Hydrozoa (Cnidaria) symbiotic with Porifera: a review

Marine Ecology. ISSN 0173-9565

REVIEW ARTICLE

Hydrozoa (Cnidaria) symbiotic with Porifera: a review S. Puce1, B. Calcinai1, G. Bavestrello1, C. Cerrano2, C. Gravili3 & F. Boero3 1 Dipartimento di Scienze del Mare, Universita` Politecnica delle Marche, Via Brecce Bianche, Ancona, Italy 2 Dip.Te.Ris., Universita` di Genova, Corso Europa, Genova, Italy 3 Di.S.Te.B.A., Universita` di Lecce, Lecce, Italy

Keywords Hydroids; hydrozoans; marine benthos; sponges; symbiosis. Correspondence S. Puce, Dipartimento di Scienze del Mare, Universita` Politecnica delle Marche, Via Brecce Bianche, I-16131 Ancona. E-mail: [email protected] Accepted: 16 August 2005 doi:10.1111/j.1439-0485.2005.00050.x

Abstract Many hydroids are symbiotic with other organisms. Sponges, because of their complex canal system and their filter-feeding activity inducing a continuous water flow, are used by numerous species as either exclusive or facultative substrata. The associated hydroid fauna thriving on or inside sponges shows a wide range of relationships with their hosts. Hydroids may be simply epibiotic on sponges, their stolons running on the host surface. Alternatively, the stolons may grow inside the sponge body, the polyps emerging from the sponge surface, having also the possibility of retraction inside the sponge tissue. Finally, stolons and branches may develop deeply inside the sponge body, producing a skeletal network for sponge growth. This paper reviews the described relationships of hydrozoans symbiotic with sponges and reports new observations.

Problem The hydroids of several hydroidomedusan taxa show specialized symbiotic associations with other organisms, see Piraino et al. (1994) and Boero & Bouillon (in press) for lists. Sponges, with their body permeated by a complex canal system where a continuous water flow is induced by their filter-feeding activity, are temporary or permanent substrata for many hydroid species. A rich associated hydroid fauna thrives on or inside sponges; the records of hydroid-sponge associations are scattered in the literature and mostly report only on the co-occurrence of these animals. The techniques employed for the preservation and study of sponges are not conducive to the identification of hydroids: data about this symbiosis are extremely poor in the spongological literature (Sara` & Vacelet 1973) and most information derives from hydroid-centred studies. In this paper, the described relationships of hydrozoans symbiotic with sponges are reviewed, together with new observations. Marine Ecology 26 (2005) 73–81 ª 2005 Blackwell Publishing Ltd

Relationships between hydroids and sponges Types of sponge–cnidarian association

The Cubozoa are the only cnidarian class with no species associated with sponges. In the Anthozoa, the Zoantharian Parazoanthus axinellae (Schmidt, 1862) is often epibiotic on sponge species of the genus Axinella (Arndt 1936; Lewis 1982). Host-selectivity, however, is not exclusive for this species, which, in fact, commonly settles directly on overhanging rocks. Symbiosis between sponges and octocorals is rarely recorded (Soest van & Verseveldt 1987; Calcinai et al. 2004). In the Scyphozoa, the polyps of Nausithoe punctata Kolliker, 1853 are strictly associated with horny sponges and might contribute to their skeletal structures (Uriz et al. 1992). The greatest diversity in the association between Cnidaria and Porifera, however, is found in the Hydrozoa. The relationship between hydrozoans and sponges can be divided into three categories: 73

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1 Hydroid larvae (either planulae or actinulae) settle on a non-sponge substrate and later a sponge overgrows the hydrorhizae of an already formed colony. Encrusting sponges are the best candidates for such association pattern, which might be considered as occasional (e.g. Riedl 1966; Boero 1984; Gili & Hughes 1995). 2 Hydroid larvae settle on sponges, but the hydrorhizae of the resulting colony are not embedded in the sponge tissues. The association is occasional and the involved hydroid species can grow on various substrates (Boero 1984). 3 Hydroid larvae penetrate the sponge host, developing a hydrorhizal system embedded in its tissues. The association is usually exclusive and obligatory. Only the third case can be considered as a real symbiosis, evolved by coevolutionary processes. The hydroid– sponge integration can differ according to the hydroid species: 1 The hydranths protrude from the sponge surface and cannot retract into it. 2 The hydranths protrude from the sponge surface but can retract into the host body, completely disappearing. 3 The hydranths grow into the canal system of the sponge and are not visible from the outside. Most of the hydroid species strictly associated with sponges and never found on other substrates are referred to the families Corynidae, Tubulariidae and Sphaerocorynidae, but some are also Cytaeididae and Campanulariidae.

Family Cytaeididae Genus Cytaeis

Cytaeis spongicola (Haeckel, 1889) and Cytaeis abissicola (Haeckel, 1889) occur in association with a genus of Demospongiae, Psammoclema Marshall, 1980 (¼ Psammopemma) and with some other genera (Stammophyllum, Psammophyllium, Cerelasma identified by Haeckel (1889) (Rees 1962) whose attribution to the phylum Porifera is now dubious (Hooper & Soest van 2002).

Family Corynidae (for a revision see Schuchert 2001) Genus Dipurena

The hydroid of Dipurena halterata (Forbes, 1846) was described in British waters as associated with sponges (Rees 1939). The association has also been recorded from the Mediterranean Sea (Boero & Fresi 1986). The hydroid lives in and on the sponges Haliclona cinerea (Grant, 74

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Fig. 1. Dipurena halterata in Chondrilla nucula. The hydranths cannot withdraw into the sponge.

1826) (Rees 1938 as Chalina montagui), Haliclona simulans (Johnston, 1842), Petrosia ficiformis (Poiret, 1789), Chondrilla nucula (Schmidt, 1862) and Spirastrella cunctatrix (Schmidt, 1868). The stolons, covered by thin perisarc, are deeply embedded in the tissues of the sponge host (Schuchert 2001). In the Ligurian Sea (Italy), the hydroid is characterised by an annual cycle, occurring only during a short period of the year (Boero & Fresi 1986). The rest of the year is presumably spent as resting stolons surviving in the sponge tissues (Fig. 1). Dipurena simulans Bouillon, 1965 grows in and on the sponge Haliclona simulans: the stolons, covered by thin perisarc, are deeply embedded in sponge tissue. Hydranths usually have 10–13 tentacles, but those growing in the sponge canal system have up to 16 tentacles. Only the polyps living in the oscula of the host become sexually competent and develop medusa buds (Bouillon 1965). Colonies of Dipurena halterata and Dipurena simulans can live together in the same specimen of Haliclona simulans. The polyps of the two species are very similar and distinction is based only on medusa characters (Bouillon 1971). Dipurena strangulata McCrady, 1859 presents stolons with thin perisarc and deeply embedded in the tissue of the sponge Clathria prolifera (¼ Microciona prolifera) (Ellis & Solander, 1786) (see Schuchert 2001). Marine Ecology 26 (2005) 73–81 ª 2005 Blackwell Publishing Ltd

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Dipurena spongicola Anger von, 1972 occurs in the canal system of the sponge Halichondria panicea (Pallas, 1766). The stolons show a very thin perisarc. The stolon tips that come in contact with the canals of the sponge transform into hydranths and in one occasion, a young medusa was found inside a canal of the host’s aquiferous system. The hydroid apparently feeds on matter brought in the sponge’s filter current, as well as on cyclopoids, harpacticoids, ostracods, ciliates, turbellarian and nematodes inhabiting the canals of the sponge (Anger von 1972). Schuchert (2001) observed this hydroid living in a sponge tentatively classified as Suberites domuncula (Olivi, 1792). Genus Sarsia

Sarsia bella Brinckmann-Voss, 2000 is the only one among the 10 species of the genus recorded as growing in sponges. The unidentified sponge was encrusting the shell margin of a specimen of Hinnites multirugosus (Brinckmann-Voss 2000). This fact suggests that the association between this species and the sponge might be occasional. Genus Bicorona

Bicorona elegans Millard, 1966 was described with the stem embedded in the tissue of an unknown sponge (Millard 1966). The species was subsequently recorded from several South African localities but the association with sponges was never mentioned (Millard 1975). The only other known species of this genus, Bicorona tricycla (Schuchert, 1996), occurs on rock and macroalgae at low depth (Schuchert 1996).

Family Cladonematidae Genus Cladonema

Cladonema sp. has been recorded by Boero & Fresi (1986) as Sarsia sp., the polyps stretching out the pores of the sponge host and, if disturbed, retracting completely into the sponge body, becoming invisible from the outside (Fig. 2). M. P. Miglietta (personal communication) found this species along the Apulian coast and obtained a Cladonema medusa from it.

Family Tubulariidae (for a revision see Petersen 1990) Genus Hybocodon

The hydroids of all three species of Hybocodon have been recorded living in sponges. Hybocodon prolifer Agassiz, 1862 is characterised by a single hydrorhizal process, buried in sponge tissue, widening toward its distal extremity, Marine Ecology 26 (2005) 73–81 ª 2005 Blackwell Publishing Ltd

Fig. 2. Cladonema sp. in Ircinia sp. The hydranths are able to completely withdraw into the sponge pores.

and one or two thinner supporting tubes developed from basal part of hydrocaulus (Petersen 1990; Schuchert 2001). Hybocodon cryptus Watson, 1984 generally grows in sparse clusters of up to 15 well separated stems, growing to 8 cm in height from a hydrorhiza deeply embedded in unidentified sponges; it occasionally also occurs on old shells (Watson 1984). Hybocodon unicus (Browne, 1902) has a branched or unbranched hydrorhiza, widening to irregularly shaped tuber-like structures embedded in the sponge Hymeniacidon perlevis (Montagu, 1818) (Petersen 1990). Genus Zyzzyzus

Zyzzyzus spongicolus (Lendenfeld von, 1884) lives in ‘horny sponges’. Watson (1978) described the solitary hydranth roots in the canal system of the host sponge as finger-shaped hydrorhizal processes and the hydrocaulus embedded for one-third in the host body. Zyzzyzus warreni Calder, 1988 lives in a large variety of sponge species (Haliclona clathrata Dendy, 1905, H. permollis (Bowerbank, 1866), Clathria fasciculata Wilson, 1925, Aaptos ciliata (Wilson, 1925), Mycale angulosa (Duchassaing & Michelotti, 1864), Mycale laxissima (Duchassaing & Michelotti, 1864), Mycale microsigmatosa Arndt, 1927, Tedania ignis (Duchassaing & Michelotti, 1864), characterised by different skeletal texture (Hirohito 1988). Warren (1906, p. 89) described it as Tubularia solitaria and suggested a parasitic interaction with the sponge, stating ‘The sponge appears to attempt to shut itself off as much as possible from the hydroid; the tissues of the sponge in the immediate neighbourhood of the hydroid are denser and more fibrous than further in, forming a kind of cyst-wall’. Calder (1988) reported this species on sponges, but also on the hydroid Eudendrium carneum. 75

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Zyzzyzus calderi Petersen, 1990 was described with the hydrocaulus embedded in a sponge of the genus Tedania. Different from the other species, only the most distal part of the hydrocaulus is embedded in the sponge tissue, consisting of two to three small club-shaped tubers with finger-like distal processes. Zyzzyzus floridanus Petersen, 1990 is hosted by Callyspongia vaginalis (Lamarck, 1814); the hydrocaulus has globular rather than finger-shaped hydrorhizal bulbs embedded in the sponge. Genus Ectopleura

Ectopleura exxonia Watson, 1978, was described in association with sponges: its hydrorhiza is a matted reticulum penetrating 5–6 mm into the surface of an unidentified horny sponge. Genus Tubularia

Tubularia ceratogyne Pe´re`z, 1920 is associated with Halichondria panicea. Pe´re`z (1925) described the relationship in detail. The symbiosis strongly influences the ecology and the growth of the two partners. The bathymetric distribution of the hydroid is determined by the sponge distribution. The sponges colonised by T. ceratogyne grow along the hydroid hydrocaulus, producing erect protrusions arising from a massive body. The hydrocaulus, insulated by the sponge tissue, grows untidily producing irregular ramifications and perisarc thickenings. The loss of organisation of T. ceratogyne when associated with the sponge suggests that environmental conditions strongly modulate the processes involved in the branching pattern.

Fig. 3. Sphaerocoryne sp. in Aka mucosa. The hydrorhiza is filled by numerous nematocysts and is enveloped inside the sponge spicule tracts.

enveloped inside the sponge spicule tracts (Fig. 3). This growth structure suggests a reaction of the two partners, as recently observed in the octocoral Carijoa riisei living inside the sponge Desmapsamma anchorata (Calcinai et al. 2004). Genus Heterocoryne

Family Sphaerocorynidae Genus Sphaerocoryne

Sphaerocoryne bedoti Pictet, 1893 was described as living in two unidentified siliceous sponges: the hydrorhiza embedded in the sponge tissue and the hydrocauli arising from the pores (Pictet 1893). After this first record, S. bedoti was always observed in association with sponges, but no additional information about the host is known (Mammen 1963; Millard 1975; Calder 1988; Hirohito 1988). Sphaerocoryne agassizi (McCrady, 1859) was figured by Petersen (1990) as a single polyp collected in North Carolina (USA) from a colony growing on a sponge. In the Halong Bay, Vietnam, we collected several specimens of Sphaerocoryne sp. growing on the fistules of the boring sponge Aka mucosa (Bergquist, 1965). The hydrorhiza, running in the tissue of the fistule wall, is filled by numerous nematocysts (stenoteles of two sizes) and is 76

Heterocoryne caribbensis Wedler & Larson, 1986, the only species of this genus, was often observed growing in the sponges of the genus Mycale. No other detailed observation about the association are reported, but the picture showing this species in the original description (Wedler & Larson 1986) suggests that the sponge reacts to the hydroid presence by growing along its hydrocaulus.

Family Campanulariidae Genus Gastroblasta

Gastroblasta sp. (possibly G. raffaelei Lang, 1886), cited by Boero (1980) and Boero & Fresi (1986) as Clytia sp., lives in association with sponges. Recorded from the Ligurian Sea, the Gulf of Naples and the Adriatic Sea (Italy), its hydrorhiza is always embedded in the tissues of sponges of the genera Petrosia and Ircinia (Fig. 4). This is the only thecate hydroid exclusively associated with sponges. Marine Ecology 26 (2005) 73–81 ª 2005 Blackwell Publishing Ltd

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Fig. 4. Gastroblasta cf. raffaelei in Ircinia sp. Hydranth and gonothecae containing a single medusa bud.

Hydroids growing in hexactinellid sponges

Schulze (1880) described the association between the sponge Euplectella aspergillum Owen, 1841 and a gymnoblastic hydroid, named for this reason Bibrachium euplectellae (Schulze, 1880). As Schulze observed (p. 671), the hydrorhiza forms a ‘long-meshed net’ from which hydranths ‘project freely into the inhalant lacunae, and therefore toward the exterior, from the zone of ciliate chambers’. The hydroid appeared so abundantly in the Euplectella that, as noticed by Schulze, one or more hydranths are found in almost every microscopic section of the tube wall. Another record of association between hydroid and hexactinellid sponges is from Tuzet (1973) who observed an undetermined gymnoblastic hydroid, morphologically different but in behaviour similar to Dipurena spongicola, occurring in the sponges Walteria flemmingii Schulze, 1886 and W. leuckarti Ijma, 1896. The sponge shape, characterised by prominent and irregularly distributed oscula, appears determined by the presence of this hydroid. Other records

A colony of Cytaeis nuda Rees, 1962 is described partly immersed in a sponge growing on living gastropod Fusinus perplexus. The stolon runs parallel to and a little below the surface of the sponge (Rees 1962; Hirohito 1988). No additional information is available about the sponge. In Bermuda shallow waters, Calder (1988) observed colonies of the clavid Turritopsis nutricula McCrady, 1859, usually growing on different hard substrates, with Marine Ecology 26 (2005) 73–81 ª 2005 Blackwell Publishing Ltd

Fig. 5. Photographs of Nemalecium lighti growing on Carteriospongia foliascens (a) and Hydrichthelloides sp. growing on a unidentified sponge (b) from Bunaken Marine Park (North Sulawesi, Indonesia).

the hydrorhiza and much hydrocaulus embedded in the tissue of an unidentified sponge. In Indonesian waters, the substrate-generalist Nemalecium lighti (Hargitt, 1924) is found only on the fan shaped horny sponge Carteriospongia foliascens (Pallas, 1766) (Fig. 5a) while Cladocoryne floccosa Rotch, 1871 lives on the fistules of the psammobiotic sponge Oceanapia fistulosa (Bowerbank, 1873). Hydrichthelloides reticulata Bouillon, 1978, originally described from Papua New Guinea, was observed on different substrates (corals, tubes of polychaetes, rocks, shells, and sponges) (Bouillon 1978). In the Bunaken Marine Park (North Sulawesi, Indonesia) we collected numerous specimens of Hydrichthelloides sp. always living on sponge surfaces. They produce a dense stolonal net not penetrating in the sponge tissue and it may be detached like a film from the sponge surface (Fig. 5b). 77

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Discussion Partners’ roles

Boero & Fresi (1986) recorded settlement on sponges by species referred to the families Tubulariidae, Bougainvilliidae, Hydractiniidae, Pandeidae, Haleciidae, Hebellidae, Campanulariidae, Aglaopheniidae and Syntheciidae. These species, however, have been found also on other substrates and can be considered as simple epibionts, taking advantage of the sponge surface as substrate for settlement. Their harm to the functioning of the sponge is negligible, since the hydrorhizae are linear and do not impair the flow of water generated by the sponge. The incoming current generated by the sponge through its pores might be of some advantage to the hydroids, as suggested by Uriz et al. (1992) for Nausithoe. This water is often loaded with nutrients and the hydranths might increase the rate of prey capture because of the current produced by the pumping activity of the sponge. Hydroids obligatorily associated with sponges invariably have their hydrorhizae embedded into the host tissues. A foreign body growing into another organism is usually considered as a parasite; the association of hydroids with sponges probably evolved as a form of parasitism in which some hydroid species succeeded in overcoming the chemical defences that prevent the settlement of other organisms on most sponges. The hydrorhizae of these species passed from the surface to the inside of the host sponge, acquiring the same position that can be observed in hydroids overgrown by encrusting sponges. In this case, however, it is the hydroid that takes the initiative of growing into the sponge through specific larval settlement. For hydroids, the advantage of this association is the already mentioned increase of water renewal around the colony, enhancing feeding efficiency. Furthermore, the sponge protects the hydroid colony from predation by nudibranchs and from overgrowth by other benthic organisms. The price paid by the sponge, also in this case, might be negligible and the association might turn to be a form of mutualism, the hydrorhizae becoming an accessory skeletal structure for the sponge, as proposed by Uriz et al. (1992) for the association of scyphozoan polyps with sponges. Along the Portofino Promontory, Boero & Fresi (1986) reported that Dipurena halterata is present on sponges (Petrosia ficiformis, Spirastrella cunctatrix and Chondrilla nucula) from January to June. It is probable that when the hydroids disappear at the sponge surface their hydrorhiza survives as a resting stage embedded in the sponge tissues. The top of sponge–hydroid association is reached by Dipurena spongicola and Bibrachium euplectellae, showing extreme cases of endosymbiosis. Dipurena spongicola pre78

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sumably completes its life cycle inside the sponge canal system (Anger von 1972). The relationships among sponges and hydrozoans are strongly unbalanced as to biomass: the sponge partner is generally much larger than the hydroid guest. The only documented cases of sponge shape modification owing the presence of hydroids concern Halichondria panicea and Tubularia ceratogyne, and Heterocoryne caribbensis and Mycale sp. because the sponges react to the hydroid presence by growing along the hydroid hydrocaules. In this situation, sponges exploit the hydroid stem, becoming erect. The body of massive sponges is three-dimensional and the hydroid growth pattern inside their tissues is different from that of the species that normally grow on two-dimensional substrates. The possibility of growing in a three-dimensional space produces a disorganised hydrorhizal pattern. The same situation was recently recorded in an octocoral living inside the sponge Desmapsamma anchorata (Calcinai et al. 2004). Evolutionary trends in hydroid symbioses with sponges and other organisms

Many hydroid species are substrate generalist, often growing also on other organisms. In some families, this attitude represented a preadaptation to more strict relationships, leading to permanent associations. When the association with a particular type of host is widespread within a single genus or family, it is highly probable that an adaptive radiation from a single ancestral association occurred. In these cases, the ancestors, once established the association, became the founders of monophyletic clades containing species with similar host preferences. The most evident example of this trend is found in the Hebellidae (see Boero et al. 1997 for a revision) where all the species of the genera Hebella and Anthohebella are associated with hydroid hosts. Another case is the strict association between hydroids and bivalve hosts, with the genus Eugymnanthea that comprises species living exclusively in the mantle cavity of bivalves (Kubota 2000). Recently, Boero et al. (2000) revised the family Zancleidae, containing many species strictly associated with bryozoans, but also species associated with corals and algae. Species unrelated with the Zancleidae (see Bavestrello et al. 2000), however, have evolved symbiotic relationships with bryozoans, involving behavioural patterns that are strickingly similar to those of the Zancleidae. The association with bryozoans, thus, is undoubtedly polyphyletic within the Hydrozoa. Other cases of strict association between hydroids of a single clade and a definite host type is to be found in the Hydractiniidae, with a sharp preference towards gastropod shells, either living or inhabited by hermit crabs. Cunningham et al. (1991) Marine Ecology 26 (2005) 73–81 ª 2005 Blackwell Publishing Ltd

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Table 1. List of the records of hydroid species living with the colonies partially embedded in sponge tissue. Hydroid

Sponge host

Author

Dipurena halterata

Haliclona cinerea, Haliclona simulans, Petrosia ficiformis, Chondrilla nucula, Spirastrella cunctatrix Haliclona simulans Microciona prolifera Halichondria panicea, Suberites domuncula(?) Unidentified Petrosia ficiformis Ircinia sp. Unidentified Unidentified Hymeniacedon perlevis Unidentified Haliclona clathrata, Haliclona permollis Clathria fasciculata, Aaptos ciliatus Mycale angulosa Mycale laxissima Mycale microsigmatosa, Tedania ignis horny sponges horny sponge Callyspongia vaginalis Tedania sp. Unidentified Halicondria panicea Unidentified Unidentified Aka mucosa Mycale sp. Stammophyllum, Psammophyllum, Psammopemma Stammophyllum, Psammophyllum Petrosia ficiformis Ircinia sp. Euplectella aspergillum Walteria flemmingi, Walteria leuckarti

Rees (1938) as Chalina montagui Bouillon (1971) as Adocia simulans Boero & Fresi (1986), Schuchert (2001)

Dipurena simulans Dipurena strangulata Dipurena spongicola Sarsia bella Cladonema sp. Bicorona elegans Hybocodon prolifer Hybocodon unicus Hybocodon cryptus Zyzzyzus warreni

Zyzzyzus spongicolus Zyzzyzus floridanus Zyzzyzus calderi Ectopleura exxonia Tubularia ceratogyne Sphaerocoryne agassizi Sphaerocoryne bedoti Sphaerocoryne sp. Heterocoryne caribbensis Cytaeis spongicola Cytaeis abissicola Gastroblasta cf. raffaelei Bibrachium euplectellae gymnoblastic hydroid

showed that both host and guest lineages underwent parallel speciation patterns. All the above mentioned associations involve exclusively athecate (i.e. Anthomedusae) hydroids, suggesting that the biology of this group is conducive to the establishment of symbiotic relationships. The hydroid–sponge association is consistent with this trend and almost all species belong to the Anthomedusae. The only known exception is Gastroblasta raffaelei, a Campanulariid species with polygastric medusae and hydroids living embedded in sponge tissues. The array of genera with sponge-inhabiting species is rather vast. Some genera are represented by species that are all associated with sponges, such as Gastroblasta, Heterocoryne, Hybocodon, Zyzzyzus and Sphaerocoryne, whereas in others the association is occasional, as it might be argued for Tubularia, Dipurena, Cladonema, Sarsia, Cytaeis. Marine Ecology 26 (2005) 73–81 ª 2005 Blackwell Publishing Ltd

Bouillon (1965), Schuchert (2001) Schuchert (2001) Anger von (1972), Schuchert (2001) Brinckmann-Voss (2000) Boero & Fresi (1986) Millard (1966) Agassiz (1862), Petersen (1990) Browne (1902), Petersen (1990) Watson (1984) Calder (1988), Hirohito (1988), C.J.A. Campos, personal communication

Lendenfeld von (1885), Watson (1978) Petersen (1990) Petersen (1990) Watson (1978) Pe´re`z (1925) McCrady (1859), Petersen (1990) Pictet (1893), Millard (1975), Petersen (1990) Puce S., personal observation Wedler & Larson (1986) Haeckel (1889), Rees (1962) Haeckel (1889), Rees (1962) Boero & Fresi (1986) Schulze (1880) Tuzet (1973)

Sponge-inhabiting hydroids, thus, are referable to a disparate assortment of phylogenetically unrelated genera. The association with sponges evidently evolved several times along the phylogeny of Hydroidomedusae and is, thus, polyphyletic. In some cases, sponge-associated ancestors initiated adaptive radiations, leading to monophyletic clades of sponge-associated species of the same genus, whereas other associations arose isolately within clades that have no tendency to evolve symbiotic relationships, as is the case of the campanulariid Gastroblasta raffaelei. Host diversity

We know 26 identified species of hydroid-inhabited sponges (Table 1), belonging to the demosponge orders Hadromerida (4 species), Poecilosclerida (8 species), Halichondrida (2 species), Haplosclerida (8 species), 79

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Dictyoceratida (1 species), and to the Hexactinellid order Lyssacinosida (3 species). These species do not share any peculiar morphological or skeletal characters suggesting selectivity in the hydroid choice. Recently, the selectivity of Z. warreni against different sponge species was experimentally tested. This experiment showed that the settling of actinulae is different in different species of sponges suggesting an important role of the sponge chemical defences on the viability of hydroid larvae (C. J. A. Campos, personal communication).

Conclusion The integration of hydroid colonies into sponge hosts is sometimes total. Some species can retract entirely into the sponge body (Cladonema sp.) and others live completely embedded into the host (Dipurena spongicola). Close inspection of the surface and the inside of massive sponge species, thus, will surely lead to the discovery of new species of hydroids, or, at least, to the elucidation of life cycles for species in which only the medusa stage is described.

Acknowledgements Financial support was provided by MIUR (PRIN and FIRB projects), NSF (PEET project), the MARBEF Network of Excellence ‘Marine Biodiversity and Ecosystem Functioning’ funded in the EU Sixth Framework Programme (contract no. GOCE-CT-2003-505446).

References Agassiz L. (1862) Contributions to the Natural History of the United States of America. 2nd monograph. Little, Brown and Co., Boston: 380 pp. Anger K. von (1972) Dipurena spongicola sp. n. (Hydrozoa, Corynidae), ein in Schwa¨mmen lebender Hydroidpolyp aus dem Kattegat und der no¨rdlichen Kieler Bucht. Kieler Meeresforschungen, 28, 80–84. Arndt W. (1936) Die Poriferen vom Standpunkt der Strahlungsbiologie. Sitzungsberichte der Gesellschaft Naturforschender Freunde zu Berlin, 315–355. Bavestrello G., Puce S., Cerrano C., Balduzzi A. (2000) Life history of Perarella schneideri (Hydrozoa, Cytaeididae) in the Ligurian Sea. In: Mills C.E., Boero F., Migotto A., Gili J.M. (Eds.), Trends in Hydrozoan Biology – IV. Scientia Marina, 64(Suppl. 1), 141–146. Boero F. (1980) Life cycles of hydroids and hydromedusae: some cases of difficult interpretation. Memorie di Biologia Marina e di Oceanografia, 8(Suppl. X), 141–147.

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