Dentitheca dendritica ( Nutting, 1900 )

Galea, Horia R., Ferry, Romain & Bertot, Jean-Marie, 2012, Medusoids in the life cycle of Dentitheca dendritica (Nutting, 1900) and Nemalecium gracile sp. nov. (Cnidaria: Hydrozoa), Zootaxa 3527, pp. 43-54 : 44-47

Dentitheca dendritica ( Nutting, 1900)

( Figs 1 , 2A–G)

Dentitheca dendritica — Galea, 2010: 28 , figs 1F, G; 7A–G (synonymy).

Plumularia habereri — Wedler, 2004: 89, fig. 2 [not Dentitheca habereri (Stechow, 1909) ].

Material examined. Martinique, La Charmeuse, lat. 14.794190, long. -61.221464, 0 8 February 2012, 8– 13 m, sample M162: numerous fragments up to 15 cm high from large (30–60 cm high), fully fertile male (MHNG- INVE-82192) and female (MHNG-INVE-82193) colonies; 13 February 2012, 8– 10 m, sample M189: a few fragments up to 8 cm high bearing rare female gonothecae.

Description. For a detailed description of the trophosome, see Galea (2010). Individual colonies are dioecious. Gonothecae are mainly borne in two parallel rows on either sides of stem and branches ( Fig. 1 B), or are carried on by the cladia. In the first case, internode apophyses bear two axillar, bithalamic nematothecae (one anterior, the other posterior), and a mamelon ending in a cone-shaped nematotheca [see Fig. 7C in Galea (2010)], the latter giving off a gonotheca (Fig. 2A). On hydrocladia, gonothecae replace either the mesial (Fig. 2D) or one of the lateral nematothecae (Fig. 2B, C), occasionally the pair.

Gonothecae are nearly similar in both sexes, pear shaped to conical, though female are more often irregular, as the mass of eggs tends to distort the lateral walls of the theca (for variation in shape and size, see Fig. 2G). Male gonothecae are comparatively smaller than female (385–520 vs. 560–790 µm long, 280–335 vs. 280–405 µm wide), and nearly radially symmetrical (Fig. 2E, F). Basal part of the theca narrows gradually and has no definite pedicel; the distal end is flattened and provided with a watch glass shaped operculum (diameter 220–280 µm in male, 190–280 µm in female). The perisarc is thickened near the insertion point of the gonotheca, thin and transparent elsewhere.

There is a single gonophore per gonotheca ( Fig. 1 C–F). Its development from young to adult has not been observed, the collected material comprising nearly or fully mature gonophores ready to spend their gametes. Each gonophore is budded off from a blastostyle ending in an apical plate (the latter almost residual to totally absent in ripe gonophores, Fig. 1 G, H), and both are enveloped by an ectodermic mantle.

The gonophore is a rounded-ovoid cryptomedusoid, with thin mesoglea, and a slightly eccentric, cylindrical spadix, nearly as long as the subumbrella ( Fig. 1 E, F), and surrounded by a densely packed mass of gametes, filling the whole subumbrellar cavity. There is a ring of nearly spherical (20–30 µm wide), solid, refringent bodies around the bell aperture ( Fig. 1 G, H). In the absence of histological sections, it is impossible to state whether a velum is either present, though reduced, or totally absent. Radial and circular canals, tentacles, mouth, and sense organs are absent. The gonophores are also devoid of nematocysts, neither on the exumbrella nor the spadix. Oocytes, up to 20 per gonophore, are large (75–150 µm wide), polygonal, with conspicuous nuclei, pink in life ( Fig. 1 C, D). Male gonophores are milky-white ( Fig. 1 E, F).

Spawning occurred within the gonotheca ( Fig. 1 I), since most medusoids remained attached to the blastostyle ( Fig. 1 K–M), or eventually detached from it after this process took place. Though not thoroughly documented, the release of oocytes occurred rapidly and synchronously without involving apparent contractions of the bell, most probably through the rupture of the ectoderm. Released oocytes changed in shape from polygonal to spherical (110–150 µm in diameter) and became more opaque, with indiscernible nuclei. Gonothecal operculum opened wide outwardly or, most often, inwardly, and occasionally was shed, allowing in either case the eggs to be partly or totally liberated from the theca.

Since male and female colony fragments were collected together (sexes could not be ascertained in situ), fertilization occurred even within the female gonotheca, and embryonic development proceeded up to the morula or blastula stages ( Fig. 1 J). Spent medusoids became very reduced and nearly spherical (270–290 µm wide), and degenerated rapidly. No myoepithelial cells could be observed in the subumbrella of emptied gonophores.

Discussion. Fertile specimens of D. dendritica were obtained for the first time by Wedler (2004, misidentified as D. habereri , a species known to occur in the Indo-Pacific) in an original experiment aiming to induce the formation of gonophores in hydroids by transplanting whole colonies from their normal habitat to a new, more stressful environment.

The gonothecae were observed so far in nature only twice in Martinique, in October 2010 and February 2012. The second observation showed that they appear and disappear in a short interval: fully fertile colonies were found nearly devoid of gonothecae five days later upon their reinspection, thus confirming the conclusions drawn earlier by Wedler. This possibly explains why D. dendritica was never reported until now in the literature in a fertile state from the field since its original description by Nutting (1900).

FIGURE 2. A–G: Dentitheca dendritica ( Nutting, 1900) —gonotheca given off from stem apophysis, replacing the coneshaped nematotheca at tip of mamelon (A); female gonothecae arising from within one of the lateral nematothecae flanking the hydrotheca, in lateral (B) and frontal (C) views, or replacing the mesial nematotheca (D); size difference between male (E) and female (F) gonotheca; size and shape variation of female gonotheca (G1–5). H–N: Nemalecium gracile sp. nov. —silhouette of a stem (H); stem internodes (I1–5); hydrotheca (J); female (K, L) and male (M, N) gonothecae. O–Z: Nemalecium cf. lighti ( Hargitt, 1924) —silhouettes of colonies from Martinique (O) and Alor (T); internodes in specimens from Martinique (P, Q), Alor (U, V), and Hatta (X); hydrotheca from material from Hatta (Y); male (R) and female (S) gonothecae from colony from Guadeloupe; male gonothecae from specimens from Alor (W) and Hatta (Z). Scale bars: 200 µm (A–D, J, Y), 300 µm (E–G), 500 µm (I, K–N, P–S, U–X, Z), 1 mm (H, O, T).

The origin of gonothecae in D. dendritica is peculiar among the genus, as they always replace nematothecae: usually, they are given off from the conical nematothecae situated in the axil of the internode apophyses of stem and branches, but also from the mesial, or one or both lateral nematothecae associated with a hydrotheca. In contrast, the gonotheca of D. alata (Bale, 1888) replaces a hydrocladium near the stem base ( Watson 1997), and is borne in the axil of internode apophyses in D. asymmetrica ( Bale 1914) , D. bidentata ( Migotto & Marques 1999) , D. habereri ( Di Camillo et al. 2010) , and D. hertwigi ( Hirohito 1995) .

Dentitheca dendritica appears to be a dioecious species, while Migotto & Marques (1999) found both mono- or dioecious cormoids in D. bidentata , yet no information is available on the remaining members of the genus.

The present study suggests that the medusoids of D. dendritica are non-released, most of them remaining attached to the blastostyle during and after the spawning, then degenerating inside the gonotheca ( Fig. 1 K–M). This is also firmly supported by the lack of muscle fibers in the ectoderm of subumbrella, and possibly of a (functional) velum. No active contractions of the bell have been seen, suggesting that they may be unable to undertake efficient movements (including swimming), thus explaining why they remain captive within the gonotheca and undertake locally their spawning, followed by their decline.

In contrast, the medusoids of D. bidentata appear comparatively more robust, having a thick-jellied umbrella provided with a basal velum, enabling them to swim actively and shed their gametes through vigorous contractions of the bell ( Migotto & Marques 1999).

It is curious to note that the non-released medusoids of D. dendritica exhibit certain common features with the dispersive stage observed in as an yet undescribed, epiphytic species of Antennella from Reunion Island, Indian Ocean ( Bourmaud & Gravier-Bonnet 2005). Both share in common the lack of muscular fibers and nematocysts, as well as the apparent absence of a velum.

The absence of stinging cells, the keystone diagnostic feature of cnidarians in general and hydrozoans in particular, is striking. A similar situation is met with in the medusoids of Sertularella diaphana (Allman, 1885) but, as a difference, they are still capable to swim due to the presence of muscle fibers in the ectoderm of the umbrella ( Gravier-Bonnet & Lebon 2002).

From the present, rather scant data, we conclude that is possible that the non-released medusoids of both D. dendritica and Antennella sp. may represent a further step towards gonophore regression. It is, however, too early to draw a solid conclusion regarding the evolutionary implications of such a phenomenon, and the discovery of additional life cycles in the thecates is necessary to provide further evidence on this question.

Figures

FIGURE 1. Dentitheca dendritica (Nutting, 1900) — fertile colony in situ (A); detail of a fertile branch showing arrangement of gonothecae (B); female (C, D) and male (E, F) gonothecae; female gonotheca seen with incident (G) and transmitted light (H), showing the terminal plate (t. p.) and the belt of refringent corpuscles (r. c.) of the medusoid; female medusoid releasing its oocytes within the gonotheca (I); eggs (e.) and developing embryo (d. e.) within the female gonotheca (J); medusoids still attached to the blastostyle after the release of the gametes in the water column (K – M). Scale bars: 100 µm (J), 200 µm (E – I, K – M), 400 µm (C, D), 2 mm (B), 3 cm (A).