First Description of Developmental Processes in Sclerodactyla Multipes (Echinodermata: Holothuroidea: Dendrochirotida) from Misaki, Sagami Bay, Japan
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Plankton Benthos Res 16(3): 228–236, 2021 Plankton & Benthos Research © The Plankton Society of Japan First description of developmental processes in Sclerodactyla multipes (Echinodermata: Holothuroidea: Dendrochirotida) from Misaki, Sagami Bay, Japan Hisanori Kohtsuka1, Kohei Oguchi2, Yusuke Yamana3 & Masanori Okanishi1,* 1 Misaki Marine Biological Station, The University of Tokyo, 1024 Koajiro, Misaki, Miura, Kanagawa 238–0225, Japan 2 National Institute of Advanced Industrial Science and Technology (AIST), 1–1–1 Higashi, Tsukuba, Ibaraki 305–8566, Japan 3 Wakayama Prefectural Museum of Natural History, 370–1 Funo, Kainan,Wakayama 642–0001, Japan Received 15 September 2020; Accepted 30 April 2021 Responsible Editor: Shinji Shimode doi: 10.3800/pbr.16.228 Abstract: More than 100 individuals of sea cucumber larvae were collected in the Japanese coastal sea of Moroiso, Sagami Bay, Kanagawa Prefecture, central-eastern Japan, in January 2018. Based on an obtained sequence of mitochon- drial 16S rRNA gene region of one juvenile, it was identified as Sclerodactyla multipes by BLAST search with 0.3% genetic distance. The developmental process of the S. multipes was observed for three months, in which time, they grew from 250 µm to about 4 mm in length; here they showed distinct tentacles and dermal ossicles. Detailed morphological features of this species were described based on stereomicroscopic, fluorescence and SEM observations for the first time. This is the first description of life history through planktonic larva to juveniles in the family Sclerodactylidae. Key words: Sea cucumber, 16S rRNA, SEM, fluorescence microscope, larvae Sclerodactyla briareus (Lesueur, 1824) from the western Introduction Atlantic and S. multipes (Théel, 1886) from the western Although embryological studies on sea cucumbers Pacific (Théel 1886, Hendler et al. 1995, Imaoka 1995, (Echinodermata: Holothuroidea) have been provided for Kuramochi 2012). In these species, although a brief text- several commercially useful species, such as Apostichopus based description of development in S. briareus has been armata (Selenka, 1867), Athyonidium chilensis (Semper, published (Ohshima 1925), no embryological study accom- 1868), and Isostichopus fuscus (Ludwig, 1875) (Inaba & panied by photographs has been reported in this genus. Maruyama 1988, Hamel et al. 2003, Guisado et al. 2012, In this study, doliolaria and pentactula forms of the lar- Eguchi 2015, Huang et al. 2018), data for non-commercial vae of sea cucumbers were collected by towing plankton species are inadequate (Inaba & Maruyama 1988). The or- nets at the sea surface in Moroiso Bay, Miura Peninsula, der Dendrochirotida is a suspension-feeding sea cucumber Kanagawa Prefecture, Japan. We identified this species by world-widely distributed on the sea floor. The accumulated DNA sequences based on 16S rRNA gene region, and doc- biological knowledge of this order is important for fisheries umented the growth of its larvae using multiple observa- management and aquaculture of sea cucumbers, but its ear- tion methods. liest life stages are scarcely studied (Gianasi et al. 2018). Recently, studies on the earliest life stages of 61 species in Methods 32 genera of 5 families have been conducted, but only 15 species have been studied following the process of growth One hundred and ten individuals were collected on 5 from larvae to juvenile (Table 1). The genus Sclerodactyla January 2018, using a plankton net (diameter 60 cm, mesh (Sclerodactylidae: Dendrochirotoda: Actinopoda) includes size 0.33 mm, net length 150 cm) towed at the sea surface for 5 min at Moroiso Inlet (35°09.405′N.139°36.345′E), Mi- * Corresponding author: Masanori Okanishi; E-mail, mokanishi@ ura Peninsula, Kanagawa Prefecture (Fig. 1). tezuru-mozuru.com Larvae of sea cucumbers were housed in a cylindrical First description of developmental processes in Sclerodactyla multipes (Echinodermata: Holothuroidea:Dendrochirotida) from Misaki, Sagami Bay, Japan Table 1. Summaruy of developmental studies of dendrochirotid sea cucumbers. “̶” means no data. Spawning Unfertilized egg Fertilized egg Time and maximum size Type of Order Family Species Remarks Reference reproduction Period Observation Observation Size Observation Size Floating larva Pentactula Juvenile Dendrochi- Cucumari- Aslia lefevrei (Barrois, 1882) Lecithotrophic Jan–May ○ ○ ̶ ○ 400– 6 days, 7 days, 6–8 weeks, ̶ Costelloe 1985, 1988, rotida idae larva 650 µm 650 µm, 700 µm 3,500 µm Thorson 1946 Doliolaria Athyonidium chilensis (Sem- Lecithotrophic ̶ ○ ○ ̶ ○ 360 µm 5 days, 7 days, 21 days, ̶ Guisado et al. 2012 per, 1868) larva 433 µm, 629 µm 689 µm Vitellaria Benthophyllophorus conchil- Asexual reproduc- May ̶ ̶ ̶ ̶ ̶ ̶ ̶ ̶ ̶ Deichmann 1922 egum (Pourtalès, 1868) tion: fission Cladodactyla crocea crocea Brooding Jan–Apr ̶ ○ 700 µm ̶ ̶ ̶ ̶ ̶ hermaphroditic. Thomson 1878 (Lesson, 1830) Cucumaria fallax Ludwig, Lecithotrophic ○ ○ ̶ ○ ̶ 3.75 days, 9.5–10.75 18–21 days, ̶ McEuen 1987, 1988 1875 larva 725 µm, days, 700– Doliolaria 600–710 µm 1,125 µm Cucumaria frondosa (Gun- Lecithotrophic Mar, June ○ ○ ̶ ○ 900 µm 8 days, 9–11 days, 46 days, ̶ Gianasi et al. 2018, nerus, 1767) larva 1,550 µm, 1,300 µm 1,400 µm Hamel & Mercier 1996, Vitellaria So et al. 2011 Cucumaria georgiana (Lam- Brooding ̶ ̶ ○ 1,000 µm ̶ ̶ ̶ ̶ ̶ ̶ Vaney 1925 pert, 1886) Cucumaria ijimai Ohshima, Brooding ̶ ̶ ○ 550 µm ̶ ̶ ̶ ̶ ̶ ̶ Hyman 1955, Ohshima 1915 1915 Cucumaria japonica Semper, ̶ Apr–Junu, ○ ̶ ̶ ○ 500 µm ̶ ̶ ̶ Each individual casts Levin 1995 1868 Sep–Oct 300,000 floating eggs. Cucumaria joubini Vaney, Brooding ̶ ̶ ○ 1,200 µm ̶ ̶ ̶ ̶ ̶ ̶ Hyman 1955, Vaney 1914 1925 Cucumaria miniata (Brandt, Lecithotrophic ○ ○ ̶ ○ 400– 3.5 days, 8–13 days, 29–30 days, ̶ McEuen 1987 1835) larva 500 µm 675–765 µm, 700–800 µm 875– Doliolaria 1,230 µm Cucumaria piperata (Stimp- Lecithotrophic ̶ ○ ○ ̶ ○ 480– 3.5 days, 8–9.5 days, 22–25 days, ̶ McEuen 1987 son, 1864) larva 601 µm 675–765 µm, 740–770 µm 925– Doliolaria 1,325 µm Cucumaria pseudocurata Brooding mid Dec– ○ ○ ̶ ○ 916– Just observed Just observed Just Gonochoric. McEuen 1987, Deichmann, 1938 early Janu 1,237 µm observed Rutherford 1977 Cucumaria vaneyi Cherbon- Brooding ̶ ̶ ̶ ̶ ̶ ̶ ̶ ̶ ̶ ̶ Hyman 1955 nier, 1949 Cladodactyla crocea crocea Brooding ̶ ̶ ̶ ̶ ̶ ̶ ̶ ̶ ̶ ̶ Hyman 1955 (Lesson, 1830) Echinopsolus koehleri Brooding ̶ ̶ ̶ ̶ ̶ ̶ ̶ ̶ ̶ ̶ Hyman 1955 (Vaney, 1914) Hemiocnus syracusanus ̶ Nov–Dec ̶ ̶ ̶ ̶ ̶ ̶ ̶ ̶ ̶ Lo Bianco 1899 (Grube, 1840) Incubocnus incubans (Cher- Brooding Apr ○ 500 µm Gonochoric. Cherbonnier 1972 bonnier, 1972) Leptopentacta panamica ̶ Jan? ̶ ̶ ̶ ̶ ̶ ̶ ̶ ̶ ̶ Deichmann 1941 Deichmann, 1941 Lissothuria antillensis Paw- Brooding all ○ 400 µm Miller 1985 son, 1967 Neoamphicyclus lividus Brooding Dec ○ 370 µm Hickman 1978 229 Hickman, 1962 H. Kohtsuka et al. 230 Table 1. Continued.Summaruy of developmental studies of dendrochirotid sea cucumbers. “̶” means no data. Spawning Unfertilized egg Fertilized egg Time and maximum size Type of Order Family Species Remarks Reference reproduction Period Observation Observation Size Observation Size Floating larva Pentactula Juvenile Ocnus glacialis (Ljungman, Brooding ̶ ̶ ○ 700 µm ̶ ̶ ̶ ̶ ̶ ̶ Mortensen 1894, 1879) Ludwig 1900 Ocnus planci (Brandt, 1835) Lecithotrophic Mar–Apr ̶ ̶ ̶ ̶ 500 µm ̶ ̶ ̶ ̶ Hyman 1955, Vaney larva 1925 Paraleptopentacta elongata Lecithotrophic Jan ○ ○ ̶ ○ 250– Doliolaria Just observed 22–25 days, In vitro observatipn. Chia & Buchanan 1969 (Düben & Koren, 1846) larva 350 µm 925– 1,325 µm Pawsonia saxicola (Brady & Lecithotrophic ̶ ̶ ̶ ̶ ̶ 400 µm ̶ ̶ ̶ ̶ Orton 1914, Thorson Robertson, 1871) larva 1946 Pentactella laevigata Verrill, Brooding ̶ ̶ ○ 1,500 µm ̶ ̶ ̶ ̶ ̶ ̶ Hyman 1955, Simpson 1876 1982 Pseudocnus echinatus (von Lecithotrophic June–Aug ○ ○ ̶ ○ 300– 2 days, 7 days ○ The pentactula has 5 Ohshima 1921 Marenzeller, 1882) larva 400 µm 500 µm, tentacles Doliolaria Pseudocnus grubii (von ̶ Nov–Dec ̶ ̶ ̶ ̶ ̶ ̶ ̶ ̶ ̶ Lo Bianco 1899 Marenzeller, 1874) Pseudocnus lamperti Brooding ̶ ̶ ○ 800 µm ̶ ̶ ̶ ̶ ̶ Hermaphroditic. Hyman 1955, Ohshima (Ohshima, 1915) 1915 Pseudocnus lubricus (Clark, Brooding Nov–Dec ○ ○ 1,050 µm ○ 877– 2 days, 7 days ○ The pentactula has 5 McEuen 1987, Engstrom 1901) 1,078 µm 500 µm tentacles. Gonochoric. 1982 Doliolaria Pseudopsolus macquariensis Brooding May–June ○ 1,800 µm Hermaphroditic. Simpson 1982 (Dendy, 1897) Psolicrux coatsi (Vaney, Brooding ̶ ̶ ̶ ̶ ̶ ̶ ̶ ̶ ̶ ̶ Hyman 1955 1908) Stereoderma imbricata Brooding ̶ ̶ ○ 1,200 µm ̶ ̶ ̶ ̶ ̶ ̶ Hyman 1955, Ohshima (Ohshima, 1915) 1915 Trachythyone parva (Lud- Brooding ̶ ̶ ○ 200 µm ̶ ̶ ̶ ̶ ̶ ̶ Hyman 1955, Clark wig, 1875) 1946 Phyllo- Pentamera chiloensis (Lud- ̶ ̶ ̶ ̶ ̶ ̶ ̶ ̶ ̶ 9,000 µm A record of juvenile. Deichmann 1941 phoridae wig, 1886) Pentamera populifera (St- Lecithotrophic Feb–Mar ○ ̶ ○ 339– 2.25 days, 6–7.5 days, 17 days? ̶ McEuen 1987 impson, 1864) larva 439 µm 550 µm, 490–600 µm Doliolaria Pentamera pulcherrima ○ ̶ ̶ ̶ ̶ ̶ ̶ ̶ ̶ McEuen 1988 Ayres, 1852 Phyllophorus (Phyllophorus) Brooding May–Aug ̶ ̶ ̶ ̶ ̶ ̶ ̶ ̶ ̶ Hyman 1955, Ludwig urna Grube, 1840 1898 Thyone benti Deichmann, Lecithotrophic Winter ̶ ○ 512– ̶ ̶ ̶ ̶ ̶ ̶ McEuen 1987 1937 larva? 560 µm Thyone inermis Heller, 1868 ̶ Oct–Nov ̶ ̶ ̶ ̶ ̶ ̶ ̶ ̶ Lo Bianco 1899 Psolidae Lissothuria nutriens (Clark, Brooding all ○ 600 µm Gonochoric. Wootton 1949 1901) Lissothuria ornata Verrill, Brooding ̶ ̶ ̶ ̶ ̶ ̶ ̶ ̶ ̶ ̶ Hyman 1955 1867 Psolidium incubans Ekman, Brooding ̶ ̶ ○ 640 µm ̶ ̶ ̶ ̶ ̶ ̶ Hyman 1955, Ekman 1925 1925 First description of developmental processes in Sclerodactyla multipes (Echinodermata: Holothuroidea:Dendrochirotida) from Misaki, Sagami Bay, Japan Table 1.