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University of Groningen Sperm Storage and Mating in the Deep-Sea University of Groningen Sperm storage and mating in the deep-sea squid Taningia danae Joubin, 1931 (Oegopsida Hoving, Hendrik Jan T.; Lipinski, Marek R.; Videler, John J.; Bolstad, Kat S. R. Published in: Marine Biology DOI: 10.1007/s00227-009-1326-7 IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite from it. Please check the document version below. Document Version Publisher's PDF, also known as Version of record Publication date: 2010 Link to publication in University of Groningen/UMCG research database Citation for published version (APA): Hoving, H. J. T., Lipinski, M. R., Videler, J. J., & Bolstad, K. S. R. (2010). Sperm storage and mating in the deep-sea squid Taningia danae Joubin, 1931 (Oegopsida: Octopoteuthidae). Marine Biology, 157(2), 393- 400. https://doi.org/10.1007/s00227-009-1326-7 Copyright Other than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons). The publication may also be distributed here under the terms of Article 25fa of the Dutch Copyright Act, indicated by the “Taverne” license. More information can be found on the University of Groningen website: https://www.rug.nl/library/open-access/self-archiving-pure/taverne- amendment. Take-down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons the number of authors shown on this cover page is limited to 10 maximum. Download date: 02-10-2021 Mar Biol (2010) 157:393–400 DOI 10.1007/s00227-009-1326-7 ORIGINAL PAPER Sperm storage and mating in the deep-sea squid Taningia danae Joubin, 1931 (Oegopsida: Octopoteuthidae) Hendrik Jan T. Hoving · Marek R. Lipinski · John J. Videler · Kat S. R. Bolstad Received: 10 February 2009 / Accepted: 9 October 2009 / Published online: 10 November 2009 © The Author(s) 2009. This article is published with open access at Springerlink.com Abstract Spermatangium implantation is reported in the animals, whether washed ashore, caught by Wshing gear or large oceanic squid Taningia danae, based on ten mated retrieved from stomachs of large predators, remains an females from the stomachs of sperm whales. Implanted important source of biological information. The octopoteut- spermatangia were located in the mantle, head and neck (on hid squid Taningia danae Joubin, 1931, which may reach both sides) or above the nuchal cartilage, under the neck 124 kg (González et al. 2003) is one such poorly studied collar and were often associated with incisions. These cuts deep-sea species. Recently, one live specimen was photo- ranged from 30 to 65 mm in length and were probably graphed (Kubodera et al. 2007), but otherwise the species is made by males, using the beak or arm hooks. This is the mainly known from the stomach contents of sperm whales Wrst time wounds facilitating spermatangium storage have and sharks (Clarke 1996). Descriptions in the literature of been observed in the internal muscle layers (rather than trawl-caught, fresh material include only two mature males, external, as observed in some other species of squid). The two mature females, two maturing females and 20 juveniles implications of these observations for the mating behavior (Okutani 1974; Roper and Vecchione 1993; Santos et al. of the rarely encountered squid T. danae are discussed. 2001; González et al. 2003; Quetglas et al. 2006). This study presents the Wrst detailed information on sperm transfer and storage in T. danae. Introduction Reproduction in cephalopods is characterized by separa- tion of the sexes and semelparity, i.e., gonad maturation Some deep-sea squid are rarely encountered, and the biology and spawning (although sometimes protracted), occur once of many species remains poorly understood. Observations of at the end of the animal’s life (Nesis 1987). Spermatozoa live specimens are even rarer, and the examination of dead are packed into complex spermatophores, which are trans- ferred to the female by the hectocotylus (a modiWed arm) or, in species lacking a hectocotylus, by a long terminal Communicated by U. Sommer. organ (an extension of Needham’s sac, the storage organ for spermatophores) (Nesis 1995). During mating, the sper- H. J. T. Hoving (&) · J. J. Videler matophore is transferred and then everts after initiation of Ocean Ecosystems, Centre for Ecological and Evolutionary Studies, University of Groningen, P.O. Box 14, the ‘spermatophoric reaction’ (reported in Loligo pealei by 9750 AA Haren, The Netherlands Drew (1919), Octopoteuthis sicula by Hoving et al. (2008b) e-mail: [email protected] and Todarodes paciWcus by Takahama et al. (1991)). This reaction begins when the spermatophore is removed from M. R. Lipinski Department of Environmental AVairs and Tourism, the Needham’s sac by the hectocotylus; in unhectocotylized Private Bag X2, Roggebaai 8012, Cape Town 8000, South Africa species, the distal tip of the long terminal organ triggers the reaction as the spermatophore exits its aperture (observed K. S. R. Bolstad in Onykia ingens by Hoving and Laptikhovsky (2007)). Earth & Oceanic Sciences Research Institute, Auckland University of Technology, The spermatangium, which is the sperm mass enveloped in Private Bag 92006, Auckland 1142, New Zealand an outer casing (the ‘inner tunic’ sensu Drew 1919), is then 123 394 Mar Biol (2010) 157:393–400 expelled from the spermatophore and deposited on the body into the arms, head and mantle has been reported for a vari- of the female. The remaining empty sheath of the spermato- ety of oceanic squid species (Nesis 1970, 1995; Clarke phore is lost. Spermatangium attachment locations and 1980; Okutani and Ida 1986; Norman and Lu 1997; Guerra mechanisms are species and family speciWc (Nesis 1995; et al. 2004; Jackson and Jackson 2004; Hoving et al. 2004, Hoving 2008); spermatangia may be attached at consistent 2008b; O’Shea et al. 2007; Bolstad 2008) including external sites on the female (the buccal membrane or man- T. danae (Clarke 1967; Okutani 1974), implanted sperma- tle) or in special seminal receptacles. In some species, sper- tangia associated with male-inXicted wounds have never matangia are deposited seemingly non-selectively over the been reported for this species. female’s exterior body surfaces (Nesis 1995; Hoving et al. 2004; Hoving 2008) and are often deeply implanted into the female’s tissues, while spermatangia deposited at speciWc Materials and methods consistent sites are generally superWcially attached (Nesis 1995). At Iziko Museums of Cape Town, nine specimens of In hectocotylized squids, the male probably holds evert- T. danae were examined from the stomachs of three sperm ing spermatophores against the preferred deposition site, whales commercially caught in South African waters oV and the spermatangia then attach to the female’s tissues. In Durban, between 1970 and 1973. Another twelve speci- species lacking a hectocotylus, the terminal organ positions mens, accessioned in the Museum of Natural History (Lon- the everting spermatophores. The exact mechanism by don), were examined; these specimens had been collected which spermatangia attach to and implant into female tis- from the stomachs of sperm whales caught in South African sues remains poorly understood. In some species, attach- waters between 1963 and 1965. After collection from the ment is aided by extensions on the oral side of the stomachs, all ex-sperm-whale specimens were stored in spermatangium, which penetrate the female’s tissues [e.g., 10% formalin and later transferred to ethyl alcohol. Todarodes paciWcus (Takahama et al. 1991) and Octopo- Although these specimens were not in good condition, their teuthis sicula (Hoving et al. 2008b)]. In some onychoteuth- anatomical features and organs could be diVerentiated. One ids, implanted spermatangia are associated with elongated additional specimen was examined from New Zealand exterior wounds on the female’s mantle (Torchio 1967; waters, caught August 26, 2003, by midwater trawl at Nesis 1970; Clarke 1980; Okutani and Ida 1986; Bolstad 365 m (Wshing both in midwater and on the bottom), 2008; Bolstad and Hoving submitted), which may be cre- between 41°59.1ЈS–170°35.6EЈ and 41°52.3SЈ–170°36.6ЈE. ated by the male’s beak (Torchio 1967). Although Norman This specimen is accessioned in the Museum of New and Lu (1997) speculated that Architeuthis sp. implants Zealand Te Papa Tongarewa under NMNZ M.284745. spermatangia deeply into female tissues under hydraulic Details of all mated females reported herein are given in pressure produced by the terminal organ, recent studies Table 1. have shown that some squid spermatangia implant autono- mously (Hoving and Laptikhovsky 2007; Hoving et al. 2009). Such autonomous implantation may be enabled or Results aided by proteolytic enzymes present in the spermato- phore’s cement body (Nesis et al. 1998). Mated Taningia danae from stomachs of sperm whales Fertilization occurs externally in squid, since spermatan- caught in 1970–1973 gia are stored outside of the perivisceral coelom and ovi- ducts (Hanlon and Messenger 1996). In loliginids, two Seven females (Table 1) bore bundles of spermatangia (dis- spermatangium storage sites exist—the buccal membrane charged spermatophores) or remains of spermatangia and the distal oviduct—and spawned eggs are passed along implanted in the mantle, nuchal region and nearby regions both sites for fertilization. The fertilization mechanisms in of the head and neck (Fig. 1). The spermatangia, and some oceanic squid remain unknown. tunics without sperm, were found in bundles of approxi- Taningia danae is one such species. Mature males, mately 20–40 (Fig.
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