Title Laboratory observations on Todarodes pacificus (Cephalopoda: Ommastrephidae) egg masses

Author(s) Bower, John R.; Sakurai, Yasunori

Citation American Malacological Bulletin, 13(1/2), 65-71

Issue Date 1996

Doc URL http://hdl.handle.net/2115/35242

Type article

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Hokkaido University Collection of Scholarly and Academic Papers : HUSCAP Laboratory observations on Todarodes pacificus (Cephalopoda: Ommastrephidae) egg masses

John R. Bower and Yasunori Sakurai Faculty of Fisheries, Hokkaido University, 3-1-1 Minato-cho, Hakodate, Hokkaido, 041 Japan

Abstract: Two egg masses of the ommastrephid squid Todarodes pacific us (Steenstrup, 1880) are described. Immature squid were collected from inshore waters of southern Hokkaido, Japan, and maintained in a raceway tank where they matured, mated, and spawned. Both gelatinous masses were spherical and nearly neutrally buoyant. The larger mass measured 80 cm in diameter and contained approximately 200,000 eggs. The egg-mass surface layer effectively prevented crustaceans, protozoans, and bacteria from infesting the masses. Paralarvae hatched after 4-6 days at 18-19°C and actively swam at once, with many individuals swimming at the surface. Both masses disintegrated soon after hatching. Paralarvae died approximately 6-7 days after hatch­ ing, presumably due to starvation.

Key words: reproduction, eggs, squid, Todarodes, Cephalopoda

The ommastrephid squid Todarodes pacificus Observation of the spawning of a captive (Steenstrup, 1880) is a commercially important resource in Todarodes pacificus female by one of us (YS) and our col­ Japan, occurring throughout Japanese coastal waters league Y. Ikeda in 1991 revealed that T. pacificus can pro­ (Okutani, 1983; Murata, 1989, 1990). Many studies have duce gelatinous egg masses that resemble those of captive focused on the fishery biology of T. pacificus (Murata et Iliex illecebrosus (LeSueur, 1821) (0' Dor and Balch, al., 1971, 1973; Tashiro et ai., 1972; Araya, 1976; Murata, 1985). This paper describes the second such spawning by 1978); little, however, is known about reproduction. captive T. pacificus and is the first published description of Ommastrephid squids, where known, generally pro­ a complete egg mass spawned by this species under labora­ duce large numbers of small eggs, encapsulated in gelati­ tory conditions. nous masses (O'Dor et ai., 1982a). Few records exist of naturally spawned eggs or egg masses from oceanic cephalopods (Sabirov et ai., 1987; Lapitkhovsky and MATERIALS AND METHODS Murzov, 1990), and there have been no observations of Todarodes pacificus egg masses in the natural habitat. [Egg On 1 September 1994, 20 immature squid (mean masses found near the Kuril Islands and south of Japan, and dorsal mantle length (DML) ca. 20 cm) were collected with attributed to T. pacificus by Akimushkin (1963) were pre­ automatic jigging machines and by hand jigging from the sumably misidentified (Kir Nesis, pers. comm.).] All infor­ inshore waters of Tsugaru Strait, southern Hokkaido, Japan, mation of this critical period of the life cycle comes from and transferred to the U suj iri Fisheries Laboratory, laboratory observations of spawning by captive T. pacificus. Hokkaido University. The squid were maintained in a fil­ Spawning in captivity by Todarodes pacificus was tered, recirculating raceway tank (5.5 m in length, 2.5 m in first observed by Hamabe (1961 a), who suggested that egg width, 1.2 m in depth, and 13,000 I in capacity). The main­ masses of T. pacific us are normally demersal, and either tenance procedure followed that described by Sakurai et al. attached to the sea bottom or deposited in crevices. (1993). The squid were maintained for 25 days at a mean Hamabe kept spawning females in small barrels anchored temperature of 17.3°C (range 15.8-18.5°C) while they on the sea bottom at depths of 5-20 m and obtained 15 egg matured and mated, and were fed a daily diet of frozen masses, with each mass containing 300-4,000 eggs. Pacific saury [Coioiabis saira (Brevoort, 1850)], and Hamabe (1963) further described broken and incomplete Japanese anchovy [Engrauiis japonicus (Temminck and masses spawned in small (volume < 0.13 m3) laboratory Schlegel, 1846)]. The maturity and condition of the squid tanks. were monitored daily.

American Malacological Bulletin, Vol. 13(1/2) (1996):65-71 65 66 AMER. MALAC. BULL. 13(1/2) (1996)

On 16 September, when mature eggs were first interior of the masses, which contained the eggs, consisted observed in the oviducts, all but four ripe females were of a jelly presumably secreted by the oviducal gland. removed from the tank. Water circulation was weakened The larger egg mass measured SO cm in diameter and aeration was turned off to prevent possible damage to and contained approximately 200,000 eggs (Fig. lA). egg masses. Two females spawned incomplete egg masses More than 90O/C of the eggs within the mass were fertilized, and died on 24 September, leaving two mature females. with localized areas of unfertilized eggs evident within the The DML of the two remaining females measured 26.S cm mass. Infertile eggs were translucent. One side of the mass and 27.0 cm. Two egg masses were discovered on the was damaged, and the jelly forming the surface layer was morning of 2S September. The masses were maintained a missing in this area; eggs from the inner core appeared to mean temperature of IS.7°C (range IS.3-19.2°C). To facil­ exude from this area. The smaller egg mass measured 40 itate the moving, viewing, and photographing of the mass­ cm in diameter and contained approximately 21,000 eggs. es, the smaller mass was held in a plankton-net container Percent fertilization of eggs within this mass was approxi­ with a plastic window, and the larger mass was held in a mately 9S%. All developing embryos within both station­ gill net (mesh size 49 mm in stretch length) suspended from ary masses underwent development in a vertical position, the surface. Both masses were photographed with a 3S-mm with the tail pointed upwards. Eggs were positioned 0.4- camera and videotaped with a Sony CCD-VSOOO video 2.0 cm apart throughout the inner mass. The chorion sur­ camera and an Olympus endoscope. Distances between rounding each egg expanded to diameters of 1.9-2.3 mm eggs and fertilization rates within each mass were deter­ before hatching. mined from the videotaped recordings. The mean inter-egg Examination of the egg-mass surface layer distance was used to estimate the total number of eggs in revealed that the outer nidamental-gland jelly was effective each mass. in preventing crustaceans, protozoans, and bacteria present Daily observations were made of the paralarvae. in the tank from in festing the egg masses (Fig. I B). Feeding was not attempted. Individuals were removed Sections of the larger mass where the outer jelly was dam­ daily for future scanning electron microscopic and statolith aged or missing were quickly infested by bacteria and pro­ analysis. Paralarvae were maintained at a mean tempera­ tozoans. Fragments of nidamental-gland jelly with attached ture of IS.SoC (range IS.4-19.2°C). eggs, presumably from the large mass or a previous failed spawning, were also seen floating at the surface. The buoy­ ancy of these fragments was due to embedded air bubbles RESULTS from the tank's water circulation system. Most of these eggs were quickly infected and died. Spawning females The small and large egg masses completely disin­ About two days before spawning, the two females tegrated six and seven days after spawning, respectively stopped feeding and often rested on the tank bottom. While (Fig. 2). After disintegration, pieces of the surface-layer resting, the females' chromatophores flashed rapidly over jelly were found on the bottom of the tank. Several pieces the entire body surface in a characteristic, incandescent pat­ with a few unhatched eggs attached and with embedded air tern that is indicative of imminent spawning (YS, pers. bubbles were found floating at the surface. obs.). This behavior continued through spawning. Both females died within 12 h after spawning. Postmortem Paralarvae examination of the oviducts revealed neither female Hatching occurred 4-6 days after spawning at ca. spawned all of her eggs. The 27-cm and 26.S-cm DML 19°C. This development rate was similar to that described females had approximately 110,000 eggs and 93,000 eggs, by Hamabe (1961 b) for Todarodes pacificus (4-S days at respectively, remaining in the oviducts after spawning. The IS-20°C). The DML of hatchling paralarvae measured 1.1 anterior ends of the nidamental glands from both females mm. At hatching, paralarvae appeared to swim vertically were attenuated and slightly translucent. out of the egg masses. Once free, they swam freely in the tank, with many at the surface. No paralarvae appeared to Egg masses remain within either mass after hatching. Both spherical egg masses were nearly neutrally Two general swimming patterns were seen. Many buoyant and found floating near the surface. Both were paralarvae followed a general pattern of slow ascent from attached to fragments of previously spawned incomplete midwater in the tank until they reached the surface, where masses floating at the surface. The two layers of the egg they swam in circular or random patterns at the surface. mass described by Hamabe (l961a, 1963) were clearly visi­ These paralarvae spent a long period swimming at the sur­ ble. Externally, the masses were covered with a jellylike face, after which they would cease swimming and sink secretion, presumably from the nidamental gland, and the from the surface. Another pattern seen in several paralar- BOWER AND SAKURAI: EGG MASSES OF TODARODES PACIFICUS 67

Fig. 1. Egg masses of Todarodes pacificus. A. The floating 80-cm-diameter spherical egg mass spawned in a laboratory tank. Positive buoyancy was due to attached fragments from previously spawned masses floating at the surface. Note the two dead spawned females on the tank bottom. Scale bar = 50 cm. B. Top surface of the 40-cm-diameter egg mass. Crustaceans, protozoans and bacteria visible on the outer nidamental-gland jelly layer of the egg mass could not infest the egg mass. Scale bar = 5 mm. 68 AMER. MALAC. BULL. 13(1/2) (1996)

Fig. 2. Time series showing the 80-em-diameter egg mass held in a gill net suspended from the surface. Scale bar = 50 em (A-F). A. 2 days after spawning. B. 3 days after spawning. C. 4 days after spawning. D. 5 days after spawning. E. 6 days after spawning. F. 7 days after spawning. Arrows indicate outline of egg mass. BOWER AND SAKURAI: EGG MASSES OF TODARODES PACIFICUS 69 vae was a slow ascent to the surface, cessation of swimming Egg masses once the surface was reached, followed by immediate sink­ Our observations demonstrate that Todarodes paci­ ing. Feeding by the paralarvae was not observed. ficus can produce nearly spherical egg masses up to 80 cm Paralarvae swam with rapid mantle contractions of ca. 125 in diameter, with ca. 200,000 eggs. Hamabe (1961 a) beats per minute (normal adult rate = 75 beats per minute). obtained 15 small egg masses, with each mass containing While swimming at the surface, many paralarvae had 300-4,000 eggs, however, the small size of the barrels used unidentified particles stuck to their mantle surface. Two during his experiment (barrel length = 50 cm; barrel inner paralarvae were also seen swimming with mucus strands diameter = 33 cm) presumably prevented the formation of a approximately 2 cm in length trailing from the mantle sur­ complete mass. face. Egg masses formed by Todarodes pacificus resem­ No pattern of phototaxis was seen; paralarvae were ble those formed by the ommastrephid Illex illecebrosus found at the surface in uniform numbers both day and night. (Durward et ai., 1980; O'Dor and Balch, 1985). Percent When we shined lights directly on the paralarvae at the sur­ fertilization within the T. pacificus masses, however, was face while photographing, however, the paralarvae avoided significantly higher than the maximum of 40% reported for the strong light by sinking in a somersault motion. 1. illecebrosus egg masses (O'Dor et ai., 1980). The main Paralarvae at the surface displayed positive rheotaxis when difference during spawning between these species is the a weak flow was generated from a bubbling stone. manner in which fertilization occurs. During egg-mass for­ Paralarvae died approximately 6-7 days after mation by T. pacificus, sperm from the seminal receptacles, hatching, presumably due to starvation. located on the buccal membrane, must pass through the nidamental gland jelly and mix with the oviducal jelly and eggs in the inner layer of the egg mass. An uneven flow of DISCUSSION sperm from the seminal receptacles to the egg mass could account for the localized variability in fertilization rates Spawning females within the large egg mass. In contrast, I. illecebrosus has The observed resting behavior on the bottom by no seminal receptacles, and fertilization occurs when mature females before spawning appears to support females form a mixture of concentrated jelly (nidamental Hamabe's (l961a, 1963) suggestion that Todarodes pacifi­ and oviducal), eggs and broken spermatophores within the cus is a demersal spawner. The female observed by mantle cavity (Durward et ai., 1980). Hamabe spawned while resting on the bottom of a barrel. A notable difference in embryonic development Such resting behavior has been reported in other neritic rates was found between Todarodes pacificus eggs that ommastrephids (Bradbury and Aldrich, 1969; Boletzky et developed within an egg mass and those reared by artificial ai., 1973; O'Dor and Balch, 1985; Vecchione and Roper, fertilization. Hatching from the egg masses occurred 4-6 1991; Young, 1995). However, while spawning could occur days after spawning at ca. 19°C. This developmental rate near the bottom in shallow inshore waters, T. pacificus like­ was approximately one day longer than that for T. pacificus ly spawns at the same depths when over deep waters, which paralarvae reared by artificial fertilization at the same tem­ would ensure that the nearly neutrally buoyant egg masses perature (Sakurai et ai., 1996). O'Dor et ai. (l982b) also are maintained in the warm surface layer, where tempera­ reported delayed hatching from Illex illecebrosus egg mass­ tures are adequate (above 12oC; Sakurai et at., 1996) for es. The longer developmental period within egg masses normal embryonic development. The delicate nature of the suggests that animals reared by artificial fertilization might masses indicates that they are not attached to the sea bot­ hatch at a premature stage. Watanabe et al. (1996) con­ tom, as Hamabe proposed. firmed that artificially fertilized T. pacificus eggs hatched Our findings suggest that captive post-spawning approximately two developmental stages earlier than eggs females die with many eggs still remaining within their within the egg masses (stage criteria defined by Watanabe). oviducts. Such incomplete spawning is common in captive, The enveloping oviducal-gland and nidamental-gland jellies spawned females (Ikeda et ai., 1993). In Novembet 1994, a of the egg masses presumably reduce mechanical stimula­ pre-spawning female (DML = 26.8 cm) had ca. 304,000 tion of developing embryos, a cause of premature hatching eggs within her oviducts (lB, pers. obs.). This count is in some cephalopods (Choe, 1966). comparable to the figures of Soeda (1956), who estimated the fecundity of Todarodes pacificus to be between 320,000 Paralarvae and 470,000 eggs. Future fecundity estimates of T. pacifi­ Durward et al. (1980) suggested that ommas­ cus must consider that females do not necessarily spawn all trephid paralarvae might feed on microorganisms and eggs before dying. plankton that colonize the egg mass. We saw no evidence of any feeding by the paralarvae within the egg mass after 70 AMER. MALAC. BULL. 13(1/2) (1996) hatching, however the longer developmental time within the Hamabe, M. 1961 a. [Experimental studies on breeding habit and develop­ egg mass indicates greater opportunity for developing ment of the squid, Ommastrephes sloani pacijicus Steenstrup. 2. Spawning behavior.] Zoological Maga~ine 70(11 ):385-394. [In embryos to absorb organics from the oviducal gland jelly. Japanese with English summary]. Hatching paralarvae swim upward immediately, Hamabe, M. 1961 b. [Experimental studies on breeding habit and develop­ with many animals found concentrated at the surface. ment of the squid, Ommastrephes sloani pacijicus Steenstrup. 3. Much biological emphasis has been placed on the surface Early embryonic development and morphlogical [sic] features of film of organic matter in the sea (e. g. Sieburth et al., 1976). the larvae immediately after hatching.] Zoological Maga~ine 70(11 ):408-419. [In Japanese with English summary]. Dissolved and particulate organic matter concentrations are Hamabe, M. 1963. [Spawning experiments of the common squid, significantly higher in the thin layer at the sea surface than Ommastrephes sloani pacijicus Steenstrup, in an indoor aquari­ in bulk seawater (Liss, 1975; Hunter and Liss, 1981). The um.] Bulletin of the Japanese Society of Scientific Fisheries possibility that cephalopods can use dissolved organic mat­ 29(10):930-934. [In Japanese with English summary]. ter as a nutrition source has been proposed by Hanlon et al. Hanlon, R. T., P. E. Turk, and P. G. Lee. 1991. Squid and cuttlefish mari­ culture: an updated perspective. Journal of Cephalopod Biology (1991). Several studies have published evidence in support 2(1):31-40. of this hypothesis (Castille and Lawrence, 1978; Vecchione Hunter, K. A. and P. S. Liss. 1981. Organic sea surface films. In: Marine and Hand, 1989). Further investigation of uptake of dis­ Organic Chemistry, E. K. Duursma and R. Dawson, eds. pp. 259- solved organics is needed, especially in the case of ommas­ 298. 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