The Spermatheca of Loligo vulgaris. I. Structure of the Spermatheca and function of its Unicellular Glands.
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1 The Spermatheca of Loligo vulgaris. I. Structure of the Spermatheca and function of its Unicellular Glands. By G. J. van Oordt. Department of Experimental Morphology, Zoological Institute, University of Utrecht. With Plate 49 and 1 Text-figure. 1. INTRODUCTION. IN the Decapod Cephalopods the transfer of the spermatophores from male to female takes place with the aid of the hectocotylus, the left ventral arm of the male. There are two methods of copulation in the American squid Loligo pealii. According to Drew (1910), the spermatophores are inserted into the mantle chambers of only those females which are about to deposit their eggs. The male swims by the side of such a female, with his head in the same direction. Just before attachment, he sinks slightly beneath her and grasps her body with his arms; the hectocotylus then seizes the spermatophores which appear in the opening of the funnel, and with a rapid sweep these are immediately inserted into the mantle chamber of the female. After about 5 or 6 seconds, this arm is withdrawn; the animals separate almost immediately and in another 5 or 6 seconds the empty cases of the spermatophores pass out of the funnel. The sperm-reservoirs are found later to be attached near the end of the oviduct (Drew, 1910, pp ). The secretion of glands of the hectocotylus possibly helps to attach the spermatophores to each other and to the hectocotylus during their transport into the mantle chamber of the female. Although the female of Loligo pealii may not yet be ready to deposit her eggs, she is capable of copulation. According to Drew (1910, pp ) the sperm-reservoirs are under
2 594 G. J. VAN OORDT such circumstances ejaculated from the spermatophores, and then attached to a receiving depression of the buccal membrane of the female. This type of copulation does not take place between a male and female, united parallel, but when facing each other. When the animals separate, the empty cases of the ejaculated spermatophores are held for several minutes between the arms of the female and are then finally dropped. The spermreservoirs are attached by cement, carried inside the spermatophores, 1 and liberated by the ejaculation. The depression which receives the sperm-reservoirs is situated at the anterior side of the spermatheca; the latter possesses the shape of a mamma, having a distinct nipple, the anterior tip of which bears the opening of the spermatheca. This whole structure is found at the inner side of the buccal membrane, and is therefore in the swimming animal, situated ventrally to the mouth. According to Verwey (unpublished observations) the spermatophores of specimens of Loligo vulgaris, caught off the coast of Holland, are never deposited in the mantle chamber of the female, but are always attached to the depression near the wall of the spermatheca or to the wall itself. As Drew has already described, the spermatozoa become stored in the spermatheca. The structure and size of this organ were described by him in outline, but its physiology is still practically unknown. Little or nothing is known of the following points: (1) the factors which play a part in the transit of the seminal fluid from the sperm-reservoirs into the spermatheca; (2) the function of the unicellular glands, found almost everywhere at the inner side of the spermatheca; and (3) the function of the large ganglion lying near the spermatheca. 2. MATEBIAL AND TECHNIQUE. The squid furnishing the material for the present investigation is Loligo vulgaris L., which is obtainable every spring in large quantities from the North Sea in the Zoological Station at Den Helder. It is very easy to get here abundant fresh 1 For further particulars concerning the spermatophore and its ejaculation of. Drew (1919).
3 SPERMATHECA OF LOLIGO 595 animals, but living, healthy, undamaged specimens are only available in small numbers. All spermathecae were fixed in Bouin's fluid, and stained with haemalum and eosin in the ordinary way, or with van Gieson's stain for the distinction of connective and muscle tissue. 3. THE STRUCTURE OF THE SPERMATHECA. As already mentioned, the spermatheca has mostly a mammalike shape, with a distinct nipple, on which the entrance to the interior of the spermatheca is found (fig. 1, PL 49). The wall of the spermatheca consists, contrary to the body-wall, of a deeply staining high columnar epithelium, covered by a mass of rather hard material, the cuticle; the latter is thicker in the region of the depression (where the sperm-reservoirs are mostly attached) and is evidently secreted by the epithelial cells. In many cases, sperm-reservoirs are found outside this depression; according to Drew (1910, p. 335) the spermatozoa, escaping from such reservoirs, do not find their way into the spermatheca. The wall of the spermatheca (fig. 2, PI. 49) consists further of a rather thick layer of connective tissue and muscle-fibres. The lumen of the spermatheca is divided by several partitions, outgrowths of the connective tissue and muscle sheath, into a number of primary alveoli, which in their turn are subdivided into secondary alveoli; the latter are lined by a cubical epithelium at their base and by a cubical epithelium intermixed with numerous secretory goblet-cells in the region near the entrance to the spermatheca. In the interior part of the alveoli, especially near the wall of the spermatheca, large quantities of spermatozoa are stored. When a spermatheca is opened, and its contents examined microscopically, it is found that the spermatozoa are inactive in the alveoli. 4. FUNCTION OF THE SECRETION OF THE GOBLET-CELLS. In order to determine how far the spermatozoa of Loligo enter the spermatheca owing to the attraction of a chemical substance secreted by the goblet-cells, or how far the seminal fluid is sucked into the spermatheca by the action of the
4 J. VAN OOKDT muscles of the spermatheca-wall, an examination was made of the motility of the spermatozoa in a pulp of the wall of the spennatheca and its contents. In the sperm-reservoirs the spermatozoa are motionless, but when discharged from the reservoirs into sea-water they im- AppiirotiiB used for the observation of the motility of Loligo- Mpormatossoa. A, tube filled with contents of the spermatheca. B, tube filled with sea-water; c, cork. mediately become very active. Spermatozoa were transferred into a T-shaped tube (Text-fig. 1), filled with sea-water; one of the openings of which was closed by a cork (c), the other two openings, however, were closed by small tubes covered with pieces of chamois, impregnated with sea-water. One of these small tubes (A) was filled with a pulp of the wall of a spermatheca, the other (B) contained only sea-water. Under the microscope it could be clearly seen that the spermatozoa (very active in pure sea-water) became quiet in a few minutes when in the neighbourhood of the small tube (A), containing the secretion of the spermatheca-wall. It seems clear that this secretion does not attract spermatozoa; on the contrary, the latter are immobilized by the action of a substance which must have passed through the chamois-cover. This also becomes evident when a
5 SPBBMATHECA OF LOLIGO 597 small quantity of the contents of a spermatheca is transferred to sea-water containing very active L o 1 i g o -sperm; the spermatozoa are then totally immobilized after 5 to 10 minutes. From these simple experiments it followed that chemotaxis is not the cause of the spermatozoa entering the spermatheca. When the spermatozoa have entered this structure they become inactive after a few minutes. The experiments of Gray (1928) have shown that the activity of sea-urchin spermatozoa is due to the grade of dilution of the seminal fluid. From my experiments it does not seem likely that, in the squid, mechanical overcrowding can be the origin of the inactivity of the spermatozoa in the spermatheca. Lack of living healthy squids made it impossible to determine in vivo how the seminal fluid, discharged from the spermreservoirs, is taken up by the spermatheca. The structure of its wall, in which many muscle-fibres are found, makes it probable that the seminal fluid is sucked up by the spermatheca by means of movements of its muscles. This is also suggested by an observation of Drew (1910, p. 346) that the spermatozoa enter the opening of the spermatheca in a narrow stream, and with the tails all turned in the same direction, i.e. the heads going first and the tails trailing behind; my own observations show that, sometimes, a whole sperm-reservoir may be found in the interior of the spermatheca. The above experiments clearly show that the secretion of the inner epithelium of the spermatheca has an immobilizing effect on stored spermatozoa. The function of this organ therefore may be compared to that of the mammalian epididymis. In this gland the spermatozoa are also preserved, till they are ejaculated during coitus (von Lanz, 1924, 1926, 1936). Moreover, it was found (von Lanz, 1929) that the acid reaction of the secretion of the epididymal epithelium renders the spermatozoa quite inactive. The hydrogen-ion concentration of the contents of the spermatheca had to be determined. The small size of the spermatheca made it impossible to determine the hydrogen-ion concentration of its contents by means of the more usual laboratory methods. In the Laboratory of Comparative Physiology at the University NO. 320 S S
6 598 G. J. VAN OORDT of Utrecht, the ph of the interior of the spermatheea (sent from Den Helder to Utrecht) was measured by the glass-electrodemethod, and found to be A pulp of the spermatheca-wall in distilled water showed a ph of The contents of the L o 1 i g o-spermatheea are thus definitely acid, as is the case with the contents of the mammalian epididymis (von Lanz, 1929). When, moreover, the acidity of sea-water in which large quantities of Loligo-spermatozoa are active, is artificially brought to the same level as that of the spermatheea contents, the sperm shows less activity after 5-10 minutes. These observations, therefore, make it highly probable that L o 1 i g o- spermatozoa, stored in the spermatheea, are immobilized by the acid reaction of the secretion from the inner epithelium of this organ. 5. SUMMAHY. The structure of the spermatheea of Loligo vulgaris is described; it lies on the inner wall of the buccal membrane and within it large quantities of inactive spermatozoa are stored. This inactivity of the spermatozoa within the spermatheea is attributed to the effect of the secretion of the goblet-cells, situated as unicellular glands on the inner wall of the spermatheea. Inactive spermatozoa from the spermatheea become very active in sea-water, but are immobilized again after a few moments' contact with the pulp of the spermatheea contents. The hydrogen-ion concentration of the spermatheea contents is approximately 6-06; and, since spermatozoa become inactive in sea-water, the hydrogen-ion concentration of which is increased to this level, it seems probable that the inactivity of the spermatozoa within the spermatheea is due to the presence of hydrogen-ions. The spermatheea is functionally comparable to the mammalian epididymis. 6. ACKNOWLEDGEMENTS. I wish to express my thanks to Mr. L. H. Bretschneider for his valuable technical help, to Dr. H. J. Vonk and Miss A. M. W. Mennega for measuring the ph of the spermatheea contents,
7 SPBRMATHECA OF LOLIGO 599 and to Dr. J. Verwey, director of the Zoological Station at Den Helder for providing the material during my stays at this station and for giving much information on the habits and lifehistory of the common squid. EBFEBENCBS. Drew, G. A., "Sexual activities of the squid, Loligo pealii", ' Journ. Morph.', "Sexual activities of the squid, Loligo pealii. The spermatophore; its structure, ejaculation, and formation", ibid., 32. Gray, J., "Effect of dilution on activity of spermatozoa", 'Brit. Journ. exp. Biol.', 5. von Lanz, T., "Nebenhoden einiger Saugetiere als Samenspeicher", 'Verh. Anat. Gesellsch.', "Bau u. Funktion d. Nebenhodens u. ihre Abhangigkeit von d. Keimdruse", 'Zeitschr. f. Anat. und Entw.-gesch.', "Die reelle Aciditiit i. d. einzelnen Abschnitten d. mannliohen Genitalapparates der Ratte u. ihre hormonale Bedingtheit", 'Pflugers Arch.', "Die Samenspeicherung beim Mann", 'Klin. Wochenschr.', 1936, ii, p EXPLANATION OF PLATE 49. Fig. 1. A median section of the spermatheca of Loligo vulgaris. Conn.muac., sheath of connective tissue and muscle-fibres; depr., depression for attachment of the sperm-reservoirs; sperm., spermatozoa, stored in alveoli of the spermatheca. ( X 18). Fig. 2. Part of the wall of the spermatheca. (X 120.)
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