Male reproductive tract, spermatophores and spermatophoric reaction in the giant octopus of the North Pacific, Octopus dofleini martini

Abstract

The male reproductive tract of Octopus dofleini martini lies enclosed in the genital bag, inside the mantle cavity. It consists of the testis, vas deferens proximale, spermatophoric gland system I (seminal vesicle), spermatophoric gland system II (prostate), vas deferens distale, spermatophoric sac (Needham’s sac) and the terminal spermatophoric duct. The spermatozoa, which upon leaving the testis are as yet not encased, pass first into the vas deferens proximale, which in its gross appearance resembles the epididymis; they then traverse the two tubular spermatophoric gland systems I and II, where they become encased into the spermatophores. Subsequently the spermatophores pass through the vas deferens distale into the spindle-shaped spermatophoric sac, and from there they enter singly the terminal spermatophoric duct consisting of the diverticulum and terminal organ or ‘penis’. The slender cylindrical body of the spermatophore is about 1 m long and consists of two parts, approximately equal in length. The thicker ‘proximal’ ‘male-oriented’ portion, which emerges first from the orifice of the ‘penis’, contains the tightly coiled sperm rope suspended in a viscous and transparent fluid, the spermatophoric plasma; the thinner ‘distal’ ‘femaleoriented’ half of the spermatophore is taken up by the rod-shaped, hyaline core of the ejaculatory apparatus. In between is located the cement body, and the amber-coloured cement liquid. At the distal end of the spermatophore the outer coating forms a cap and a filamentous appendage, the cap-thread. Chemical analyses were performed on spermatozoa, spermatophoric plasma, cement liquid, outer tunic and the hyaline core of the ejaculatory apparatus, obtained from freshly recovered spermatophores. Glycogen was identified as a major constituent of spermatozoa. The extraordinarily high dry-weight content of spermatophoric plasma (nearly 30%) was shown to be largely due to bound amino sugar, carbohydrate, peptide and protein. A peptide separated from the spermatophoric plasma by ultrafiltration was found to be made up to a great extent of aspartic acid and serine. The outer tunic, a tough and elastic membrane, which envelops the body of the spermatophore, was shown to consist mostly of a protein which is rich in proline, lysine, aspartic acid and threonine. The mechanics of the spermatophoric reaction in vitro have been studied in spermatophores extracted manually from the male octopus and placed in sea-water. The complete spermatophoric reaction under such conditions lasted 1 to 2 h. During that interval the sperm rope gradually advanced a distance of about 1 m, from the proximal towards the distal end of the spermatophore. The terminal phase of this process involved an evagination of the ejaculatory apparatus, followed by a rapid movement of the sperm rope; as the sperm rope entered the end portion of the spermatophore, the latter ballooned out into an egg-shaped bladder. Among the factors which contribute to the formation of the spermatophoric bladder, the most important ones are (i) the elasticity of the membranes of the spermatophore, (ii) the extrusion, and subsequently evagination, of the ejaculatory apparatus, and (iii) the influx of sea-water into the spermatophore’s body which causes an approximately fivefold increase in the volume of spermatophoric plasma. Concomitantly with the uptake of sea-water, the dry weight of the spermatophorie plasma declines but the sodium chloride concentration increases. However, the osmolality of the spermatophoric plasma, as assessed by freezingpomt depression, is not altered during the spermatophoric reaction. Events at copulation, that is under conditions in vivo , closely resembled those observed in spermatophores undergoing a spermatophoric reaction in vitro . An interval of 2 to 3 h usually elapsed from the time when the male, using his hectocotylized arm, mserted mto the female the distal (female-oriented) end of a spermatophore, to the moment of the male's withdrawal. After accomplished copulation two spermatophores were usually found firmly lodged in the two oviducts. The sperm-free remnants of the spermatophore bodies dangled free from the orifices of the oviducts. Upon dissection of recently mated females the spermatophoric bladder was usually found within the oviduct, held firmly in position by the evaginated ejaculatory apparatus.

Functional Histology: The Tissues of Common Coleoid Cephalopods

“…4.31,4.32,4.33,4.34 and 4.35) The male reproductive system of coleoid cephalopods consists of a single testis and the gonoduct, which comprises the proximal deferent canal (male duct, spermiduct), blind-end seminal vesicles (spermatophoric glands) and associated accessory gland, the distal deferent canal and a dilatation that, in mature animals, contains spermatophores, the Needham's sac. It opens into the pallial cavity through the gonopore (Mann et al 1970;Wells 1978).…”

“…The spermatozoa leaving the octopus testis pass into the proximal vas deferens (Mann et al 1970). In mature octopus, this highly convoluted duct consists of a ciliated epithelium surrounded by connective tissue.…”

Nocturnal mating behaviour and dynamic male investment of copulation time in the southern blue-ringed octopus, Hapalochlaena maculosa (Cephalopoda: Octopodidae)

“…This disparity might be especially prominent among the octopods (Cephalopoda: Octopoda). For example, at any given time males of the giant Pacific octopus, Enteroctopus dofleini, (Hochberg, 1998) carry up to approximately ten spermatophores (Mann et al, 1970), each of which can take over an hour to be placed during mating (Anderson et al, 2003). By contrast, females of this species spawn up to 100,000 eggs, and are not limited in the number of males with which they can mate (Hartwick, 1983).…”

Treatise Online, no. 17, Part M, Chapter 3: Anatomy of Recent forms

“…From the testis, sperm pass into the seminal duct, which joins the spermatophoric organ. This organ is a complex of glandular tissue and laminae where the sperm are formed into a spiral mass and coated with a tough, elastic membrane to form the spermatophore (Mann, Martin, & thierSCh, 1970). Each spermatophore is tubular and consists of two parts, one largely filled with compacted sperms and the other an invaginated, folded tube forming the ejaculatory apparatus.…”

“…Each spermatophore has a brittle outer coat and a complicated internal structure; the features of spermatophores are of taxonomic value (Mangold, 1989b). The spermatophores range in size from 16 to 18 mm in length in Sepia officinalis and Loligo vulgaris of 300 to 400 mm mantle length, to 65 mm in Octopus vulgaris of 200 mm mantle length, to more than 1 m in Octopus dofleini of about 1.5 m total length (Mangold-wirz, 1963;Mann, Martin, & thierSCh, 1970). The spermatozoa, within the spermatophore, have complex features, and their morphology has been found to support the accepted taxonomic divisions of the subclass (healy, 1995).…”