteristic which better displays evidence of the trend of integration between the hydroid and its host is the evolution of hydrorhiza protection. The hydrorhiza of almost all the bryozoan inhabiting species of Zanclea grows among the zooeciae of the bryozoan and is then covered by the growing skeleton of the host. The polyps come out from small holes in the bryozoan skeleton (Boero et al., 2000). The herein described Zanclea exposita is the only species with the naked hydrorhiza exposed on the bryozoan skeleton. Other species with an exposed hydrorhiza are known living on the bivalve shells (Z. costata Gegenbaur, 1857 and Z. fanella Boero, Bouillon & Gravili, 2000), on ascidians (Z. costata Gegenbaur, 1857) (Millard & Bouillon, 1973) and on algae (Z. alba (Meyen, 1834)). These species have a hydrorhiza covered by perisarc which forms smooth or annulated pedicels at the base of the hydranths. Only the three species Z. sessilis (Gosse, 1853), Z. giancarloi Boero, Bouillon & Gravili, 2000 and the herein described Z. tipis have a hydrorhiza surrounded by perisarc and creeping inside the bryozoan skeleton. In this way we may hypothesize that the primitive species of Zanclea were epibiontic, living on several substrata as algae or bivalves producing a hydrorhiza covered by perisarc. Later, the association with bryozoans and the protection represented by the bryozoan skeleton induced a progressive elimination of the perisarc until the evolution of species completely deprived itself of this structure (Figure 8). It is likely that from these species the genus Halocoryne and Zanclella, known associated only to bryozoans, are derived. Zanclea exposita with naked hydrorhiza, although not covered by the bryozoan skeleton, suggests that the loss of perisarc is not a phenotypical reaction to the bryozoan covering but a loss of genetic information necessary for its production. Examining this tendency, it is possible to follow a change in the position of medusa buds (Figure 8). The species with hydrorhiza exposed and covered by perisarc have medusa buds arising in clusters among proximal tentacles; the species with hydrorhiza covered by perisarc and creeping inside the bryozoan skeleton have buds clustered at the base of the hydranth; the species with Journal of the Marine Biological Association of the United Kingdom (2002) S. Puce et al. 953 hydrorhiza deprived of perisarc have buds growing at the base of the hydranth and from the hydrorhiza. REFERENCES Allman, G.J., 1883. Report on the Hydroida dredged by H.M.S. Challenger during the years 1873^1876. Part I. Plumularidae. Scienti¢c Results of the Challenger Expedition. Zoology, 7, 1^54. Allman, G.J., 1888. Report on the Hydroida dredged by H.M.S. Challenger during the years 1873^1876. Part II. The Tubularinae, Corymorphinae, Campanularinae, Sertularinae and Thalamophora. Scienti¢c Results of the Challenger Expedition. Zoology, 23, 1^90. Barber, P.H., Palumbi, S.R., Erdmann, M.V. & Kasim Moosa, M., 2000. A marine Wallace’s line? Nature, London, 406, 692^ 693. Bavestrello, G., Puce, S., Cerrano, C. & Balduzzi, A., 2000. Life history of Perarella schneideri (Hydrozoa, Cytaeididae) in the Ligurian Sea. Scientia Marina, 64, 141^146. Bedot, M., 1909. Sur la faune de l’Archipel malais (Re¤sume¤). In Voyage dans l’Archipel malais (M. Bedot and C. Pictet). Revue Suisse de Zoologie, 17, 143^169. Billard, A., 1913. Les Hydroides de l’expe'dition du Siboga. I. Plumularidae. Siboga Expedition, 7a, 1^115. Billard, A., 1925. Les Hydroides de l’expe'dition du Siboga. II. Synthecidae et Sertularidae. Siboga Expedition, 7b, 117^232. Boero, F., Bouillon, J. & Gravili, C., 2000. A survey of Zanclea, Halocoryne and Zanclella (Cnidaria, Hydrozoa, Anthomedusae, Zancleidae) with a description of new species. Italian Journal of Zoology, 67, 93^124. Boero, F. & Hewitt, C.L., 1992. A hydrozoan, Zanclella bryozoophila n.gen., n.sp. (Zancleidae), symbiotic with a bryozoan, with a discussion of the Zancleoidea. 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