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Novel Cnidocysts of Narcomedusae and a Medusivorous Ctenophore, and Confirmation of Kleptocnidism

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Novel Cnidocysts of Narcomedusae and a Medusivorous Ctenophore, and Confirmation of Kleptocnidism TISSUE & CELL 1989 21 (5) 723-734 0 1989 Longman Group UK Ltd DANIkLE CARRk*, CLAUDE CARRl!* and CLAUDIA E. MlLLSt NOVEL CNIDOCYSTS OF NARCOMEDUSAE AND A MEDUSIVOROUS CTENOPHORE, AND CONFIRMATION OF KLEPTOCNIDISM Keywords: Cnidocyst. nematocyst. apotrichous isorhiza, hydrozoa, ctcnophora, jellyfish ABSTRACT. Cnidocysts have been examined from the tentacles of the ctenophore Haeckelia rubra (Euchlora rubra) and five species of hydrozoan narcomedusae (Solmundella bitentaculata. Aegina citrea, Solmissus marshalli, Solmissus albescem. and Cunina sp.) using TEM, both in sections and by tiring whole cnidocysts onto EM grids. The study revealed that these apotri- chow isorhiza cnidocysts have a novel morphology in which the intracapsular inverted tubule has five circumferential pleats when viewed in transverse section, rather than the usual three pleats. Accordingly, the definition of helicoptychoneme cnidocysts has been broadened to include both the usual three-pleated cnidocysts and these new five-pleated cnidocysts. In general. apotrichous isorhizas have subspherical capsules with a thick, bilaycrcd wall, whose interior is nearly tilled with the regularly coiled, helically folded, five-pleated inverted tubule. Upon discharge, the everted tubule is several mm long and the five circumferential pleats become manifested as five helical rows of spines running up the tubule, which has three morpho- logically different segments. The very short basal segment is devoid of ornamentation; the remaining proximal portion is characterized by live spirals of uniform, closely packed short spines; the long distal portion is charactcrizcd by a single spiral of regularly spaced large spines that derive from all five spiralcthe five spirals are otherwise demarcated in the distal portion by ‘scales’ that are visible only with the electron microscope. Introduction ing by cerianthid anemones (Mariscal et al., 1977). During a recent ultrastructural study of the It was subsequently determined that the ctenophore Haeckelia (Euchlora) rubra cnidocysts of Haeckelia rubra are of exoge- (Kblliker, 1853), which has cnidocysts rather nous origin (CarrC and Car& 1980a,b) and than the typical ctenophoran colloblasts on that they are acquired when the ctenophore its tentacles for the capture of prey, we disco- preys on the cnidocyst-laden tentacles of vered that these ctenophore cnidocysts have hydrozoan narcomedusae (Mills and Miller, a novel morphology in that the intracapsular 1984). After ingestion by the ctenophore, the (inverted) tubule has five circumferential medusan cnidocysts are incorporated into the pleats when viewed in transverse section ctenophore’s own tentacles for use in further (CarrC and Carr6, 1980a, Fig. 8). All pre- prey capture. Having established the predatory link viously described cnidocysts (from cnidarian between the medusivorous ctenophore tissue) have only three circumferential Haeckelia rubra and its narcomedusan prey, pleats, with the exception of the unusual and having seen an indication of an unusual multi-folded ptychocysts used in tube build- new morphology during the earlier study of ctenophore cnidocysts, we have now under- *Station Zoologique, CEROV. 06230 Villefranchc-sur- taken a more complete, comparative ultra- Mer, France. tFridav Harbor Laboratories. Universitv of Wash- structural study of the tentacle cnidocysts of ington, 620 University Road, Friday Harbor.‘Washington several species of narcomedusae and the 98250, USA. cnidocysts of H. rubra. Received 17 January 1989 The present study began as a comparison --.- - _,_”.,_ ,.. “^ CNIDOCYSTS OF NARCOMEDUSAE 725 of the tubule morphologies within undis- posium on the Biology of Nematocysts in charged cnidocyst capsules, and then Irvine, California (Hessinger and Lenhoff, expanded to include the microanatomy of the 1988). ornamentation of the tubules of discharged Animals were collected from the Bay of cnidocysts. Villefranche, Villefranche-sur-Mer, Medi- Both Haeckelia rubra and all of the species terranean Sea [Solmundella bitentaculata of narcomedusae that we examined have two (Quoy and Gaimard, 1833); Solmissus albes- sizes of subspherical cnidocysts on their ten- tens (Gegenbaur, 1856); and Haeckelia tacles. Similar cnidocysts are also found on rubra] and from Friday Harbor, Washington, the exumbrellas of most narcomedusae. NE Pacific [Aegina citrea (Eschscholtz, Based on light microscopy, narcomedusan 1829); Solmissus marshalli (Agassiz and cnidocysts have previously been described as Mayer, 1902); and Cunina sp.]. ‘atrichs’ (without spines) in the narco- Cnidocysts were examined both with the medusae Polypodium hydriforme (Lipin, light microscope and transmission electron I911 as interpreted by Weill, 1934), Cunina microscope (TEM). Material to be viewed lativentris (Weill, 1934), in the pelagic larva in thin section was fixed using the low of Solmundella bitentaculata (Weill, 1934, osmium-glutaraldehyde pre-fixative tech- species identified by C. Carre), and on the nique of Eisenman and Alfert (1982) and exumbrellas of Aegina citrea and Solmissus embedded in Spurr’s epoxy resin. Thin sec- marshalli (Mackie and Mackie, 1963), or as tions were observed on a Hitachi HU600 ‘apotrichous isorhizas’ (having an iso- TEM. diametric tubule with spines only on the distal Whole discharged cnidocysts were exa- portion) in Aegina citrea, Solmissus marshalli mined by TEM using Robson’s (1953) tech- and Solmissus albescens (Mackie and nique of discharging cnidocysts directly onto Mackie, 1963; Bouillon, 1985; Purcell and coated EM grids. Tentacles were snipped off Mills, 1988). In the present study we have living medusae and were then gently dragged examined the two sizes of subspherical cnido- across a parlodion-carbon or collodion- cysts found in the tentacles of several species coated TEM grid. Each grid was then rinsed of narcomedusae, all of which can be classi- in distilled water, air-dried, and subsequently fied as apotrichous isorhizas in the sense of examined in a Hitachi HU600 or Philips Mackie and Mackie (1963) and Mariscal EM300 TEM without further preparation. (1974). Materials and Methods Results The terminology for cnidocysts used in this Cnidocysts of Haeckelia rubra (Ctenophora, paper is that agreed upon at the 1986 Sym- Family Haeckeliidae) (Figs l-6) Plate 1. Haekelia rubra (Figs l-6). Fig. 1. Stock of apotrichous macroisorhizas and microisorhizas at the tentacle base. x2000. Fig. 2. Stretched tentacle, showing three microisorhizas (arrows). X 1400. Fig. 3. Discharged apotrichous microisorhiza. The tubule extends many times the width of the photograph. x2ooO. Fig. 4. Microisorhiza in its endocytotic vesicle, seen in longitudinal section. Note the five longitudinal pleats exhibited by each profile of the cnidocyst tubule, the coiled organization of the tubule around the axis of the capsule, and the reduction of the tubule diameter from its base (near the operculum, upper right) towards its distal end (at the opposite pole). ~22,000. Fig. 5. Profiles of a cnidocyst tubule in an undischarged macroisorhiza seen in section. Spines till the lumen of the inverted tubule. X60,000. Fig. 6. Inverted (undischarged) cnidocyst tubule showing the helically folded tubule super- coiled around its own axis. ~40,000. 726 CARRIj ETAL. Specimens of Haeckelia rubra possessed both tional profile of the intracapsular inverted a small number of macroisorhizas (mean tubule shows the presence of five longitudinal diameter in life of 8pm) and many more pleats (Figs 4 and 5). It is also clear that the microisorhizas (4 pm) (Figs l-3). These inverted tubule within the capsule is helically cnidocysts were regularly arranged in a row folded along its axis (Fig. 6). along the length of each of the two tentacles Haeckelia rubra is a rare species in all (Fig. 2) and in a cluster at the tentacle base known locations. Because of its scarcity, we (Fig. 1). have not had a chance to study the micro- In sections, these two categories of cnido- anatomy of the everted tubules of its cnido- cysts could be differentiated by the diameters cysts on grids in the electron microscope. By of the capsules as well as by the diameter light microscopy, its cnidocysts correspond and length of the tubule contained within-in well to those we have seen in the five species other respects their morphologies are similar. of narcomedusae described below. The capsules were devoid of the cnidocil and all other accompanying structures of the cnidocyte (see Fig. 14 for a cnidocyte of Cnidocysts from the tentacles of narco- Aegina citrea), as expected since only the medusae (Cnidaria, Class Hydrozoa) naked cnidocyst capsules are incorporated We studied a total of five species of narco- within endocytotic vesicles (Fig. 4) into the medusae all of which co-occur with the cteno- tissues of the ctenophores (Car& and Carre, phore Haeckelia rubra (Carre and Carre. 1980a). The thick capsule wall is mostly elec- 1980a,b; Mills and Miller, 1984). The macro- tron-lucent, with a thin electron-dense outer isorhizas and microisorhizas from all of the layer (Fig. 4). The inside of the capsule is narcomedusae were ulstrastructurally simi- nearly filled by the inverted tubule, which lar. The basic structure will be described in is regularly coiled around the axis of the cap- detail below for Solmundella bitentaculata sule. A uniform reduction in the diameter and differences will then be reported under of the tubule along its length is indicated by the other species names. the tubule profiles which are thicker proxi- mally (i.e. near the
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