A study of the oviducal glands and ovisacs of Balanus balanoides (L.) together with comparative observations on the ovisacs of Balanus hameri (Ascanius) and the reproductive biology of the two species

Abstract

A mainly microscopical study has been carried out on the oviducal glands and ovisacs of two hermaphroditic sessile barnacles, Balanus balanoides and Balanus hameri . In both species each gland secretes an ovisac, once a year, for a very restricted period before copulation. The morphology of the glands of B. balanoides has been worked out from serial sections and a Plasticine model. Three regions have been established within the glands; two are ectodermal in origin, namely the main chamber and exit canal, while the third, the proximal chamber, is mesodermal. The exit canal is always lined with cuticle, but the main chamber for most of the year is not. However, in both species main chamber cells begin to secrete the ovisacs several weeks before copulation. Ovisacs are undoubtedly cuticular structures. The cytology of B. balanoides main chamber cells during the sequence of events leading to the formation of ovisacs has been followed by means of transmission electron microscopy. The cells each develop a long apical cytoplasmic extension; from these extensions and the apical cell surfaces secretions pass out to form the ovisac wall. This wall has two zones, an outer electron-dense zone 14 pm thick and an inner flocculent zone 6 pm thick. When fully formed the ovisac is released from the main chamber cells to lie in the oviducal gland lumen, although the neck of the ovisac continues to be firmly attached to specialized anchor cells. The cytoplasmic extensions of the main chamber cells break away with the ovisac as it is released and eventually form the pores in the ovisac wall. Scanning electron microscopy was used to examine such unstretched sacs. In B. balanoides the main chamber cells then partially retrogress, shedding secretions and portions of cytoplasm into the gland lumen. It is proposed that these ‘formed bodies’, by their osmotic activity, draw water and low molecular mass solutes into the gland lumen from the haemolymph. The ‘formed bodies ’ swell and burst, thereby accumulating fluid in the lumen of the gland, which becomes highly swollen. It is this fluid that has the activating factor(s), thought to be the ammonium ion, needed to activate inseminated sperm. In this condition B.balanoides becomes a receptive female. In B. hameri , although there is some retrogression of the main chamber cells with secretion of ‘formed bodies’, there is much less accumulation of fluid and so the oviducal glands do not become so highly swollen. The copulatory act of B. hameri was observed closely and comparison was made with that of B. balanoides . In B. hameri a single male is involved and a single insemination is sufficient for egg laying to commence, while in B. balanoides more than one male may be involved and multiple inseminations are needed before egg laying begins. Oocytes (eggs) pass from the ovaries down the oviducts and into the elastic ovisacs lying in the oviducal glands. As the ovisacs distend with eggs they first expel the oviducal gland fluid into the mantle cavity and then they themselves are forced out into the mantle cavity. As the stretching continues the ovisac wall becomes very thin and the pores enlarge. Although B. balanoides sperm, which are 0.5 pm in diameter, can easily pass into the 0.7 to 1.6 pm diameter pores of an unstretched ovisac, those of B. hameri , which are also 0.5 pm in diameter, need the ovisac to stretch and the pores to enlarge from their original diameter of 0.2 pm before sperm can pass through and fertilize the eggs. Inseminated sperm, in both species, are deposited as gelled masses. In B. balanoides the expelled oviducal gland fluid activates such sperm, but inseminated sperm of B. hameri become active in seawater. At any one time, only those sperm on the outer surface of the masses are active, and so a staggered release takes place. This is essential when egg laying takes more than 30 min and the sperm of B. balanoides and B. hameri are active for only 5-6 min and 12-13 min respectively. The fully formed egg masses are finally freed from the anchor cells within the glands and moved to the bottom of the mantle cavity, where egg development takes place.