A hydrozoan, Zanclella bryozoophila n.gen., n.sp ...

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Octotiara (see Boero and Bouillon 1989a), Perarella (see. Motz-Kossowska 1905), and Hydranthea (see Boero and Sari. 1987). Osman and Haugsness (1981) ...
A hydrozoan, Zanclella bryozoophila nagen.; n. spa (Zancleidae), symbiotic with a bryozoan, with a discussion of the Zancleoidea F. BOERO Dipartimento di Biologia, Universita di Lecce, 73100 Lecce, Italy AND

C. L. HEWITT Oregon Institute of Marine Biology, Charleston, OR 97420, U.S. A.

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Received October 15, 1991 Accepted April 1 , 1992 BOERO,F., and HEWITT,C. L. 1992. A hydrozoan, Zanclella bryozoophila n.gen., n.sp. (Zancleidae), symbiotic with a bryozoan, with a discussion of the Zancleoidea. Can. J. Zool. 70: 1645- 1651. A new genus and species of hydroid, Zanclella bryozoophila, symbiotic with bryozoans is described. The colony is polymorphic and highly integrated with its bryozoan host. The gastrozooids have one or, rarely, two tentacles; dactylozooids are without tentacles. The medusa stage is reduced to liberable eumedusoids produced on the hydrorhiza, and has exumbrellar nematocyst chambers. 'The cnidome of both stages consists of stenoteles and macrobasic euryteles. General morphology and cnidome structure place this newly described form in the Zancleidae. A new genus is recognized on the basis of polymorphism of the hydroid and reduction of the medusa stage. The association with the bryozoan is described as commensal. Hydranths appear to feed on particles gathered by ciliary action of the bryozoan lophophore, and the hydrorhiza is surrounded by the bryozoan skeleton. The advantage of this relationship to the bryozoan is believed to be protection, effected by the nematocysts of the hydroid. BOERO,F., et HEWITT,C. L. 1992. A hydrozoan, Zanclella bryozoophila n.gen., n.sp. (Zancleidae), symbiotic with a bryozoan, with a discussion of the Zancleoidea. Can. J. Zool. 70 : 1645- 1651. On trouvera ici la description d'un nouveau genre et d'une nouvelle espece d'hydroi'de, Zanclella bryozoophila, qui vit en symbiose avec des bryozoaires. La colonie est polymorphe et fortement intCgrCe aux bryozoaires h8tes. Les gastrozooi'des ont un tentacule, rarement deux; les dactylozooi'des n'ont pas de tentacules. Le stade mCduse est rCduit a des eumCdusoi'des libkrables, produits sur l'hydrorhize, et possede des chambres de nCmatocystes hors de l'ombrelle. Le cnidome des deux stades se compose de stCnot5les et d'euryt5les macrobasiques. La morphologie gCnCrale et la structure du cnidome placent cette nouvelle forme dans les Zancleidae. Le polymorphisme de l'hydroi'de et la rCduction du stade mCduse justifient la crCation d'un nouveau genre. L'association avec le bryozoaire est de type commensal. Les hydranthes semblent se nourrir de particules accumulCes par les mouvements ciliaires du lophophore du bryozoaire et l'hydrorhize est entour6 par le squelette du bryozoaire. L'avantage que tire le bryozoaire de cette association en est probablement un de protection assure par les nCmatocystes de l'hydroi'de. [Traduit par la rCdaction]

Introduction Commensal association with bryozoans is well known in hydroids. Examples are found in the genera Zunclea (see Russell and Rees 1936), Halocoryne (see Hadii 1917), Octotiara (see Boero and Bouillon 1989a), Perarella (see Motz-Kossowska 1905), and Hydranthea (see Boero and Sari 1987). Osman and Haugsness (1981) showed that the symbiosis between a Zunclea sp. and bryozoans is mutualistic. Both hydroid and bryozoan benefit from the defensive structures of their associate. The calcareous skeleton of the bryozoan covers the hydroid hydrorhiza, while Zunclea provides the bryozoan with the protection afforded by nematocysts. Furthermore Osman and Haugsness (198 l) demonstrated experimentally that the bryozoan colonies (Schizoporella errata (Waters) and Celleporaria brunnea (Hincks)) associated with hydroids are more successful competitors for space and suffer less predation than colonies without associated hydroids. Riestedt and Schuhmacher (1985) obtained similar results in an in situ study on the competitive ability of a coral reef bryozoan associated with an unidentified species of Zunclea. This association demonstrated considerable integration between the hydroid and bryozoan structures, the hydroid hydrorhizae being enclosed by the bryozoan skeleton. We describe herein a new hydroid living with a bryozoan, Schizoporella sp., in central California. The association is an Printed in Canada I Imprime au Canada

intimate one and probably represents another example of mutualism between a hydroid and a bryozoan.

Materials and methods The first specimen of this species was found on a colony of the bryozoan Schizoporella sp. (Fig. 1) on June 25, 1983. It was collected at -0.3 m mean lower low water in a sheltered position on the North Jetty at the entrance of Bodega Harbor, Sonoma County, California. Given the unique and peculiar features of the colony, it was immediately preserved. Extensive collections of Schizoporella spp. colonies from the same locality were made. On June 29, a second, much larger colony of the bryozoan with the symbiotic hydroid was found. This colony was fragmented into five pieces, which were maintained in a flow-through seawater table at the Bodega Marine Laboratory. Other colonies were subsequently found from the same locality. Newly hatched Artemia nauplii and the larvae of the echiuran Urechis caupo were used in attempts to feed the hydroid.

Results Systematics

TYPE

herein.

Zanclella n. gen. SPECIES:Zunclella bryozoophila, n. sp., designated

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FIG. 1 . Frontal view of Schizoporella sp. with Zanclella bryozoophila n.sp. hydrorhiza covered by the bryozoan calcified frontal surface.

ETYMOLOGY: Zanclella =

"little Zanclea, ' ' gender feminine. DIAGNOSIS: Colony polymorphic, with gastrozooids and dactylzooids, gastrozooids with reduced number of tentacles. Gonophores eumedusoids, arising from hydrorhiza, bearing exumbrellar nematocyst chambers. Cnidome consisting of stenoteles and macrobasic euryteles in both hydroid and eumedusoid.

Zanclella bryozoophila n. sp. TYPE MATERIAL: Holotype consisting of fragments of a large Schizoporella sp. colony hosting the hydroid, and a vial containing 12 eumedusoids with additional colony fragments. Deposited in the Royal Ontario Museum, Department of Invertebrate Zoology, Catalog No. ROMIZ B 1151. TYPE LOCALITY: North Jetty of Bodega Harbor at Bodega Bay, Sonoma County, California (latitude 38 " 18'N, longitude 123'3'W). DIAGNOSIS: Colony stolonal and polymorphic, gastrozooids with one or, rarey, two oral capitate tentacles. Dactylozooids with a distal nematocyst cluster. Eumedusoids arising from hydrorhizae, with four perradial nematocyst chambers on exumbrella containing macrobasic euryteles, four radial canals, a ring canal, a narrow velum, gametes in a single mass encircling the manubrium, with stenoteles in the manubrium. Cnidome of both stages: stenoteles and macrobasic euryteles.

Description Hydroid contracted, disappearing into bryozoan skeleton, and practically invisible. Only nematocyst clusters of tentacles and dactylozooids visible as minute refringent spheres, usually above the zooecial openings of bryozoan. Colony stolonal, hydrorhizae appearing as refringent tracks between bryozoan zooecia, following shallow grooves on surface of bryozoan colony. Hydrorhizae mostly covered by bryozoan skeleton. Two polyp types (gastrozooids and dactylozooids) arising directly through openings in the bryozoan skeleton, or from hydrorhizae emerging from the skeleton for a short distance. Polyps occurring at intersections of bryozoan zooecia or directly in front of zooecial openings. Gastrozooid tube-like, hypostome short, with one short tentacle, inserted below hypostome, contractable independent of the polyp (Fig. 2A); gastrozooids rarely with two tentacles (Fig. 2B). Dactylozooid long, slender, with a capitate tip, deprived of mouth and tentacle(s) (Fig. 2C). Nematocysts on capitate tip of gastrozooid tentacle and dactylozooid consisting of stenoteles of two rather constant sizes: 20 x 13 and 7 x 4 pm (Figs. 3B, 3C). The same nematocysts, in lower densities, found in polyp body and hydrorhizae. Large macrobasic euryteles (30 x 17 pm) found solely in hydrorhizae (Fig. 3A). Medusa stage in form of eumedusoids (Figs. 4A, 4B) arising

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FIG. 2. Zanclella bryozoophila n.sp. ( A )Common gastrozooid with single tentacle. (B) Rare gastrozooid with two tentacles. (C) Dactylozooid.

from the hydrorhizae, spawning either when still attached to colony or upon being released and free-living for a few hours. Liberated eumedusoids nearly spherical, bell thin, four radial canals, ring canal present, velum narrow, manubrium quadratic at base and containing stenoteles, completely surrounded by gametes in the distal two-thirds. Four perradial nematocyst

chambers on exumbrella, containing macrobasic euryteles. Tentacular bulbs, tentacles, and mouth absent. Cnidome identical with that of the hydroid. Slightly contracted specimens wi'th an octagonal subumbrella and umbrella. ETYMOLOGY: The specific name bryozoophila refers to the affinity between the hydroid and its bryozoan host.

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FIG. 3 . Nematocysts of Zanclella bryozoophila n.sp. ( A ) Undischarged and discharged macrobasic euryteles. (B) Undischarged and discharged small stenoteles. (C) Undischarged and discharged large stenoteles.

Systematic position of Zanclella bryozoophila The presence of nematocyst chambers on the exumbrella and the cnidome of both polyp and medusa stages indicate that this species is referable ot the Zancleoidea (see Bouillon 1985; Petersen 1990). The morphology of both stages, however, is very different from that of other zancleoid families (for diagnoses see Bouillon 1985 and Petersen 1990). The association with bryozoans, the cnidome, and the presence of nematocyst chambers on the exumbrella suggest that Zanclella is a specialized member of the Zancleidae. Characters such as polymorphism and reduction in number of tentacles of the hydroid stage, and reduction of the medusa stage with gametes completely surrounding the manubrium, however, do not fit the diagnosis of any of the other known genera in the Zancleidae

(see Bouillon 1985 and Petersen 1990), and a new genus is proposed for the present species. Zanclella is here considered to be derived from a Zanclea-like ancestor, and it seems unwise to propose a new family for it. Additional differences between Zanclella and Zanclea (the best studied genus of the Zancleidae) are the distribution of nematocysts, particularly in the medusa stage. The exumbrellar chambers of Zanclea, in fact, contain stenoteles, whereas macrobasic euryteles are in the cnidophores on the tentacles. The eumedusoid of Zanclella, deprived of tentacles, has stenoteles on the manubrium and macrobasic euryteles restricted to the exumbrellar chambers. The macrobasic euryteles of Zanclella hydroids and medusae, furthermore, are similar in shape to those of Zanclea hydroids, but differ markedly from the shape of the macro-

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FIG. 4 . Zanclella bryozoophila n.sp. ( A ) Liberated eumedusoid, oral view. (B) Liberated eumedusoid, lateral view.

basic euryteles of Zanclea medusae (Bouillon 1974). When discharged, the macrobasic euryteles of Zanclella have a shaft that is less distinctly swollen at its tip than is usual. In shape, they more closely resemble the mastigophores. Macrobasic mastigophores are reported for Millepora hydroids (Bouillon 1985), so it would not be surprising to report them in another capitate hydroid. The study of abundant material of both hydroids and medusae of several undescribed Zanclea species (F. Boero and J. Bouillon, unpublished data) has demonstrated such a wide variation in shaft morphology in various species that a gradation can be detected, from 'true' euryteles to 'apparent' mastigophores. Picard (1957) reported the presence of macrobasic euryteles similar to mastigophores for Rosalinda incrustans (Kramp), as did Bouillon and Gravier-Bonnet (1987) for Pseudosolanderia picardi Bouillon and GravierBonnet. The evolutionary trend leading to the transformation of euryteles into the 'mastigophores' of the Zancleidae is probably different from that leading to the mastigophores of the Leptomedusae, for instance. For this reason we prefer to use the term eurytele for the nematocysts of Zanclella. The resemblance of the hydroid stage of Zanclella bryozoophila with the tentacle-less Halocoryne epizoica Hadii, which is also symbiotic with a Schizoporella species of the Mediterranean Sea, is remarkable. Bouillon (1974, 1985), followed by Petersen (1990), included Halocoryne in the Corynoidea, owing to the absence of macrobasic euryteles in the hydroid stage. This is confirmed by further examination of Mediterranean material of H. epizoica (Piraino et al. 1992). Picard (1957) established a new monotypic family, the Halocorynidae, for Halocoryne. The eumedusoid of H. epizoica, figured by Bouillon (1974) without a description, has no nematocyst chambers on the exumbrella and its cnidome was reported by Bouillon (1985) to consist of stenoteles and occasional desmonemes. These features are typical of corynoid polyps and medusae. A member of the Zancleidae (Zanclea protecta Hastings), on the other hand, has been described as

having stenoteles only in its hydroid stage (Hastings 1930), the typical cnidome of many corynoid hydroids. Examination of type material of 2. protecta on microscope slides deposited in the Natural History Museum in London, England, confirms the absence of macrobasic euryteles in Hastings' material. Likewise the hydroid Zanclea alba (Meyen) has stenoteles only (Calder 1988). Recent examination of abundant material of Halocoryne epizoica from the Mediterranean (Piraino et al. 1992) established the presence of macrobasic euryteles (?) and macrobasic mastigophores in the eumedusoid. When undischarged, the macrobasic mastigophores have a shaft coiled like that of desmonemes, but the presence of discharged threads confirmed that they were mastigophores. The absence of exumbrellar chambers in the eumedusoid of Halocoryne could justify retention of the genus in a separate family, but the presence of euryteles and mastigophores in the medusa allows its inclusion in the Zancleoidea and not in the Corynoidea. These new findings require emendation of the diagnoses of the superfamily Zancleoidea to include features of Zanclella and Halocoryne, and of the family Zancleidae to include features of Zanclella. Owing to its complete coverage of hydromedusan genera and supragenera, the paper by Bouillon (1985) is taken as the source of the diagnoses to be emended. The emendations to the translations from French of Bouillon's diagnoses are in italics. SUPERFAMILY

Zancleoidea

Polyps colonial, monomorphic o r polymorphic, with hydrorhizae formed either by tubes of coenosarc covered with perisarc, or by an encrusting coenosarc forming a plate, or by a coenosarc with a 'horny or calcareous' exoskeleton. Hydranth simple, with no diaphragm, generally with one oral ring of capitate tentacles (exceptionally claviform, or reduced to one in number, or absent), usually associated with aboral tentacles

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FIG. 5. Zanclella bryozoophila n.sp. Schematic representation of three gastrozooid behaviors (see text for description).

in verticils or scattered, either moniliform, or branched capitate, or simple capitate, or cane-like, rarely only oral capitate tentacles, or tentacles all capitate and arranged irregularly. Reproduction by free medusae, or liberable eumedusoids, or fixed gonophores. Medusae, when present, with two to four radial marginal tentacles, with cnidophores, with and without ocelli. Gonads rarely in a single mass, usually divided into four distinct masses. Nematocysts: Atrichous haplonemes, macrobasic mastigophores (?), microbasic euryteles, macrobasic euryteles, stenoteles. FAMILY

Zancleidae

Colonial Zancleoidea, monomorphic or polymorphic, with simple perisarc enveloping just the hydrorhiza, or both hydrorhiza and stem. Hydanths rarely with no or few tentacles, usually with a large number of tentacles all capitate or claviform, arranged into an oral ring, the others being in verticils or scattered on the polyp body. Medusae with pockets or tracts of exumbrellar nematocysts, a simple circular mouth, with or without oral tentacles. Four radial canals, exceptionally bifurcated. Gonads rarely in a single mass on the manubrium of eumedusoids, usually differentiated in an interradial position, two or four marginal tentacles armed by abaxial rows of cnidophores, marginal tentacles sometimes absent. No ocelli. Biological observations Of about 50 colonies of bryozoans, primarily Schizoporella spp., collected from the North Jetty of Bodega Harbor, 10 were host to symbiotic hydroids. Eight of these hydroid colonies were Zanclea spp. and two were the new species Zanclella bryozoophila. Of the latter, the most obvious evidence of the hydroid in recently disturbed colonies is the nematocyst clusters of the polyps, which appear as minute refringent spheres on the bryozoan surface. Given time and freedom from disturbance, the bryozoans extend their lophophores and the hydroid polyps extend. A fully extended polyp reaches well above the adjacent lophophores and may extend to a length of about 6 mm. The dactylozooids were about twice as numerous as the gastrozooids. We counted 20.6 ( f3.5) dactylozooids/cm2 and 10.2 ( f2.6) gastrozooids/cm2. The bryozoan zoecia were much more abundant, occurring at a density of about 404.1 ( f52. 2)/cm2.

A hydroid colony collected in July was broken into five pieces, which were kept in individual finger bowls submerged in circulating seawater. Artemia nauplii and Urechis caupo larvae were offered as food. Both gastrozooids and dactylozooids captured these food items, but did not ingest them. In spite of our failure to observe feeding by the hydroid, the five colony pieces thrived and eumedusoids were first noted in late August. As colonies seemingly thrived and reproduced, squash preparations of both bryozoan zooids and hydroid gastrozooids were made to determine what, if anything, these organisms were eating. The preparations revealed many small particles in the digestive tracts of both species. The majority of the particles were of similar size, were greenish in color, and appeared to be unicellular algae. Observations of hydroid behavior strongly suggest that the polyps may take food particles from the bryozoan. When the bryozoan lophophores were expanded, the hydroid polyps were active and displayed different behaviors. The dactylozooids extended above the lophophores, easily surpassing them in height. The gastrozooids had three distinct behaviors (Figs. 5A, 5B, 5C). The hydroid bent over until the hypostome was inside the tentacular crown of the lophophore; the tentacle was held upright during this maneuver (Fig. 5A). Gastrozooids were also seen extending the tentacle inside the lophophore, placing the hypostome near the bryozoan lophopore tips (Fig. 5B). Gastrozooids were also seen placing the tentacle inside the lophophore, while the mouth was held upright. This action was immediately followed by the tentacle bending up towards the hypostome and then touching the mouth (Fig. 5C). None of these actions caused the lophophore to retract. Although no particles were seen passing between the bryozoan and the hydroid, the observed behavior suggests that the hydroid was indeed feeding from material gathered by the brozoan with the filtering action of the lophophore. The similarity of the particles we observed in the digestive tracts of the two partners reinforces this idea.

Discussion Osman and Haugsness (1981) studied hydroids symbiotic with bryozoans along the coast of southern California. They did not report finding a hydroid that could have been Zanclella

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BOERO A N D HEWITT

bryozoophila, thus we assume that this species is restricted to the colder waters of central and northern California. T o date, however, we have noted its presence only in the Bodega Bay area. In observing the living hydroid we were unable to determine how it obtained the small green particles observed in its coelenteron. The behavior of the polyps suggests that the hydroid may be talung its food from the particles collected by its bryozoan host, thus having a microphagous diet. We also assume that the association is one that benefits both partners. The large macrobasic euryteles contained in the hydrorhizae would presumably be effective only when the calcareous skeleton of the host (the calcified frontal surface of Schizoporella sp.) is disturbed by some predator, such as a nudibranch. The smaller stenoteles of the polyps presumably would be effective against predators such as flatworms, which would otherwise prey upon the bryozoan. We have no experimental evidence, however, to support the assumption of mutualism, but can speculate that this hydroid depends upon its host for food and is protected by its host's skeleton, while the hydroid protects its host from specific predators. The association, then, is a most intimate one and is possibly mutually beneficial. The phylogenetic affinities detectable from the available characters tend to place Zanclea, Zanclella, and Halocoryne along the same evolutionary line. They are all zancleoids showing different levels of reduction and integration with bryozoan colonies. The described bryozoan-associated Zanclea species, with hydrorhizae covered by the bryozoan skeleton, have normally developed, monomorphic polyps with a large number of tentacles, and are usually unable to contract within the bryozoan host. Their medusae are liberated as immature stages from the colony and sexual maturity is attained after a relatively long period in the plankton. Zanclella has a more intimate association with the bryozoan, being able to completely retract into the skeletal structure and having smaller polyps and fewer tentacles than Zanclea. Further specializations are found in the mode of feeding, the polymorphism of the colony, and the reduction of the medusa, represented by a short-lived eumedusoid already ripe at liberation which, however, retains the exumbrellar chambers typical of the Zancleidae. Halocoryne is polymorphic like Zanclella, but its polyps are completely deprived of tentacles, and the absence of macrobasic euryteles in the hydroid can also be considered a reduction. The eumedusoid of Halocoryne is more reduced than that of Zanclella, having lost the exumbrellar chambers typical of the Zancleidae. The reduction of the medusa stage is a common theme in the evolution of hydromedusae (for recent discussions see Boero and Bouillon 1987; Boero and Sari 1987; Boero and Bouillon 1989b); in this case this pattern is paralleled in the polyp stage by both reduction and suppression of tentacle number, and by the formation of polymorphic colonies.

Acknowledgements This work was carried out with financial contributions from The United Nations Food and Agriculture organization and Environment Programme and the Minister0 della Ricerca Scientifica e Tecnologica (funds of 40 % and 60 % programs), F. Boero's stay at the Bodega Marine Laboratory was funded by the Consiglio Nazionale delle Ricerche. Comparative work on Zanclea nematocysts was funded by the Fonds de la

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Recherche Fondamental Collective no 2.900 1.86. Profs. Cadet Hand (Bodega Bay) and Ralph Smith (Berkeley) greatly encouraged and helped us during our stay at the Bodega Marine Laboratory, aiding in the revision of early drafts of the manuscript. Prof. Jean Bouillon (Bruxelles) and Dr. Dale Calder (Toronto) read and commented on the manuscript. Drs. Paul F. S. Cornelius and Simon Moore (London) made type material of Zanclea protecta available. Boero, F., and Bouillon, J. 1987. Inconsistent evolution and paedomorphosis among the hydroids and medusae of the Athecatael Anthomedusae and the ThecataeILeptomedusae (Cnidaria, Hydrozoa). In Modern trends in the systematics, ecology, and evolution of hydroids and hydromedusae. Edited by J. Bouillon, F. Boero, F. Cicogna, and P. F. S. Cornelius. Clarendon Press, Oxford. pp. 229-250. Boero, F., and Bouillon, J. 1989a. The life cycles of Octotiara russelli and Stomotoca atra (Cnidaria, Anthomedusae, Pandeidae). Zool. Scr. 18: 1-7. Boero, F., and Bouillon, J. 1989b. An evolutionary interpretation of anomalous medusoid stages in the life cycles of some Leptomedusae (Cnidaria). In Reproduction, genetics and distributions of marine organisms. Edited by J . S. Ryland and P. A. Tyler. Olsen & Olsen, Fredensborg, Denmark. pp. 37-41. Boero, F., and Sara, M. 1987. Motile sexual stages and evolution of Leptomedusae (Cnidaria). Boll. Zool. 54: 131- 139. Bouillon, J. 1974. Description of Teissiera milleporoides, nouveau genre et nouveau espkce de Zancleidae des Seychelles (Hydrozoaires; Athecates-Anthomeduses). Cah. Biol. Mar. 15: 113154. Bouillon, J. 1985. Essai de classification des Hydropolypes Hydromeduses (Hydrozoa - Cnidaria). Indo-Malayan Zool. 2: 29 - 243. Bouillon, J ., and Gravier-Bonnet, N. 1987. Pseudosolanderia picardi, nouveau genre et nouvelle espkce de Rosalindidae de la RCunion (Anthomedusae, Hydrozoa, Cnidaria). Bull. Mus. Natl. Hist. Nat. 4 3 e r . Vol. 9. Sect. A No. 4. pp. 755 -771. Calder, D. 1988. Shallow-water hydroids of Bermuda: the Athecatae. R. Ont. Mus. Life Sci. Contrib. No. 148. Hadii, J. 1917. Rezultati bioloSkih istraiivanja Jadranskoga mora. Hidroidi 11. Halocoryne epizoica g.n., sp.n. ; Lafoeina vilaevelebiti sp.n., Prirodosl. Istraz. Hrv. Slav. Potak. 11: 1-61. Hastings, A. 1930. On the association of a gymnoblastic hydroid (Zanclea protecta, sp.n.) with various cheilostomatous Polyzoa from tropical E. Pacific. Ann. Mag. Nat. Hist. Ser. 10, 5: 552 560. Motz-Kossowska, S. 1905. Contribution a la connaissance des Hydraires de la MCditerranCe occidentale. I. Hydraires Gymnoblastiques. Arch. Zool. Exp. Gen. 4(3): 39-98. Osman, R., and Haugsness, J. 1981. Mutualism among sessile invertebrates: a mediator of competition and predation. Science (Washington, D.C.), 211: 846- 848. Petersen, K. W. 1990. Evolution and taxonomy in capitate hydroids and medusae. Zpol. J. Linn. Soc. 100: 101 -23 1. Picard, J. 1957. Etudes sur les hydroides de la superfamillle des Pteronematoidea. I. GCnCralitCs. Bull. Inst. Oceanogr . (Monaco) No. 1106. pp. 1-12. Piraino, S., Bouillon, J., and Boero, F. 1992. Halocoryne epizoica (Cnidaria), a hydroid that bites. Sci. Mar. 56: 141- 147. Riestedt, H., and Schuhmacher, H. 1985. The bryozoan Rhynchozoon larreyi (Audouin 1926) - a successful competitor in coral reef communities of the Red Sea. Mar. Ecol. (Berlin), 6: 167179. Russell, F., and Rees, W. 1936. On rearing the hydroid Zanclea implexa (Alder) and its medusa Zanclea gemmosa McCrady, with a review of the genus Zanclea. J. Mar. Biol. Assoc. U.K. 21: 107 - 129.