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Development of the Ommastrephid Squid Todarodes Pacificus, from Fertilized Egg to the Rhynchoteuthion Paralarva

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Development of the Ommastrephid Squid Todarodes Pacificus, from Fertilized Egg to the Rhynchoteuthion Paralarva Title Development of the ommastrephid squid Todarodes pacificus, from fertilized egg to the rhynchoteuthion paralarva Author(s) Watanabe, Kumi; Sakurai, Yasunori; Segawa, Susumu; Okutani, Takashi Citation American Malacological Bulletin, 13(1/2), 73-88 Issue Date 1996 Doc URL http://hdl.handle.net/2115/35243 Type article File Information sakurai-23.pdf Instructions for use Hokkaido University Collection of Scholarly and Academic Papers : HUSCAP Development of the ommastrephid squid Todarodes pacific us , from fertilized egg to rhynchoteuthion paralarva Kunli Watanabel , Yasunori Sakurai2, Susumu Segawal , and Takashi Okutani3 lLaboratory of Invertebrate Zoology, Tokyo University of Fisheries, Konan, Minato-ku, Tokyo 108, Japan 2Faculty of Fisheries, Hokkaido University, Minatocho, Hakodate, Hokkaido 041, Japan 3College of Bioresource Sciences, Nihon University Fujisawa City, Kanagawa 252, Japan Abstract: The present study establishes for the first time an atlas for the normal development of Todarodes pacificus Steenstrup, 1880, from fertilized egg to rhynchoteuthion paralarva. In the course of the study, observations on embryogenesis and histological differentiation in T. pacificus were made for consideration of the developmental mode of the Oegopsida, which is a specialized group with a reduced external yolk sac. It appears that differentiation of the respiratory and digestive organs is relatively delayed in the Oegopsida, with reduction of the yolk sac as well as the egg size. These characters could be related to a reproductive strategy for paralarval dispersion in the open ocean. Key words: Todarodes pacificus, oceanic squid, development, rhynchoteuthion, yolk sac The pelagic squid, Todarodes pacificus Steenstrup, atlas of stages. 1880, is distributed all around Japan and its neighboring The development of a technique of artificial fertil­ waters, extending from the northern part of the Kurile ization for ommastrephid squids (Sakurai and Ikeda, 1992; Islands south to Hong Kong (Okutani et ai., 1987; Okutani, Ikeda et al., 1993; Sakurai et al., 1995) has made it possible 1995). This squid is one of the most commercially impor­ to examine the embryonic development and early life stages tant cephalopods in Japan. Knowledge of the early life his­ of Todarodes pacificus. In the present study, embryogenesis tory of T. pacificus would provide basic information for and histological differentiation of T. pacificus were fishery biology. It would also be invaluable in the analysis observed in artificially fertilized eggs, and a complete atlas of the phylogeny of the Cephalopoda by clarifying the of developmental stages was established for the first time. embryogenesis of an oegopsid species that has seldom been Comparisons are made with several other species of the previously pursued by researchers. Oegopsida (Ommastrephidae, Enoploteuthidae, and There are only a few embryological studies on the Thysanoteuthidae), Myopsida, and Sepioida (Watanabe, Oegopsida, despite the many embryological studies on the unpub.) to characterize the developmental mode of oceanic Myopsida (e. g. Naef, 1928; Arnold, 1965, 1990; Segawa, oegopsids. 1987; Segawa et ai., 1988; Baeg et ai., 1992) and Sepioidea (e. g. Naef, 1928; Yamamoto, 1982). Soeda (1952, 1954) MATERIAL AND METHODS and H. Hayashi (1960) observed the embryonic develop­ ment of Todarodes pacificus from artificially inseminated Artificial Fertilization and Cultivation eggs, and described only a part of the development because embryonic development became abnormally arrested. Fertilized eggs of Todarodes pacificus were Hamabe (1961, 1962) described and illustrated the embry­ obtained by artificial fertilization using the method onic development of T pacificus without defining develop­ described by Sakurai et al. (1995). Female squids were cap­ mental stages. Naef (1928) proposed the developmental tured in the waters near Hakodate, Hokkaido, and main­ stages for one ommastrephid species (as ommastrephid Y), tained in a tank at the Usujiri Fisheries Laboratory of subsequently identified as Iliex coindetii (Verany, 1837) Hokkaido University until they reached maturity. Ova were (Boletzky et ai., 1973), but the stages were separated by obtained by dissecting the oviducts of a sacrificed female. large intervals and applied only after organogenesis. Recent Sperm masses were dissected from the seminal receptacles observations of the embryonic development of I. illecebro­ in the labral area of the same female and suspended in fil­ sus were made by O'Dor et ai. (1982) without providing an ter-sterilized, aerated seawater. After the sperm-seawater American Malacological Bulletin, Vol. 13(l/2) (1996):73-88 73 74 AMER. MALAC. BULL. 13(1/2) (1996) mixture was added to the ova, freeze-dried oviducal gland egg shape became spherical, measuring ca. 0.74 mm in powder, which had been dissolved in seawater beforehand, diameter. The embryos took 90-95 hr at 20°C to develop was added and mixed with the ova in a petri dish. The eggs from fertilization to hatching in vitro and the mean mantle were divided into groups of 15-20 per petri dish (60 mm in length of hatchlings was 0.95 mm. diameter) filled with filter-sterilized, aerated seawater. The After hatching, paralarvae were maintained for up seawater in each petri dish was changed twice daily. The to ca. seven days without being fed while the internal yolk fertilized eggs were incubated at 17°,20°, and 23°C, on the was completely absorbed. Paralarval mantle length mea­ advice of Sakurai et al. (1996) who reported that the peak sured 1.25 mm on the seventh day. The proboscis started to of embryonic survival rates occurred between 14.7° and grow on the second day after hatching. The length of the 22.2°C. At each temperature unit, about 1,000 eggs were proboscis from the anterior edge of the eyes was 0.27 mm incubated for morphological and histological observations. on the third day and 0.49 mm on the seventh day, respec­ tively. Arms III were not yet differentiated seven days after Observation of Development and hatching. Determination of Stages In artificially fertilized eggs, hatching occured at Observations were made of developing embryos stage 26, whereas eggs that developed within the egg mass under a light microscope and an atlas of developmental spawned in the tank hatched at stage 28. stages was prepared. Regular stages were identified mainly from embryos incubated at 20°C and supplementary obser­ Fertilization and Meiosis (Figs. 1 and 5) vations at either 17° or 23°C were made for stages 9, 10, Stage 1 (Stage 1 of Arnold), 10 min after insemina­ 11, 19,20,21, and 25. tion: Fertilization. Following fertilization, perivitelline To discriminate the developmental stages, the criter­ space expands and egg shape changes from ovoid to spheri­ ia established by Naef (1928) for ommastrephid Y and cal. Micropyle is visible at the animal pole. Arnold (1965, 1990) for Loligo were used. In the following Stage 2 (Stage 2), 30 min: First maturation division. description in the Results section, Arabic stage numerals in First polar body appears close to the animal pole. brackets represent the stages of Arnold (1965, 1990) and Stage 3 (Stage 3), 1.5 hr: Second maturation divi­ Roman stage numerals represent the stages of Naef (1928). sion. Second polar body appears next to the first. Polar bod­ Developmental stages were defined to seven days ies are visible until stages 12 or 13. Blastodisc appears and after hatching, because many organs were differentiated increases in size. The blastodisc area is more transparent after hatching. Measurements and means were taken on at than the ooplasmic area. least ten live animals. Cleavage (Figs. 1 and 5) Observation of Hatchlings from an Egg Mass Stage 4 (Stage 4), 2.6 hr: First cleavage. The furrow In addition to artificially fertilized eggs, newly occurs at the center of the blastodisc running beneath the emerged hatchlings from an egg mass spawned in a tank at polar bodies and extending to the equator of the egg. the Usujiri Fisheries Laboratory of Hokkaido University on Stage 5 (Stage 5), 3.7 hr: Second cleavage. Second 30 September 1994 (Bower and Sakurai, 1996) were inves­ furrow occurs across the first one at right angle and divides tigated. Eggs within the large spherical egg mass were sur­ the first cells into anteriorly, where the polar bodies are sit­ rounded by a large quantity of nidamental and oviducal uated, and posteriorly located segments. gland jelly. Stage 6 (Stage 6), 4.5 hr: Third cleavage. The cells are divided differently in the anterior half and the posterior Histological Observation half. In the posterior half, the furrow slants, almost parallel to the first one, while in the anterior half it extends radially Histological sections were prepared by fixing the pulling the second one forward. specimens in Bouin's fixative, embedding in paraffin, sec­ Stage 7 (Stage 7), 5.0 hr: Fourth cleavage. Inner tioning, and staining with haematoxylin and eosin. four cells are established as blastomeres while the sur­ rounding 12 cells remain contiguous at their outer margins as blastocones. RESULTS Stage 8 (Stage 8), 5.5 hr: Fifth cleavage; 32 cells (14 blastomeres and 18 blastocones). ATLAS OF DEVELOPMENT Stage 9 (Stage 9), 4.5 hr at 23°C: Sixth cleavage. Ova were ovoid in shape, and measured ca. 0.83 x The cells divide asynchronously and finally become 64 0.70 mm before fertilization. Following fertilization, the cells. A group of eight very small cells exists near the cen- WATANABE ET AL.: EMBRYONIC DEVELOPMENT OF TODARODES PACIFICUS 75 ps lkIfertized L Stage 1 L Stage 2 L Stage 3 L pb Stage 4 L 4A Stage S L SA Stage 6 L 6A Stage 7 L 7A Stage S L SA Stage 9 L 9A rc Stage 10 A 10 L Stage 11 L Stage 12 L Fig. 1. Development of Todarodes pacificus, from fertilized egg to Stage 12 embryo. A or L with stage number indicates apical or lateral view. Egg mem­ brane is omitted from Stage 4.
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