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Embryonic and Larval Development of the Trochid Gastropod Umbonium Moniliferum Reared in the Laboratory

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Embryonic and Larval Development of the Trochid Gastropod Umbonium Moniliferum Reared in the Laboratory VENUS 63 (3-4): 135-143, 2005 Embryonic and Larval Development of the Trochid Gastropod Umbonium moniliferum Reared in the Laboratory Kazuyuki Harada1, Satoshi Ohashi2, Akihiko Fujii2 and Akio Tamaki1,* 1Marine Research Institute, Nagasaki University, Taira-Machi 1551-7, Nagasaki 851-2213, Japan; *[email protected] 2Nagasaki Prefectural Institute of Fisheries, Taira-Machi 1551-4, Nagasaki 851-2213, Japan Abstract: The embryonic and larval development of the trochid gastropod Umbonium moniliferum (Lamarck, 1822) is described, based on material reared in filtered seawater at 22.6-25.1°C in the laboratory. Fertilized eggs were obtained via artificially induced spawning of adults collected from an intertidal sandflat in southern Japan in October 2002. Each egg was 170 µm in diameter, surrounded by a vitelline membrane and a gelatinous coating. The trochophore larvae hatched at 6 h after fertilization, and became veliger larvae at 8 h, with the completion of the velum. At 48 h, the larvae began to crawl on the substratum and swim in the water column alternately. Metamorphosed larvae (= juveniles) of 200-µm shell width appeared at 200 h, with the velum lost. This was induced by the provision of sediment inhabited by adults and seawater agitation. The reported time for larvae of the other two congeneric species to reach the metamorphosis is shorter [48 h in U. vestiarium (Linnaeus, 1758) at 28-30°C; 3 d in U. giganteum (Lesson, 1833) at 20°C]. The longer time required in the present case could reflect delayed metamorphosis due to lack of more appropriate stimuli. Keywords: Umbonium moniliferum, embryo, larva, morphology, laboratory culture Introduction In Japanese waters, the trochid gastropod, Umbonium moniliferum (Lamarck, 1822) (subfamily Umboniinae) is a common member of the benthic infaunal community on lower intertidal sandflats. The population density of U. moniliferum often becomes remarkably high, accompanied by an assemblage of predators, ectoparasites, and inhabitants of empty shells (Nojima et al., 1980; Ozawa, 1981; Nishino et al., 1983; Tamaki & Kikuchi, 1983; Shimoyama, 1985; Kikuchi & Doi, 1987; Tamaki, 1994; Asakura, 1995; Flach & Tamaki, 2001). Although several life history studies have been conducted for U. moniliferum (Nishino et al., 1983; Shimoyama, 1985; Tamaki, 1994; Asakura, 1995), they were limited to its benthic stage, with no information on the biology and ecology of the larva. Even when all species of Umbonium are considered, only two brief descriptions have been given of the embryonic and larval development. Berry (1986) described the early development of U. vestiarium (Linnaeus, 1758) inhabiting a sandy beach in Penang, Malaysia, but with no illustrations. Ohata et al. (2002) gave a description of U. giganteum (Lesson, 1833) inhabiting a shallow subtidal sand bottom off the Boso Peninsula in central Honshu, Japan, with a number of photographs only. The aim of the present paper is to give a detailed account of the embryonic and larval development of U. moniliferum reared in the laboratory. Materials and Methods Collection of adult gastropods and induction of spawning Several hundred adult Umbonium moniliferum were collected from an intertidal sandflat in Kyushu, southern Japan (Tomioka Bay; sandflat located at 32°31´ N, 130°02´ E) during low tide 136 K. Harada, S. Ohashi, A. Fujii & A. Tamaki Embryonic and Larval Development of Umbonium moniliferum 137 5 A B 3 C D E on 8 and 21 October 2002. The spawning season of U. moniliferum on this sandflat is from the 4 end of September to early November (K. Harada & A. Tamaki, in preparation). The seawater temperatures just below the low tide line on the two collection dates were 24.5°C and 23.4°C, respectively. To induce spawning of the gastropods, several stimuli were given sequentially in the 2 field and laboratory, following the method by Kikuchi & Uki (1974) developed for the induction 1 of spawning in abalones. The gastropods were wrapped in several seawater-soaked paper towels in the field and transported to the laboratory, being kept in a sealed styrene foam box for 3 h. Then F 6 G H I J 8 each of the equally divided half batches of gastropods on each sampling date was maintained in a 13 12 10 container with 3 l of filtered seawater at room temperature, which was gently aerated (10 ml/min). After a while, each group of the gastropods was transferred to an aquarium filled with 20 l of filtered (through sand with 100-µm interstitial openings) seawater with no aeration, to which 7 7 11 7 7 9 9 another combination of stimuli was given. Running filtered seawater was irradiated by ultraviolet rays of 253.7 nm wave length, using a UV-irradiating device (FLONLIZER: Chiyoda-Kohan L' 18 18 2 K L M N Corp., Japan), which gave energy to the seawater at a rate of 930,000 µW·s/cm . At the same time 12 14 16 19 the seawater temperature was adjusted to be higher than that in the aquarium seawater by 2 to 17 } 12 { 3°C, using heating-cooling equipment (TS-2200ESO-6H: Yamaichi Corp., Japan). The aquarium 14 seawater was continuously replaced by this running seawater at a rate of 10 l/min for 15 or 30 15 20 min, during which checks were made for the occurrence of spawning. After a 30-min cessation, 15 the supply of running seawater was resumed. This set of stimuli was repeated several times. 7 The adult gastropods collected on 8 October were stimulated by placement in still seawater at O 21 P 23 Q 26 R 28 19 room temperature (21.4 to 22.5°C) for 15 h and subsequent exposure to ultraviolet ray-irradiated } } seawater for a total of 125 min. The seawater temperature was raised from the initial value of 22 22.5°C to a final one of 27.0°C, but this induced no spawning. After being given a second set 24 27 of stimuli (still seawater for 18 h and ultraviolet ray-irradiated seawater with an increase in 24 temperature from 22.8 to 25.0°C for a total of 120 min), some gastropods began to spawn at 11:00 25 on 10 October. The eggs were isolated demersal ones. Tens of thousands of fertilized eggs were collected (Batch A). A third and fourth set of stimuli were given to these adult gastropods several S 29 30 T hours later and one day later, respectively, each comprising a 30 min exposure to ultraviolet ray- 28 irradiated seawater together with an increase in temperature from 23.0 to 25.0°C or from 22.5 to 25.0°C. They spawned at 18:30 on 10 October and at 14:00 on 11 October, and several tens of 100 µm 100 µm 100 µm fertilized eggs were collected on both occasions (Batch B, B´). The adult gastropods collected on A - F G - J K - T 21 October were stimulated by still seawater for 15 h and ultraviolet ray-irradiated seawater with an increase in temperature from 22.0 to 25.0°C for 90 min. They spawned at 11:00 on 22 October, and several thousands of fertilized eggs were collected (Batch C). Fig. 1. Embryos and larvae of Umbonium moniliferum arranged chronologically (Table 1). Note that almost all velum cilia are omitted in illustrations M - S. A. Single-celled embryo just after fertilization (1. Treatment of fertilized eggs and rearing of larvae vitelline membrane; 2. gelatinous coating). B. Single-celled embryo with polar bodies (3. first polar body; First, the fertilized eggs from Batches A and C were washed to remove excess sperm. 4. second polar body). C. Two-celled embryo. D. Four-celled embryo. E. Gastrula embryo (5. prototrochal To isolate the eggs from the adults, the seawater in the aquarium was transferred to another cilia). F. Trochophore larva within vitelline membrane (6. prototroch). G. Trochophore larva just after hatching out (7. rudimentary protoconch). H. Veliger larva before completion of protoconch (8. velum; aquarium of the same type by siphoning. Ten minutes later the eggs had sunk to the bottom, 9. larval retractor muscle; 10. granular substance). I. Veliger larva before completion of protoconch (11. and the supernatant was decanted off. This procedure was repeated three times. The larvae from attachment of visceral mass to protoconch). J. Veliger larva before completion of protoconch, with first Batch A were maintained within a cylindrical nylon bag (87 cm in diameter × 65 cm in height 90° torsion (12. foot, 13: mantle). K. Veliger larva with completed protoconch, with second 90° torsion. with 100-µm openings) hung in a polycarbonate tank (150 cm in diameter × 80 cm in height) L, L´. Veliger larva with completed operculum (14: setae on tips of future metapodium, 15: operculum). containing 1,000 l of filtered (through polypropylene filter with 1-µm openings) seawater at room M. Veliger larva with swollen cephalic tentacles (16: cilia on foot, 17: cilia on dorsal part of body within mantle cavity, 18: cephalic tentacles). N. Veliger larva with swollen future propodium (19: propodium, temperature. No food was given. The seawater was continuously replaced by running filtered 20: metapodium). O. Veliger larva with elongated propodium (21: first process on tip of cephalic tentacle, seawater at a rate of 1.0 to 1.5 l/min. No aeration was supplied until most larvae reached the with setae, 22: statocyst). P. Veliger larva with second process on tip of cephalic tentacle (23: first and late veliger stage (between Figs. 1K and 1L) to avoid the possibility of inducing malformation. second processes on tip of cephalic tentacle, 24: first epipodial tentacle, 25: ciliary process on ceiling The seawater temperature and salinity varied from 22.6°C to 25.1°C and from 33.7 to 33.8, of mantle).
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