Getting under the skin: autonomous implantation of squid spermatophores.

Squid spermatophores are complex structures that store sperm and, when transferred to the female, evert into spermatangia. Some deep-sea squid implant spermatangia into unmodified tissue of the female. Several hypotheses have been proposed to explain this peculiar implantation process. Here, through on board observation of freshly caught deep-sea squid (Moroteuthis ingens), we show for the first time that spermatophores have an autonomous mechanism that enables them to migrate into body tissue. Cephalopod spermatophores are complex secreted structures that hold sperm masses and that consist, in part, of an ejaculatory apparatus for releasing the sperm mass and a cement body presumably for attaching the sperm mass to the female (1). Spermatophores are either transferred to the female by the male’s hectocotylus, a specialized arm, or by a long penis, which is present in species that lack hectocotyli (2). After being discharged from the spermatophore in the spermatophoric reaction, the sperm mass is encased in a thin covering, with the cement body at one end. This discharged structure, the spermatangium, may attach to the skin of the female or be deeply embedded in her skin or muscle. Many aspects of reproduction remain unknown for deepsea squids owing to the inaccessibility of their habitat and the difficulty in obtaining large adult animals. In an extensive review on reproduction in oceanic cephalopods, Nesis (2) stated that “one of the most intriguing puzzles of spermatophore transfer is the rather common case of spermatophore embedding in the outer surface of the mantle—in special sites or simply in almost every place.” Although common, the process of deep spermatophore implantation is highly controversial. It is not known what structure or process is responsible for spermatangia penetrating into body tissue. Because squid that implant spermatangia have a long penis and no hectocotylus, embedding has been suggested to involve the penis in a process by which the spermatophores are perhaps hydraulically forced into the tissue (3, 4). Since implanted spermatangia are sometimes associated with wounds or cuts, other hypotheses consider the action of the beaks or the hooks present on the arms and tentacles of many oceanic squid to be responsible for the implantation of spermatangia. Finally, an intrinsic chemical mechanism in the spermatophore’s cement body has been proposed to be able to dissolve the female’s tissue (5). All the above hypotheses are based solely on morphological observations of preserved male and female squid. This study presents the first observations on the process of spermatophore implantation in a deep-sea squid. In addition to showing that the spermatophores of the deep-sea squid Moroteuthis ingens, Smith 1881, are able to autonomously migrate through body tissue, we have determined the role of the penis in the transfer of spermatophores. On board the research vessel Dorada of the Falkland Islands Government Fisheries Department, spermatophores were taken from the penis of a moribund specimen of the deep-water squid M. ingens, a species that embeds spermatangia (4). The spermatophores were positioned on the outer mantle of a dead male (Fig. 1a), and the spermatophoric reaction was induced by gently pushing on the oral end of the spermatophore, which contains the ejaculatory apparatus. After pressure was exerted on the ejaculatory apparatus, the spermatophores started ejaculating (Fig. 1b); after a few minutes, spermatangia had autonomously embedded themselves into the tissue (Fig. 1c, d). Received 1 December 2006; accepted 4 March 2007. * To whom correspondence should be addressed. E-mail: H.J.T.Hoving@ rug.nl Reference: Biol. Bull. 212: 177–179. (June 2007) © 2007 Marine Biological Laboratory