Alcyonidium nodosum O’Donoghue and de Watteville, 1944

Ryland, J. S., 2001, Convergent colonial organization and reproductive function in two bryozoan species epizoic on gastropod shells, Journal of Natural History 35 (7), pp. 1085-1101 : 1089-1091

Alcyonidium nodosum O’Donoghue and de Watteville, 1944

The colony of A. nodosum is thick, mammillate, and deep orange or purple in colour. The mammillae, with a nearest neighbour distance of ~ 2.6 mm ( table 1), are elevated ~ 1 mm above the surround; they appear to follow a spiral course parallel to the whorls of the shell, although the shell itself is almost smooth. The summits of mammillae are occupied by large zooids, the surrounding area by smaller zooids. Those occupying the mammillae, as O’Donoghue and de Watteville (1944) noted, are very large (~ 0.65 Ö 0.55 mm, table 1) and polygonal, but often associated with small intercalary zooids (®gures 1D, E). Sectioning showed these large zooids to be deeper than wide (®gures 1E, 2A), extending virtually to the base of the colony. They overlay a few small, defunct and presumably neanic zooids.

The area between the mammillae comprises much smaller (~ 0.43 Ö 0.38 mm), variously polygonal zooids (®gures 1B±D, 2B). The mammilla zooids in freshly collected specimens everted tall lophophores of 11±12 tentacles, each raised on an elongated`neck’ composed partly of an oral papilla and partly of the evaginated tentacle sheath (see ®gure 6). The lophophores displayed marked departure from radial symmetry, the adneural tentacles being longest. Surrounding zooids had less elevated lophophores, which were smaller though comprising more (15±16) tentacles, and displayed little departure from radial symmetry. The tentacles of both types of lophophore appeared to carry the normal complement of cilia and were feeding. The lophophores of surrounding zooids emerged readily in the vigorously moving water of the holding tanks but were reluctant to do so in small containers under the microscope. Though several authors have inferred that mammillae determine the position of permanent exhalant chimneys ( Banta et al., 1974; Cook, 1977; Taylor, 1979; Cook and Chimonides, 1980), the failure of lophophores to emerge in large numbers made it impossible to verify this.

The mammilla zooids are closed by a sphincter muscle (®gure 2A), have a functional polypide with conspicuous retractor muscle ®bres, and generally contained several small brown bodies. At the time of collection, at the end of October, these zooids had conspicuously white contents (®gure 1B±D), which suggested that they contained spermatozoa. The sections con®rmed that the vast coelomic lumen was ®lled with developing and mature spermatozoa (®gure 1E). They suggest that testes were situated along the lateral and frontal zooid walls, where signs of spermatogenesis and clusters of sperm morulae were apparent. The remaining volume was packed with mature sperm. No ovary was ever seen, so that zooids are assumed to be male only.

An intertentacular organ was present in many of the lophophores of the surrounding zooids. The intertentacular organ is a small, internally ciliated, funnel located between the dorso-medial tentacles in lophophores of the anascan bryozoans Conopeum , Electra and Membranipora , and in some species of Alcyonidium , at certain seasons of the year. It was similar to that occurring in A. mytili Dalyell (see Cadman and Ryland, 1996) and in an unidenti®ed species occurring on the west coast of Canada and northern USA (unpublished observation). In Electra , Membranipora and Alcyonidium mytili the intertentacular organ has been shown to function for the discharge of ova and either as a site for fertilization or for the ingress of sperm ( SileÂn, 1966; Cadman and Ryland, 1996; Temkin, 1996), occurring onlyÐwith the

Notes: 1, maculae: in Hippoporidra the spots (not equivalent to the mammillae or the sum of the mammilla zooids); mammillae: in Alcyonidium the sum of the mammilla zooids (for two colonies, A and B). 2, maximum linear dimensions. 3, (max. length1 min. length) / 2 Ö (max. width1 min. width) / 2. 4, based on the longer pair of tentacles. 5, the four tentacles were commonly not spread at all.

apparent anomaly of Alcyonidium diaphanum (Hudson)Ðin species that are oviparous. The presence of the intertentacular organ on the lophophore of the surrounding zooids indicated that they were actually or potentially female. This was con®rmed when the process of egg discharge was observed. A slenderly ovoid object was observed just below the intertentacular organ in each of two neighbouring zooids. Shortly afterwards in one of the zooids this object, evidently an egg, was noted as being in the chamber of the intertentacular organ. Both lophophores were then retracted. The one with the egg in the intertentacular organ soon everted, with the egg now more distally situated. The egg slowly moved to the opening of the funnel, assuming spherical shape as it did so, until it was free and dropped down to the surface of the colony, where it remained. An egg of this size, approximately 60 m m diameter, is clearly destined to develop into a small cyphonautes larva (see Cadman and Ryland, 1996).

The serial sections showed that, between mammillae, the smaller zooids are multi-laminar, and only those near the frontal surface of the colony contain polypides (®gure 2B). Such zooids contain a few small brown bodies whereas the more basal, enclosed zooids contain many. This suggests that each zooid supports several generations of polypides before being overgrown, presumably by zooid buds of intercalary origin as described in A. mytili (see Cadman and Ryland, 1996). The very small size of the accumulated brown bodies suggests that at least two arise from each polypide degeneration, as happens in certain other species of Alcyonidium . These zooids were female only and retained their functional lophophores whilst the oocytes were developing. Ovaries were present in many of these zooids, situated between the base of the stomach caecum and the body wall, and usually quite close to the latter (®gures 1F, 2C±F). Small ovaries appear subspherical but later, when some of the oocytes are larger (®gure 2E), they have a hollow, lens shape. At no stage of oogenesis, from small ovaries (®gure 2C) through to the laying of eggs, was there any evidence of polypide degeneration. This accords with what has been described in the oviparous A. mytili ( Cadman and Ryland, 1996) ; but in A. nodosum it is not known either whether the polypide degenerates prior to commencement of oogenesis or at what stage the intertentacular organ appears.

All developing oocytes contain a large germinal vesicle, which stains less densely with Mallory’s than the ooplasm and yolk, and contains a single, prominent nucleolus (®gures 1F, 2D±F). It appears that the follicle cells of the ovary dissociate and / or break down to release free oocytes into the coelomic lumen. These lack the germinal vesicle and nucleolus (®gure 2G), which accords with what Temkin (1996) has described in an unidenti®ed oviparous Alcyonidium from the Paci®c coast of North America. The present observations are therefore consistent with Temkin’s demonstration that fertilization (syngamy) occurs at about the time of ovulation of eggs from the ovary (though sperm transfer and insemination may occur earlier). Very few free eggs have been found in the sections cut, suggesting that they are spawned soon after ovulation (which contrasts with the species from North America, which may contain vast numbers of eggs, personal observation).

Sperm are presumed to be liberated in the usual bryozoan manner, via all or just the adneural tentacles, but no observations were possible with the magni®cation of a stereo-microscope. The huge production of sperm is one of the most striking features of reproduction in A. nodosum and emphasizes once again the need for bryozoans to overcome problems of dilution by diOEusive and turbulent processes during sperm transfer. It was noted that the whelks tended to occur on the shore in little groups, perhaps aggregatin g for mating purposes, but cross-fertilizatio n between Alcyonidium colonies on diOEerent whelks will still present major problems (see Levitan, 1995; and Levitan and Petersen, 1995, for general discussion on sperm limitation and appropriate references).