Description and life cycle of the hydrozoan Hydractinia uniformis, sp. nov. (Cnidaria: Hydrozoa: Hydractiniidae), from the coast of southeastern Brazil Author Stampar, Sérgio N. Author Tronolone, Valquiria B. Author Morandini, André C. text Zootaxa 2006 2006-05-11 1200 43 59 journal article 27012 10.5281/zenodo.2646450 aade9a88-65f1-48d3-985f-43d4d4ace1a8 1175-5326 2646450 5F60BFC9-371C-456B-A9EB-0394E3112E1D Genus Hydractinia van Beneden, 1841 Hydractinia uniformis sp. nov. ( Figures 1–11 ) Type material Holotype specimen: MZUSP 932 , male medusa, 2.1 mm high, 3.5 mm width, preserved in 4% formaldehyde solution in sea water in 8 October 2003 (from polyp cultures, reared in laboratory for 3.5 months). Paratype specimens: 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 2002 in Parcel da Praia Grande ( 23°51.06’S 45°24.77’W ); 10 m depth; São Sebastião Channel , Ilhabela county , São Paulo state, 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 2002 in Parcel da Praia Grande ( 23°51.06’S 45°24.77’W ); 10 m depth; São Sebastião Channel , Ilhabela county , São Paulo state, 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). Etymology The specific name uniformis , derived from the Latin unus (one) and forma (form), refers to the monomorphic polyps. Diagnosis Hydractinia species 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 mm high and 0.14–0.25 mm wide, hypostome prominent, extensible, nipple shaped. Tentacles in one whorl, filiform, 7–9 in number, in life up to 4 mm long 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 µm long given off from hydranth body. Color: white to yellow­brownish. Nematocysts distributed spirally along tentacles: heterotrichous microbasic euryteles ( 5.8–6.8 µm x 2.9–3.9 µm ) and desmonemes ( 2.9–3.9 µm x 1.9 µm ). Newly­released medusa round with slightly flattened top (figs 3, 4 and 5), 0.44 mm high, maximal diameter 0.52 mm , mesoglea thin. Radial canals four; ring canal present. Velar opening ca 2/3 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 µm x 2.9–3.9 µm ); mouth lips with microbasic mastigophores ( 7.8–8.8 µm x 2.9–3.9 µm ) and desmonemes ( 2.9–3.9 µm x 1.9 µm ); tentacles with heterotrichous microbasic euryteles ( 5.8–6.8 µm x 2.9–3.9 µm ) and desmonemes ( 3.9 µm x 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 mm high, 0.9–3.5 mm wide, 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 µm x 3.9–5.8 µm ); mouth lips with microbasic mastigophores ( 7.8–8.8 µm x 1.9–2.9 µm ) and desmonemes ( 2.9–3.9 µm x 1.9–2.9 µm ); tentacles with heterotrichous microbasic euryteles ( 5.8–6.8 µm x 2.9–4.9 µm ) and desmonemes ( 4.9–5.8 µm x 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 ( Artemia nauplii) 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 Hydractinia was 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. sarsii are 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 sarsii Steenstrup, 1850 which 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 Hydractinia having 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. ocellata has vacuolated cells at the base of the stomach (at the insertion of the radial canals) — a trait otherwise typical for the genus Turritopsis McCrady, 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. borealis does not have ocelli, while H. polystyla has 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 Hydractinia whose 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 Hydractinia medusae 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 type of 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 Hydractinia are 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 Hydractinia present 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 Hydractiniidae unquestionably 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 Podocoryna and Stylactaria are considered synonymous with Hydractinia , some secondary homonyms are created (see appendix).