Description and life cycle of the hydrozoan Hydractinia uniformis, sp. nov. (Cnidaria: Hydrozoa: Hydractiniidae), from the coast of southeastern Brazil Stampar, Sérgio N. Tronolone, Valquiria B. Morandini, André C. Zootaxa 2006 2006-05-11 1200 43 59 7P6J4 van Beneden, 1841 van Beneden 1841 [351,737,1796,1822] Hydrozoa Hydractiniidae Hydractinia Animalia Anthoathecata 2 45 Cnidaria genus  ( Figures 1–11)   Type material   Holotypespecimen: MZUSP 932, male medusa, 2.1 mmhigh, 3.5 mmwidth, preserved in 4% formaldehyde solution in sea water in  8 October 2003(from polyp cultures, reared in laboratory for 3.5 months).   Paratypespecimens: MZUSP 934, one male medusa, preserved in 4% formaldehyde solution in sea water in  20 November 2003(from polyp cultures, reared in laboratory for 2 months). — MZUSP 935, five recently released medusae, preserved in 70% ethanol in  5 January 2005(from polyp cultures). — MZUSP 933, two polyps, preserved in 4% formaldehyde solution in sea water in  5 January 2005(from polyp cultures, reared in laboratory), originally collected in  25 July 2002in Parcel da Praia Grande( 23°51.06’S 45°24.77’W);  10 mdepth; São Sebastião Channel, Ilhabela county, São Paulostate, Brazil—  MHNG INVE 37181, one male medusa, preserved in 4% formaldehyde solution in sea water  20 November 2003(from polyp cultures, reared in laboratory for 2 months) and one polyp, preserved in 4% formaldehyde solution in sea water in  5 January 2005(from polyp cultures, reared in laboratory), originally collected in  25 July 2002in Parcel da Praia Grande( 23°51.06’S 45°24.77’W);  10 mdepth; São Sebastião Channel, Ilhabela county, São Paulostate, Brazil. Additional specimens: MZUSP 936, half of a male medusa, preserved in 4% formaldehyde solution in sea water in 20 November 2003(from polyp cultures, reared in laboratory for 2 months).   EtymologyThe specific name  uniformis, derived from the Latin unus(one) and forma(form), refers to the monomorphic polyps.   Diagnosis   Hydractiniaspecies with monomorphic hydranths; tentacles in one whorl, extended much longer than polyp height; stolons flat and plate­like; vegetative frustules produced from hydranth. Gonophores produced on hydranths. Gonophore a free medusa; bell top flat; manubrium cross­shaped in section; with peduncle; mouth with four branched lips, each ending in up to four bulbous nematocyst clusters; marginal tentacles up to 24, each with an adaxial ocellus.   Description Polyps sessile (figs 1 and 2), arising directly from a hydrorhiza consisting of adhering, ramified, flat, plate­like stolons, perisarc thin, without spines. Polyps without notable polymorphism, variable in shape but generally spindle­shaped, 1.30–1.58 mmhigh and 0.14–0.25 mmwide, hypostome prominent, extensible, nipple shaped. Tentacles in one whorl, filiform, 7–9 innumber, in life up to 4 mmlong and thus more than two times as long as body height, width rather uniform. Medusa buds developing on lower 2/3 of hydranth, up to two per hydranth. Vegetative frustules about 100 µmlong given off from hydranth body. Color: white to yellow­brownish. Nematocysts distributed spirally along tentacles: heterotrichous microbasic euryteles ( 5.8–6.8 µmx 2.9–3.9 µm) and desmonemes ( 2.9–3.9 µmx 1.9 µm). Newly­released medusa round with slightly flattened top (figs 3, 4 and 5), 0.44 mmhigh, maximal diameter 0.52 mm, mesoglea thin. Radial canals four; ring canal present. Velar opening ca2/3 of umbrella margin diameter. Four perradial marginal bulbs, each with a short tentacle and an adaxial red ocellus. Manubrium opaque, conical, ca.half the height of subumbrellar cavity, with four perradial simple mouth lips with nematocyst knobs. Gonads not developed. Nematocysts: exumbrella with heterotrichous microbasic euryteles ( 5.8–6.8 µmx 2.9–3.9 µm); mouth lips with microbasic mastigophores ( 7.8–8.8 µmx 2.9–3.9 µm) and desmonemes ( 2.9–3.9 µmx 1.9 µm); tentacles with heterotrichous microbasic euryteles ( 5.8–6.8 µmx 2.9–3.9 µm) and desmonemes ( 3.9 µmx 1.9–2.9 µm). Mature medusa bell­shaped with flattened top (figs 6, 7, 8, and 9), sometimes with slight apical depression, and thus almost cylindrical, bell 0.7–2.1 mmhigh, 0.9–3.5 mmwide, diameter of umbrella margin 1.8 mm. Mesoglea thicker at top of umbrella. Velar opening ca.4/5 of umbrella margin diameter. Four radial canals and ring canal present. Tentacular bulbs up to 24, with four perradial ones slightly larger; each bulb bearing one marginal tentacle and one red adaxial ocellus. Tentacles not very contractile, provided with evenly­distributed nematocysts. Manubrial peduncle about 1/3 of subumbrellar height. Manubrium cruciform in cross­section, length about 1/2 of the subumbrellar cavity; mouth lips four, perradial, folded and branched, each ending in four nematocyst knobs (fig. 10). Gonads consisting of four interradial pads, large, covering nearly whole manubrium, adnate perradially, orange to red in living animals. All observed animals were male. Nematocysts: exumbrella with heterotrichous microbasic euryteles ( 5.8–7.8 µmx 3.9–5.8 µm); mouth lips with microbasic mastigophores ( 7.8–8.8 µmx 1.9–2.9 µm) and desmonemes ( 2.9–3.9 µmx 1.9–2.9 µm); tentacles with heterotrichous microbasic euryteles ( 5.8–6.8 µmx 2.9–4.9 µm) and desmonemes ( 4.9–5.8 µmx 3.9–4.9 µm).  Life cycle The monomorphic polyps of  Hydractinia uniformis, sp. nov., release both frustules (up to 8) (fig. 11) and medusae (up to 2) (fig. 2, 11) at the same time. Frustules attach to the substratum on the first or second day of liberation, and three days after settlement a new polyp arises. Over the two­year period of this study we observed continuous production of medusae and frustules. The polyp tentacles are generally bent down, usually all reaching the same length and always longer than the body. The hydrorhiza grows slowly, never forming a dense stolonal network or a closed mat. Notably, the polyps agglutinate around their column several different materials (sponge spicules, foraminiferan tests, etc.). The frustules bud off from all parts of hydroid column and they do not move far, generally attaching themselves close to the parental polyp.   FIGURE 1–4.Overview of a polyp of  Hydractinia uniformis,  sp. nov.1, showing the hydrorhiza and a medusa bud shortly before release. Scale = 1 mm. 2, showing a medusa bud and the nippleshaped hypostome. Scale = 0.5 mm. 3, side view (confocal microscopy) of a newly released medusa of  Hydractinia uniformis, sp. nov.Scale = 200 µm. 4, oral view using confocal microscopy of a newly released medusa of  Hydractinia uniformis, sp. nov.Scale = 200 µm. Newly released medusae have four marginal tentacles (figs 4 and 5) and four simple mouth arms with nematocyst knobs. After 15 days, medusae have 8 marginal tentacles (fig. 6) and the gonads start to develop. During this time, the number of branches on the mouth lips increase, reaching up to four branches each; from this stage on the mouth arms grow only in size (fig. 10). Forty days after release the medusae have 16 tentacles (fig. 7), and the gonads increase in size; the umbrella apex begins to flatten and the manubrium reaches almost 1/2 of the subumbrellar cavity. In mature medusae (fig. 8), the outline of the adaxial ocellus is not especially clear. During subsequent days, the medusae grow in size and between each pair of tentacles a new one arises, reaching a maximum of 24. We considered the medusae at this stage as adults, because thereafter they do not change in form, tentacle number (24) does not increase(figs 8 and 9), and during the following months they released gametes (sperm) into the water.   FIGURE 5–10.  Hydractinia uniformis, sp. nov.5, side view of a newly released medusa; note the presence of only four tentacles. Scale = 350 µm. 6, side view of a 15­day­old medusa; note the eigh tentacles. Scale = 550 µm. 7, side view of a 40­day­old medusa; note the 16 tentacles. Scale = 950 µm. 8, side view of a mature medusa (~ 65 days old); note the 24 tentacles. Scale = 1.5 mm. 9, oral view of a mature medusa (~ 65 days old); note the 24 tentacles. Scale = 2 mm. 10, side view of the oral lips of a young medusa; note the branches with nematocysts knobs. Scale = 100 µm. Curiously, the medusae swam only in the presence of light and with air bubbling into the water (which provided some current). Without these factors the medusae remained on the bottom and the marginal tentacles were kept contracted. During swimming, food (  Artemianauplii) was held on the umbrella margin and was ingested by contraction of the umbrella and extension of the manubrium and mouth arms.   Discussion The most recent published compilation of the nominal species belonging to the genus  Hydractiniawas presented by Bouillon & Boero (2000). However, the list included only those species with a medusa stage and no diagnosis or synonymy was included. Bouillon et al.(1997)provided a more detailed list (with some systematic comments), but only for members of the genus  Stylactaria. We thus conducted an extensive search in the literature and found about 97 potentially valid nominal species in the genus (see details in Appendix).   FIGURE 11.Schematic side view of a colony of  Hydractinia uniformis, sp. nov.Note: the polyp tentacles are slightly retracted; the polyp on the right side is contracted and has frustules and medusa buds; the polyp on the left side has an older medusa bud. Scale = 500 µm.   Hydractinia uniformis, sp. nov., has some unique features that make it distinct from all other congeners: the extraordinarily long tentacles of the polyp; the unusual plate­like stolons; and the production of frustules from the hydranth body. The medusa has some additional features that are not very common in Hydractiniidae, namely the ocelli and the branched mouth lips. The monomorphic colonies are also unusual among Hydractiniidae, although colonies of  H. sarsiiare likewise monomorphic (see Tab. 1).   TABLE 1.Comparison between the polyp stages of  Hydractinia uniformis, sp. nov., and some other hydractiniids which produce free­swimming medusae, and  Hydractinia sarsiiSteenstrup, 1850which also have monomorphic polyps (mostly after Mayer, 1910; Edwards, 1972; Mills,1976; Hirohito, 1988; Schuchert, 2001).    Polyp character   H. uniformis sp. nov.  H. americana   H. areolata  Frustules yes no no  Gonophores free medusa free medusa free medusa  Gonophores with tentacles no yes yes  Gonophores with marginal bulbs no yes yes  Distinct gonozooid no yes yes  Number of gonophores 1–2 2–10 1–2  Spines (mm) absent 0.2–0.5 up to 0.9  Relative gonozooid/gastrozooid size 1/1 1/2 0.5–0.8  Hypostome shape nipple dome dome  continued.    H. borealis H. carnea   H. hayamaensis   H. minoi   H. sarsii   H. selena  no no no no no no  free medusa free medusa free medusa free medusa sporosacs free medusa  yes yes yes yes no yes  yes yes no no no yes  yes yes yes yes yes yes  2–8 2–10 more than 10 4–7 2–4 2–10  0.2 0.2–0.5 0.5 absent 0.1–1 up to 1.2  1/2 1/2 1/2 1/2–1/4 0.8–1 1/2  dome dome dome dome nipple, capitate dome Of the species of  Hydractiniahaving medusae with more than 8 tentacles (see Tab. 2), the one most resembling  H. uniformis, sp. nov., is  H. ocellata(Agassiz & Mayer, 1902)from South Pacific Ocean. However,  H. ocellatahas vacuolated cells at the base of the stomach (at the insertion of the radial canals) — a trait otherwise typical for the genus  TurritopsisMcCrady, 1857, to which it might perhaps belong (their polyps are unknown so far). Moreover, it possesses up to 50 marginal tentacles. Two other species that also have branched oral lips are  Hydractinia borealis(Mayer, 1900)and  H. polystyla( Haeckel, 1879)(see Haeckel, 1879; Mayer, 1910; Edwards, 1972). However,  H. borealisdoes not have ocelli, while  H. polystylahas more tentacles and differs in the shape and size of the umbrella. The medusa species  Hydractinia dubia(Mayer, 1900), described from the Tortugas, Florida( USA), is probably a young stage of another species. It resembles juveniles of  Hydractinia uniformis, sp. nov., but differs in having black ocelli and swellings on the radial canals ( Mayer, 1910: 141).  TABLE 2.Comparison of species of  Hydractiniawhose adult medusae have more than 8 tentacles (after Haeckel, 1879; Mayer, 1910; Kramp, 1961; Edwards, 1972, Mills, 1976).    Medusa character  H. uniformis sp. nov.   H. americana H. areolata H. borealis  Size of umbrella in adult 0.9–3.5 mm 0.5–3.5 mm 0.72–4 mm 0.7–6.3 mm  Shape of bell top flat to deep globular cone­shaped cone­shaped  Manubrium bulbous­shaped fusiform tubular tubular  Mouth lips 4, branched 4, unbranched 4, unbranched 4, branched  Branches per mouth lips 4 ­ ­ 2–4 or more  Tentacles 8–24 4–32 16–57 18–39  Ocellus present absent absent absent  continued.    H. carnea   H. dubia   H. ocellata   H. polystyla   H. selena  1–3.5 mm 1.5 mm 4 mm 1.5 mm 0.9–1.8 mm  flat rounded flat rounded cone­shaped  flask­shaped pear­shaped tubular cubical tubular  4, unbranched 4, unbranched 4, branched 4, branched 4, unbranched  ­ ­ 4 4 ­  4–8, rarely 16 8 up to 50 32 8–14  absent present present present absent Until now, only two species of  Hydractiniamedusae have been recorded from the entire coast of Brazil:  H. minima(Trinci, 1903)and  H. minuta(Mayer, 1900) ( Migotto et al., 2002). Medusae of  H. uniformis, sp. nov., differ from them in tentacle number and in having an ocellus on each tentacle bulb. Even more notably, we never observed production of medusa buds on the manubrium of  H. uniformis, a typeof asexual reproduction found in the other two species. The two dissimilar ways of producing a dispersive phase — by frustules and by medusae — in  Hydractinia uniformis, sp. nov., represent different dispersal strategies of the species. The free swimming medusae increase genetic variability and the distributional range of the species. Meanwhile, the frustules increase the number of individuals in a small area and can act as resting stages. Many other species of the genus  Hydractiniaare epizoic on other invertebrates, particularly encrusting mollusk shells (of living snails or inhabited by hermit crabs) (e.g., Cerrano et al., 2000; 2001). Polyps of  H. uniformis, sp. nov., were collected on dead coral fragments, which were sometimes buried on the sediment. Based on the available published literature (e.g. Schuchert, 1996; Bouillon & Boero, 2000; Bouillon et al., 2004), several species of  Hydractiniapresent characters which are not listed or differ from the ones that have been incorporated in the diagnosis of the family Hydractiniidae. Among these is the occurrence of monomorphic colonies, observed in certain valid species of the genus (see above). Also, the presence/absence of ocelli is a feature that can be misinterpreted depending on the condition of the observed specimen (e.g., ocelli tend to lose their coloration in badly­preserved or long­preserved specimens). Finally, the family Hydractiniidaeunquestionably needs morphological revision. In particular, the family diagnosis does not include all the variations observed in the genus  Hydractinia. Moreover, complete life cycles are known for few of the species. Finally, when  Podocorynaand  Stylactariaare considered synonymous with  Hydractinia, some secondary homonyms are created (see appendix). 2236573276 2003-10-08 MZUSP 3 46 MZUSP 932 1 holotype 2236573278 2002-07-25 2005-01-05 2002-07-25 MZUSP Brazil Ilhabela county 10 -23.851 Parcel da Praia Grande 12 -45.412834 Sao Sebastiao Channel 3 46 MZUSP 934, MZUSP 935, MZUSP 933 1 Sao Paulo paratype 2236573277 2002-07-25 2005-01-05 2002-07-25 MHNG Brazil Ilhabela county 10 -23.851 Parcel da Praia Grande 12 -45.412834 Sao Sebastiao Channel 3 46 INVE 37181 1 Sao Paulo paratype