Hydrocoryne iemanja (Cnidaria),a new species of Hydrozoa with unusualmode of asexual reproduction

andr�e c. morandini1

, s�ergio n. stampar2

, alvaro e. migotto3

and antonio c. marques2

1Grupo de Sistematica e Biologia Evolutiva (GSE), Nucleo em Ecologia e Desenvolvimento Socio-Ambiental de Macae (NUPEM/UFRJ), Universidade Federal do Rio de Janeiro, C.P. 119331, Macae, RJ, 27910-970, Brazil, 2Departamento de Zoologia, Instituto deBiociencias (IB-USP), Universidade de Sao Paulo, R. Matao, trav. 14, 101, Sao Paulo, SP, 05508-900, Brazil, 3Centro de BiologiaMarinha (CEBIMar-USP), Universidade de Sao Paulo, Avenida Manoel H. do Rego km 131,5, Sao Sebastiao, SP, 11600-000, Brazil

Hydrocoryne iemanja sp. nov. was found in an aquarium, growing on rhodoliths of coralline algae collected on the south-eastern coast of Brazil (208400S 40820W). The colonies were reared through maturity in the laboratory. Each colony had up to7 sessile, long and thin monomorphic zooids, very extensible and flexible, arising from a chitinous, hard dark-brown platewith minute spines. Medusae budded from near the basal part of hydrocaulus, and were released in immature condition,acquiring fully developed interradial gonads 5–7 days after release. Asexual reproduction by longitudinal fission was observedon the hydrocaulus of the polyps, both for those in normal condition and those with injuries. Fission started at the oral region,extending aborally, with a new hard plate formed in the basal part of hydrocaulus. When fission reached the new hard plate,the new polyp detached, becoming free and sinking to the bottom, starting a new colony. Detached polyps were morphologi-cally indistinguishable from other polyps, being able to produce medusae. Mother and daughter polyps undertook subsequentfissions. This mode of longitudinal fission is distinct from other modes of longitudinal fission, a process known for a few speciesof cnidarians. Further studies of this process may shed light on the understanding of the evolutionary pathways in Cnidariaand animals. Hydrocoryne iemanja sp. nov. is distinguishable from its two congeners by the distinct marginal tentacles of themedusae—short and with a median nematocyst knob—an unambiguous character useful even for the identification of newlyliberated medusae.

Keywords: Anthoathecata, Hydrocorynidae, medusa, polyp, life cycle, cnidome, fission, Brazil

Submitted 18 January 2008; accepted 4 March 2008

I N T R O D U C T I O N

Hydrozoans are common and widespread invertebrates onshallow water. Yet, as they are mostly represented by specieswith small body dimensions and cryptic life habits, theirstudy is neglected and the knowledge on their biodiversity isfar from satisfactory. In general, accumulated knowledge isgeographically concentrated, with some areas almostunknown. This is particularly true for the Brazilian coast, inwhich just a few localities of its south-eastern region are rela-tively well-known (Migotto et al., 2002; Marques et al., 2003;Migotto & Marques, 2006). New species of hydroids continueto be described every year worldwide, even in relatively well-known regions, with the discovery of inconspicuous speci-mens and re-evaluation of morphological variation.

Amonghydrozoans, thepoorly-known familyHydrocorynidaeRees, 1957 (Cnidaria: Hydrozoa: ‘Anthoathecata’) comprises twovalid genera (Kubota, 1988; Mangin, 1991): HydrocoryneStechow, 1907, and Samuraia Mangin, 1991. The three speciesof the group so far described are restricted to Pacific waters(Kubota, 1988; Mangin, 1991), with only one unidentified

record (Hydrocoryne sp.) for the Atlantic Ocean (Wedler &Larson, 1986).

A hydroid belonging to the family Hydrocorynidae wasnever reported in the southern hemisphere, including theAtlantic Ocean. Species such as Hydrocoryne, which are incon-spicuous and difficult to collect individually by hand, are usuallyfound after examining substrata—larger organisms such as algaeand invertebrates with hard skeletons, and pebbles and biogenicnodules—in the laboratory. Nevertheless, delicate specimensusually get damaged during or after collecting procedures (e.g.manual, trawling, dredging or grabbing techniques) and theirsoft parts may shrink, degrade or be resorbed, making theirremains indistinguishable or simply hard or impossible to see,even under a microscope. However, when pieces of substratasuch as pebbles, broken shells and calcareous nodules are keptin the laboratory under favourable conditions, the shrunkpolyps or the regressed or dormant tissues may become activeor give rise to new polyps. Many species of hydroids weredescribed employing intentionally this technique or just bychance, as was the species described here.

Distinction between species of the genus Hydrocoryne isbased on the medusa stage, thus development and life cycleobservations are essential for identification. In rearing thespecies, we gathered data of not only its sexual phase butalso of an unusual mode of asexual reproduction withinHydrozoa—longitudinal fission.

Corresponding author:A.C. MorandiniEmail: andre.morandini@gmail.com

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Journal of the Marine Biological Association of the United Kingdom, 2009, 89(1), 67–76. #2009 Marine Biological Association of the United Kingdomdoi:10.1017/S0025315408002968 Printed in the United Kingdom

Asexual reproduction is a poorly known reproductive trait inseveral cnidarian groups. Although hydrozoans present a widevariety of asexual processes, fission seems restricted to a fewspecies, and may be considered a rare phenomenon within theHydrozoa (Shostak, 1993). Longitudinal fission, in particular,is reported for a few hydromedusae (e.g. Stretch & King, 1980)and hydropolyps (Shostak, 1993; Bouillon et al., 2004).

The uniqueness of the process of longitudinal fissionamong the hydrozoans highlights the importance of the newfinding, which may shed light on the understanding of theevolutionary pathways in Cnidaria and animals. Therefore,the goal of this study is to describe a new species ofHydrocorynidae, from the tropical waters of the south-easternBrazilian coast, and its unusual mode of asexual reproduction.

M A T E R I A L S A N D M E T H O D S

The hydroids were found growing on rhodoliths of corallinealgae (called ‘living stones or rocks’ by Brazilian aquarists)in an aquarium in August 2005. Rhodoliths were collectedfrom the Guarapari county region (208400S 0408290W), stateof Espırito Santo, Brazil (Figure 1). Certainty concerning theoriginal location of the species was possible because theaquarium contained only artificial seawater and recently col-lected rhodoliths from the same place. Two colonies were iso-lated from the substratum and transferred to a small glassaquarium (500 ml) with constant air bubbling.

The hydroids were reared in the laboratory at theDepartamento de Zoologia of the Universidade de Sao Paulo.The colonies were kept in natural seawater from the SaoSebastiao Channel. The aquariumwas kept under a natural day-light regime at room temperature (20–258C). The seawater ofthe cultures was changed every week and the polyps were fedevery other day with Artemia nauplii (method adapted fromJarms et al., 2002).

After the medusae were released from the polyp, they werekept in glass Erlenmeyer flasks of different sizes (250 and500 ml) with gentle air bubbling to provide water current (see

a fuller description of the method in Stampar et al., 2006).Seawater was changed three times per week, and Artemianauplii and gonad macerate of the clam Perna perna(Linnaeus, 1767) were offered daily as food. The medusae werealso kept under natural light and room temperature at 20–258C.

Morphological, morphometric, and cnidome studies wererecorded from fresh and preserved material. Measurementswere carried out under a dissection microscope. Preserved andfresh materials were used in squash preparations, with distilledwater and saliva, for cnidome observations under interference-contrast light microscopy (cf. Migotto, 1996). The terminologyfor the cnidome is that ofWeill (1930, 1934) andMariscal (1974).

Type material was deposited in the cnidarian collection ofthe Museu de Zoologia da Universidade de Sao Paulo(MZUSP).

R E S U L T S

SYSTEMATICSClass HYDROZOA Huxley, 1856

Subclass ANTHOATHECATA Cornelius, 1992Order CAPITATA Kuhn, 1913

Family HYDROCORYNIDAE Rees, 1957Hydrocorynidae Rees, 1957: 525; Petersen, 1990: 134–135;

Bouillon & Boero, 2000: 124.

A M E N D E D D E S C R I P T I O N

Colonies unbranched, hydranths monomorphic spindle-shaped not well demarcated from hydrocaulus, oral tentaclescapitate, long, hollow, in 5–6 close sets of whorls aroundconical hypostome, hydrocaulus long, highly extensible,naked, with thickened mesolamella issuing from hard hydro-rhizal stolonal plate; medusa buds in clusters on basal part ofhydrocaulus. Medusae bell-shaped; with or without gastricpeduncle; four marginal tentacles with scattered cnidae andmedian knob; clasping tentacular bulbs with ocelli; manu-brium broadly flask-shaped or tubular, quadrate or cruciformin cross-section; mouth cruciform, with or without cnidocystclusters; gonads interradial without longitudinal groove,almost totally surrounding manubrium.

R E M A R K S

In a review of the capitate hydroids, Petersen (1990) establishedthe suborder Sphaerocorynida including two superfamilies,Sphaerocorynoidea (with three families: Paragotoeidae Ralph,1959, Sphaerocorynidae Prevot, 1959 and Zancleopsidae,Bouillon, 1978) and Hydrocorynoidea (encompassing exclu-sively the family Hydrocorynidae). The genus ParagotoeaKramp, 1942 is considered presently among theCorymorphidae Allman, 1872 (cf. Bouillon et al., 2004).

The family Hydrocorynidae was proposed by Rees (1957) toaccommodate the Japanese hydroid Hydrocoryne miurensisStechow, 1907. Polyps of this species are notable for theirlength when fully expanded, reaching up to 6 cm long or more(Rees et al., 1976). Nevertheless, the polyps have quite simplemorphologies, and the systematics of the genus is based ondifferences of the medusae stage (cf. Kramp, 1961). The family

Fig. 1. Map of Brazil, showing the type locality (Guarapari) of Hydrocoryneiemanja sp. nov.

68 andr �e c. morandini et al.

comprises only two genera (Hydrocoryne Stechow, 1907 andSamuraiaMangin, 1991) and three species have been describedso far (Hydrocoryne bodegensis Rees, Hand & Mills, 1976;Hydrocoryne miurensis and Samuraia tabularasa Mangin,1991) (see Rees et al., 1976; Mangin, 1991). In addition,Hydrocoryne sp., possibly representing a new species, is referredto Puerto Rico by Wedler & Larson (1986: 79) and Panama byCalder & Kirkendale (2005: 481). The genera are differentiatedby the production and release of medusae (as in Hydrocoryne)or eumedusoids that are either retained or not on the polyps (asin Samuraia) (Kubota, 1988; Mangin, 1991).

Genus Hydrocoryne Stechow, 1907Hydrocoryne iemanja sp. nov.

(Figures 2–7)

T Y P E M A T E R I A L

Holotype: female medusa from polyp culture, 0.9 mm high,0.7 mm wide, preserved in 4% formaldehyde solution in sea-water (Guarapari, state of Espırito Santo, Brazil, 208400S0408290W), reared in the laboratory for 7 days, 12 September2005 [MZUSP 1972].

Paratypes: one 7-day-old male medusa, preserved in 4%formaldehyde solution in seawater (same locality as holotype),12 September 2005 [MZUSP 1973]; five recently releasedmedusae, preserved in 70% ethanol (same locality as holo-type), 5 September 2005 [MZUSP 1974]; two polyps rearedin the laboratory, preserved in 4% formaldehyde solution inseawater, 5 January 2005 [MZUSP 1975].

E T Y M O L O G Y

The specific name iemanja is derived from the name of thequeen of the waters and seas (Iemanja in Portuguese) of theAfrican–Brazilian religions, derived from the Yorubalanguage expression Yeye o

˙mo˙e˙ja (‘mother which sons are

little fishes’). Iemanja is the daughter of the God or Goddessof the Sea (Olookun), and also the name attributed by theYoruba ethnic nation in Nigeria of a river (Yemo

˙ja) (Verger,

1981; Walker, 1990).

D I A G N O S I S

Hydrocoryne species with hydrorhiza embedded in chitinousdark-brown hard-plate with minute spines; asexual repro-duction by longitudinal fission, and hydrorhizal platearising from column. Tentacle of medusa filiform, exceptfor a large, adaxial nematocyst cluster on its middle(Figure 2).

D E S C R I P T I O N

Colonies with up to 7 sessile polyps (usually 2–3) (Figure 3A),arising from hydrorhiza embedded in chitinous hard dark-brown plate up to 2.5 cm in diameter, with minute spines(Figure 3A). Living polyps 7.0–8.5 cm high, 1–2 mm wide,whitish (or slightly orange tinted because of Artemia diet),

monomorphic, variable in shape, generally elongate, spindle-shaped; hypostome prominent, nipple-shaped when relaxed,proboscis-like when extended, up to 2 mm high. Capitate tenta-cles (Figure 3B–D) up to 20 in number, 0.2–0.4 mm long, in4–5 closely arranged whorls at suboral region; capitulum0.08–0.12 mm in diameter. Stalked medusa buds on lateralbranches, closely and alternately arranged at basal third of hydro-caulus; up to 9 lateral branches per hydranth and up to 7medusabuds on each branch (Figure 3F). Asexual reproduction by longi-tudinal fission and production of a chitinous hard plate at basal1/3 of parental hydrocaulus; fission process starts from oral endtowards new hard plate; polyp becomes free and starts a newcolony (Figures 3C–E & 5A–D). Nematocysts (Figure 7A–J):tentacles—heterotrichous microbasic euryteles with inclusion13.7–14.7� 4.9–5.8 mm (N¼ 10, mean ¼ 14.4 � 5.19 mm,SD+ 0.47 � 0.47 mm), and stenoteles 14.7–16.6 � 9.8–10.7 mm (N¼ 10, mean ¼ 15.4 � 9.9 mm, SD+ 0.9�0.41 mm); column—heterotrichous microbasic euryteles 10.7–12.7 � 4.9–6.8 mm (N ¼ 10, mean¼ 11.5 � 5.9 mm,SD+ 0.77 � 0.55 mm), smaller stenoteles 11.7–14.7�5.8–8.8 mm (N ¼ 10, mean ¼ 12.9 � 7.4 mm, SD+ 1.2�1.0 mm), and larger stenoteles 17.6–19.6 � 11.7–13.7 mm(N ¼ 5, mean ¼ 18.6 � 13.1 mm, SD+ 0.98 � 0.87 mm).

Newly-released medusa is released in immature condition,transparent, slightly flattened on top, higher than wide(0.57 mm high; 0.51 mm in diameter) (Figure 4A–B).Mesoglea thin, without apical process and apical canal.Exumbrella with scattered nematocyst clusters; 3–4 nematocystsper cluster. Radial canals four, simple and straight; circular canalnarrow. Velum narrow; velar opening�1/3 of total diameter atmargin (0.32 mm). Four perradial marginal bulbs, each with ashort tentacle (0.16 mm long, 0.032 mm wide) and a largeabaxial red ocellus (Figure 4A–B&F). Tentacles hollow, filiform,except for a large, adaxial nematocyst cluster on its middle.Manubrium quadratic, 0.24 mm high, with simple mouth;peduncle lacking. Gonad rudiments not visible on release.Nematocysts (Figure 7K–T): tentacles—smaller stenoteles6.8–9.8� 4.9–5.8 mm (N¼ 10, mean ¼ 8.2 � 4.9 mm,SD+ 0.82 � 0.3 mm) with shaft length 9.8 mm, spineslength 4.9 mm, and larger stenoteles 12.7–15.6� 8.8–10.7 mm(N ¼ 10, mean ¼ 14.5 � 9.9 mm, SD+ 0.77 � 0.61 mm)

Fig. 2. Hydrocoryne iemanja sp. nov. (A) Basal half of a medusa with tentacles;(B) detail of the tentacle knob and contracted tentacle, note that in the tentaclethere are nematocysts only in the knob.

hydrocoryne iemanja sp. nov., a new hydroid with longitudinal fission 69

with shaft length 11.7 mm, spines length 5.8 mm; tentacularbulbs—microbasic mastigophores 9.8–10.7 � 8.8–9.8 mm(N ¼ 10, mean ¼ 10.3� 9.2 mm, SD+ 0.5� 0.5 mm) anddesmonemes 6.8–7.8 � 3.9–5.8 (N ¼ 10, mean ¼ 7.4 �4.9 mm, SD+ 0.5 � 0.46 mm); exumbrella–holotrichousisorhizae in scattered pads with 2–6 nematocysts 7.8–9.8 �4.9 mm (N¼ 10, mean ¼ 8.4 � 4.9 mm, SD+ 0.68� 0 mm).

Mature medusa bell-shaped (Figure 4C–D); bell 1.2–1.4 mmhigh, 0.9–1.1 mm in diameter at median part; umbrellar margindiameter up to 1.2 mm. Velum large; velar opening�1/5 of totalaboral diameter. Four radial canals, ring canal present. Four per-radial tentacular bulbs with one marginal tentacle and one redadaxial ocellus each (Figure 4C–D). Tentacles short, contractile,with a large, adaxial nematocyst knob at middle of tentacle.Manubrium tubular, about 1/2–4/5 of subumbrellar height,without concentrations of nematocysts on lips. Males withshorter manubrium than females (Figure 4C–D). Gonads inter-radial, covering nearly whole manubrium, light orange to deeporange in male specimens and deep orange to red in female

living specimens (Figure 4C–D & E). Eggs (0.05–0.06 mm)visible by transparence through thin manubrial epithelium(Figure 4D–E). Nematocysts (Figure 7K–R): tentacularbulbs—microbasic mastigophores 12.7–15.6� 9.8–11.7 mm(N¼ 10, mean¼ 13.5� 10.9 mm, SD+ 1 � 0.77 mm); tenta-cles—smaller stenoteles 8.8–10.7� 5.8–6.8 mm (N¼ 10,mean¼ 9.9 � 6 mm, SD+ 0.61� 0.41 mm) and larger steno-teles 13.7–15.6� 9.8–12.7 mm (N¼ 10, mean¼ 15� 11 mm,SD+ 0.68 � 0.8 mm). Exumbrella without nematocysts.

L I F E C Y C L E A N D B I O L O G I C A L D A T A

The long and thin polyps of Hydrocoryne iemanja sp. nov.are very extensible and flexible. They preferably stayupwards, moving back and forth, when subjected to strongwater circulation in the aquarium; not being able to main-tain an erect position, they lay on the bottom in quietwater. Polyps that stayed longer periods laid on the

Fig. 3. Hydrocoryne iemanja, sp. nov. (A) Polyp colony base with hard plate and five zooids partly laid on the bottom; (B) detail of a zooid with gonophores at thebasal region of hydrocaulus; (C–D) zooid undergoing longitudinal fission; (E) hard plate formation at middle of hydrocaulus; (F) reproductive branch arising fromthe hydrocaulus, with stalked medusae in different stages of development.

70 andr �e c. morandini et al.

bottom had fewer and less developed tentacles. Polyps thatwere overgrown by filamentous algae reduced the numberand length of their tentacles, and their basal chitinous hard-plate started to produce new hydranths, functioning as astolon-like structure.

Asexual reproduction by longitudinal fission was com-monly observed (Figures 3E & 5). Although this processoccurred in normal condition polyps, it was also initiatedwhen the polyp remained lying on the bottom for extendedperiods or presented some kind of injury in their column.

Fission started at the oral region (Figures 3C & 5A), extend-ing aborally (Figures 3D& 5B, C). The hypostome expanded lat-erally and the division proceeded along the oral–aboral axis ofthe polyp, resulting in a polyp with two oral ends well-defined,each with a hypostome and a half crown of tentacles, whichgradually formed new tentacles, completely encircling thehypostome. At this point, the dividing polyp looked like a Y,both oral ends being able to catch food independently; their indi-vidual gastrodermal cavity merged at the point of fission, and

food passed to the common cavity from either end, as couldbe clearly seen by transparence. Meanwhile, a new hard plateof epidermal origin and involving soft tissues gradually appearedin themiddle of hydrocaulus, being globular (0.25–0.3 mm) andflexible when well developed (Figures 3E & 5C). When thefission process reached the new hard plate—which keeps itsglobular shape or becomes dish-like in recumbent polyps—thehydrocaulus separated from each other and the new hard plategradually detached from the other hydrocaulus. Subsequently,one of the polyps detached from the other, becoming free andsinking to the bottom, where its hard plate attached, forming anew colony (Figure 5D). The whole fission process took about48 hours. After detachment, the original polyp remained aliveand functional, without scars on its hydrocaulus. Soon afterrelease, the new polypwas about half the length of the remainingone, beingmorphologically indistinguishable fromother polyps;it was able to bud off medusae and soon attained the size of fullydeveloped polyps.Mother and daughter polypsmight undertakesubsequent fissions.

The species is metagenetic (Figure 6). Polyps releasedmedusae during the period of cultivation (from August 2005to September 2007); the medusae were easily reared throughmaturity. Since the first visual indication of the formation ofthe gonophores, it took about 24 hours for the medusae tostart to be released; polyps released medusae for about a week.Medusae production was triggered by intense feeding ofpolyps. Newly-liberated and mature medusae exhibited positivephototaxis, swimming more intensely during light hours.Medusae became mature, with fully developed gonads(Figure 4C–D), 5–7 days after release. Eight to fourteen daysafter release, the medusae shed their gametes on the watercolumn (at night), where fertilization occurred. Some planulaeattached to the bottomof the culture dishes, but further develop-ment was not obtained. Medusae degenerated after spawning.

D I S C U S S I O N

Species of the genus Hydrocoryne were recorded only in fourlocations hitherto: Japan, California (USA) and Russia (Peterthe Great Bay, Japan Sea) (Margulis & Karlsen, 1980;Hirohito, 1988; Kubota, 1988), all in the North PacificOcean, and in the Caribbean (Wedler & Larson, 1986; Calder& Kirkendale, 2005). Kubota (1988) suggested that the validityof the species H. bodegensis and H. miurensis is doubtful,because both are sympatric or partially sympatric (see alsoStepanjants, 1994). The Caribbean Hydrocoryne sp. is onlyknown from its polyp stage and newly-released medusae(Wedler & Larson, 1986). Although Wedler & Larson’s(1986) brief description does not mention tentacle features ofthe newly-released medusa, we believe that the tentacles ofthe Caribbean Hydrocoryne sp. is distinct from Hydrocoryneiemanja sp. nov. based on the unique nematocyst knob,which could hardly pass unnoticed. We therefore concludethat Hydrocoryne sp. from the Caribbean is not conspecificwith H. iemanja sp. nov., being possibly a distinct andundescribed species, as supposed by Calder & Kirkendale(2005).

Hydrocoryne iemanja sp. nov. represents the first record ofthe familyHydrocorynidae for the SouthAtlantic. Its knowndis-tributional range is restricted to the type locality on the south-eastern coast of Brazil. The knowledge on the hydrozoanfauna of the Brazilian coast is heterogeneous, the south-eastern

Fig. 4. Hydrocoryne iemanja, sp. nov. (A) Newly released medusa; (B) newlyreleased medusa just after feeding with Artemia; (C) mature male medusa(7 days old); (D) mature female medusa (7 days old), showing eggs on thesides of the manubrium; (E) detail of the manubrium of a female medusa,showing eggs; (F) detail of the umbrellar margin of a newly releasedmedusa, showing a tentacle bulb with nematocysts and an ocellus.

hydrocoryne iemanja sp. nov., a new hydroid with longitudinal fission 71

region being the best-known (Migotto et al., 2002; Marqueset al., 2003; Migotto & Marques, 2006). This region includesthe states of Sao Paulo, Rio de Janeiro, and Espırito Santo, thelast one by far with the less known fauna among the three

(cf. Marques & Lamas, 2006). Specifically concerning hydroids,72 species were recorded so far for the state, 21 anthoathecatesand 51 leptothecates (Migotto et al., 2002; Grohmann et al.,2003; Marques et al., 2003).

Fig. 5. Asexual reproduction of polyp of Hydrocoryne iemanja, sp. nov. Diagram showing the sequence of a zooid undergoing longitudinal fission from its oral tip(A), branching (B), forming a hard plate at the basal part of hydrocaulus (C), and the new, asexually produced zooid (D).

Fig. 6. Hydrocoryne iemanja, sp. nov. Diagram showing the sequence of stages in the life cycle of the species: polyp; polyp with budding medusae arising fromhydrocaulus; young medusa; mature male and female medusae; and planula larva. Drawings are not to scale.

72 andr �e c. morandini et al.

The differences among the previously described species ofHydrocoryne are well defined, although polyps and youngmedusae ofH. bodegensis andH. miurensis are morphologicallyindistinguishable from each other (see Kubota, 1988). Indeed,polyps of Hydrocoryne iemanja sp. nov. have fewer tentaclesthan the two other species of the genus, but we believe that pre-sently, before variation may be better known, polypoid charac-ters are not conclusive to distinguish among the congeners. Aswith the two other species of Hydrocoryne, the diagnostic fea-tures are present in the medusa phase. Hydrocoryne iemanjasp. nov. may be clearly set aside from the two other species bythe distinct marginal tentacles of the medusae—short, with alarge adaxial nematocyst cluster—an unambiguous characteruseful even for the identification of newly liberated medusae

(Figure 2). Hydrocoryne iemanja sp. nov. also lacks nematocystclusters on the manubrial lips of mature medusae, and itscnidome is distinct, lacking desmonemes only on the hydroidphase.

The presence of desmonemes in the medusae and absencein the polyp have been used to include the familyHydrocorynidae in the Corynoidea, though Petersen (1990:134–135) considered Hydrocorynidae assigned to theSphaerocorynida because of the quadrate manubrium andinterradial gonads in the medusae, and the absence of awhorl of oral tentacles in the hydroids.

We tentatively considered the longitudinal reproduction asa diagnostic character of Hydrocoryne iemanja sp. nov.However, the asexual process of longitudinal fission and

Fig. 7. Hydrocoryne iemanja, sp. nov. Cnidome (A–D polyp tentacle; E–J polyp hydrocaulus; O–P young medusa; K–N and Q–R mature medusa). (A–B)Undischarged and discharged heterotrichous microbasic euryteles with inclusion; (C–D) undischarged and discharged stenoteles; (E–F) undischarged anddischarged heterotrichous microbasic euryteles; (G–H) undischarged and discharged small stenoteles; (I–J) undischarged discharged large stenoteles; (K–L)undischarged and discharged small stenoteles; (M–N) undischarged discharged large stenoteles; (O–P) undischarged and discharged holotrichous isorhizae(from exumbrella of recently released medusae); (Q–R) undischarged and discharged microbasic mastigophores; (S–T) undischarged and dischargeddesmonemes. Scale bar ¼ 15 mm.

hydrocoryne iemanja sp. nov., a new hydroid with longitudinal fission 73

production of the hard plate on the column may exist in otherspecies of Hydrocoryne. From laboratory cultures, Kubota(1988: 4) found a polyp of Hydrocoryne miurensis ‘bifurcatedat the lowest portion of hydrocaulus’, but he neither recordeda new hard plate nor that the bifurcation apparently had givenrise to a new, independent polyp.

The asexual reproduction observed for Hydrocoryneiemanja sp. nov. suggests that its hydroid generation may dis-perse and successfully colonize new and favourable habitats.However, once the hard plate of the new free-living polyp gen-erated by asexual reproduction is negative buoyant, it tends tosink fast and, therefore, its dispersal is probably limited to thesurroundings of the mother colony. The chances of survival ofthe new colony are probably high, because the propagulesderived by longitudinal fission are large and provided withnematocysts, which probably makes them less vulnerable topredation than the sexually produced ones (planulae). Also,the new large polyp is capable to feed just after settlement,enhancing the chance to establish a new colony. Furthermore,keeping settlement near the parental colony increases thechance of the new hydroid to stay within the ecological toler-ance limits of the species.

Besides the possible occurrence of longitudinal fission in otherspecies ofHydrocoryne, the universality of this reproductive typeis restricted in other cnidarians. In general, some kind of longi-tudinal fission occurs in polyps of a few species of Scyphozoa(e.g. Aurelia aurita and Catostylus mosaicus; Perez, 1920; Pitt,2000), in which the fission begins at base and runs to the oraldisc. This kind of reproduction also represents a commonmode of vegetative proliferation among certain Anthozoa

(Actiniaria, Scleractinia, Corallimorpharia and Zoanthidae)(Cairns, 1988; Ryland, 1997; Fautin, 2002; Geller et al., 2005),in which the fission also proceeds from the base towards theoral disc (Geller et al., 2005). A detailed analysis on these pro-cesses, however, indicates that they are not homologous, evenin less inclusive groups (cf. Daly et al., 2003). The uniquenessof the process among the hydrozoans highlights the importanceof the new finding.

The Hydrozoa has a vast repertoire of asexual processes,which usually includes budding (almost universal and plesio-morphic for the species of the group), and the formation ofdifferent types of propagules (podocysts, frustules), morerestricted to some specific groups. Fission seems to be rarein Hydrozoa, being only reported in a few species (Table 1).

Fissiparity (either longitudinal or transversal) is an interestingcharacter to be investigated concerning its phylogenetic signifi-cance. Presently, a simple optimization of fissiparity on hydro-zoan phylogenies is impossible, because of the lack ofconsistent and broad phylogenetic frameworks for the hydrozo-ans as awhole.However, some interesting taxonomic significancein the group may be depicted. Longitudinal fission is taxonomi-cally scattered among Hydrozoa and, most probably, aroseseveral independent times in its evolutionary history, while trans-verse fission is characteristic of somewhat taxonomically (thoughstill considering classical taxonomy) related groups (Table 1).

The existence of transverse fission seems to be restricted to theCapitata, although this is probably not a monophyletic group(cf. Collins et al., 2005, 2006).Many groups presenting transversefission belong to theAplanulata (a group supported bymitochon-drial 16S and 28S rDNA analyses, and consisting of a putative

Table 1. Compilation of hydrozoan species where fission is already known, and taxonomic arrangements including these species.

Species Transversal fission Longitudinal fission Classification (Petersen, 1990)(only for Capitata)

Classification(Bouillon, 1994)

Hydrocoryneiemanja

– this work SphaearocorynidaHydrocorynoideaHydrocorynidae

CorynoideaHydrocorynidae

Polypodiumhydriforme

Bouillon (1985) Bouillon (1985) Not included in the Capitata NarcomedusaePolypodiidae

Hydractiniapruvoti

Bavestrello et al. (2000a) Not included in the Capitata FiliferaHydractiniidae

Unindentified Bavestrello et al. (2000b) Not included in the Capitata FiliferaBougainvilloidea

Staurocladia spp. Hirano et al. (2000) Corynoidea Cladonematidae TubulariidaCladonematidae

Hydra spp. Hyman (1928) Parke (1900) MoerisiidaMoerisioidea Hydridae

MoerisioideaHydridae

Moerisia lyonsi Ritchie (1915) – MoerisiidaMoerisioidea Moerisiidae

MoerisioideaMoerisiidae

Acauloides ilonae Brinckmann-Voss (1967) Brinckmann-Voss (1967) TubulariidaCorymorphoidea Acaulidae

AcauloideaAcaulidae

Boreohydrasimplex

Leloup (1952) – TubulariidaCorymorphoidea Acaulidae

TubularioideaBoreohydridae

Ectopleura larynx Tardent (1963) – Tubulariida TubularioideaTubulariidae

TubularioideaTubulariidae

Euphysa sp. Brinckmann-Voss (1967) – Tubulariida CorymorphoideaCorymorphidae

TubularioideaEuphysidae

Protohydraleuckarti

Leloup (1952) – Not included in the study MoerisioideaProtohydridae

Psammohydranana

Schulz (1950) – Not included in the study TubularioideaBoreohydridae

Zelouniesestrambordi

Gravier-Bonnet (1992) – Not included in the study Not included in the study

74 andr �e c. morandini et al.

clade unitingHydridaewithCandelabridae, Corymorphidae, andTubulariidae; Collins et al., 2005, 2006). However, as noticed byCollins et al. (2006: 111), to confirm the monophyly ofAplanulata and understand the relationship among their families,many taxa have yet to be sampled, for instance Acaulidae,Margelopsidae, Paracorynidae and Tricyclusidae.

Compilatory literature studies overlooked the process oflongitudinal fission (e.g. Boero et al., 2002), although it hasalready been described. In Hydrozoa, the most similar phenom-enon occurs in the model organism genus Hydra (Parke, 1900;Hyman, 1928). However, longitudinal fission is not an ordinarytype of asexual reproduction inHydra, and apparently occurs indamaged, regenerating, or abnormal specimens (Hyman, 1928;Shostak, 1993). The sequence of the process is the same as wefound inHydrocoryne iemanja sp. nov., beginning at the hypos-tome, and requiring several days to reach the basal disc.

Polypodium hydriforme Ussow, 1887 is a specialized para-sitic species of sturgeon ova (Raikova, 1994) and, besides itsodd morphology and life cycle, has been considered bysome authors as a Hydrozoa (e.g. Smothers et al., 1994),though some others have proposed a new class to accommo-date the species (Raikova, 1988). The free-living, creeping,non-sexual stage of this species multiplies by longitudinalfission, but this fission begins at the aboral pole and progressestowards mouth (Raikova, 2002).

Cnidarians are a key early diverging lineage among metazo-ans and, therefore, phenomena observed in the group may beprecursors to derived key characteristics in evolution ofanimals, including traits of reproduction and body plans (e.g.Galliot & Schmid, 2002). The data shown above indicatesthat the longitudinal fission in Hydrocoryne iemanja sp. nov.is a process distinct from the longitudinal fission exhibitedby other cnidarians. Therefore, the importance in the under-standing of this asexual process may be in the investigationof regulatory genes in lower metazoans and their significancein the production of clonal organisms and evolutionary trends.

The asexual reproduction is also a divergent point tounderstand the evolution of polarity processes withinCnidaria (for more detailed accounts see Geller et al., 2005;Collins et al., 2006). The hypothesis of a new method of repro-duction, the longitudinal fission in the Hydrocoryne iemanjasp. nov., may shed light on the understanding of the evol-utionary pathways in Cnidaria and animals.

A C K N O W L E D G E M E N T S

We thank F.L. da Silveira (IBUSP) for providing laboratoryfacilities and commenting on the manuscript; RicardoMiyazaki and Augusto A. Tinfre (Agua e Estilo) for providingaquarium facilities; and H.M. Pacca for the line-art drawings.A.C. Morandini was supported by a FAPESP (2003/02433-0)postdoctoral scholarship, CEPG/UFRJ–FUJB (ALV

0

200613126-1), CNPq (481399/2007-0) and FAPERJ (E-26/171.150/2006); S.N.S. was supported by CAPES MSc scholar-ship from ‘Programa de Pos-Graduacao em CienciasBiologicas, Area Zoologia, IBUSP’; A.E.M. is supported byCNPq (300194/1994-3) and FAPESP (2006/05821-9);A.C. Marquer has financial support from CNPq (55.7333/2005-9, 490348/2006-8, 305735/2006-3), FAPESP (2003/02432-3; 2004/09961-4) and NSF (AToL-EF-0531779). Theexperiments herein performed (cultivation) comply with thecurrent laws of Brazil.

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Correspondence should be addressed to:Andre C. MorandiniDepartamento de ZoologiaInstituto de Biociencias (IB-USP)Universidade de Sao PauloRua do Matao, trav. 14, n. 101Sao Paulo, SP, 05508-900Brazilemail: andre.morandini@gmail.com

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