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Giant Spoon Worms Pumped out of Their Deep Burrows: First Collection of the Main Bodies of Ikeda Taenioides (Annelida: Thalassematidae: Bonelliinae) in 88 Years

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Giant Spoon Worms Pumped out of Their Deep Burrows: First Collection of the Main Bodies of Ikeda Taenioides (Annelida: Thalassematidae: Bonelliinae) in 88 Years Plankton Benthos Res 16(3): 155–164, 2021 Plankton & Benthos Research © The Japanese Association of Benthology Giant spoon worms pumped out of their deep burrows: First collection of the main bodies of Ikeda taenioides (Annelida: Thalassematidae: Bonelliinae) in 88 years Ryutaro Goto1,*, Yumi Henmi2, Yuto Shiozaki3 & Gyo Itani3 1 Seto Marine Biological Laboratory, Field Science Education and Research Center, Kyoto University, 459 Shirahama, Nishimuro, Wakayama 649–2211, Japan 2 Maizuru Fisheries Research Station, Field Science Education and Research Center, Kyoto University, Nagahama, Maizuru, Kyoto 625–0086, Japan 3 Graduate School of Kuroshio Science, Kochi University, 2–5–1 Akebono, Kochi 780–8520, Japan Received 11 May 2020; Accepted 27 November 2020 Responsible Editor: Shigeaki Kojima doi: 10.3800/pbr.16.155 Abstract: Ikeda taenioides (Ikeda, 1904) (Annelida: Thalassematidae: Bonelliinae) is the world’s longest spoon worm species, which possesses an extremely long tape-like proboscis with a striped color pattern and a large brownish red trunk. This species is endemic to the Japanese Islands and inhabits a deep vertical burrow in intertidal and subtidal sand flats. Their proboscis, which extends from its small burrow opening, has been frequently observed around Japanese coasts. However, sampling of the main body (i.e., trunk) has been extremely rare because it always stays within a deep part of the burrow. Here, we report the success of the sampling of two specimens of I. taenioides with trunks in two different localities of the Seto Inland Sea (i.e., Ohmishima and Hachi), Japan, in 2019 and 2020 using a yabby pump. This is the first sampling of the trunk of I. taenioides in 88 years after its last collection in Onomichi Bay in 1931. We described the trunk color and morphological characteristics of the two specimens, including the internal anatomy. The trunks of the two specimens showed different colors, that is, pale brown (Ohmishima) and deep brownish red (Hachi). However, they were not distinguished to the species level by the comparison of partial COI sequences, suggesting that I. taenioides has an intraspecific variation in trunk color. Despite the difference in the sampling seasons (Ohmishima: June, Hachi: February), both specimens included numerous ripe eggs. According to previous studies, those collected in November and December also included numerous ripe eggs. Taken together, I. taenioides may be reproductive through- out the year or have multiple reproductive seasons per year. Key words: dwarf male, Echiura, reproduction, ventral chaetae, yabby pump described species (WoRMS 2020) and comprises two sub- Introduction families, Thalassematinae (with two tribes Thalassematini Echiurans or spoon worms are a group of annelids that and Echiurini) and Bonelliinae (Goto et al. 2020). They have a cylinder-shaped trunk and a spoon-shaped probos- occur from intertidal to ultra-abyssal depths, and most of cis. They were previously treated as a separate phylum, them live inside burrows in the soft sediment on the sea- class, or subclass in Annelida (Newby 1940, Ruggiero et floor, although some live inside the crevices in the hard al. 2015, Goto et al. 2018). However, to reflect their phylo- substrata (e.g., rocks and dead corals) (Stephen & Edmonds genetic placement in Annelida as a sister group of Capitel- 1972, Goto 2017). lidae (Weigert et al. 2014, Andrade et al. 2015, Struck et al. Ikeda taenioides (Thalassematidae: Bonelliinae) is 2015), they are currently treated as the family Thalasse- a large echiuran endemic to the Japanese Islands (Ikeda matidae (Goto et al. 2020). This family contains about 190 1904, 1907). This species possesses an over 60-cm long trunk and an over 2-m long proboscis and has been consid- * Corresponding author: Ryutaro Goto; E-mail, [email protected] ered as the world’s largest spoon worm species (Nishikawa 2012, Goto et al. 2017). Perhaps, it may be more appro- 156 R. Goto et al. priate to regard it as the longest spoon worm species, as currence of I. taenioides in Onomichi Bay, the Seto Inland some echiurans species have a thicker trunk and may have Sea, with a photograph of an I. taenioides specimen. This more volume (e.g., Urechis caupo). Ikeda taenioides lives specimen contained a proboscis and part of the trunk. Al- in deep vertical burrows in intertidal or subtidal sand flats though Sato (1934) did not provide any information on this and extends its proboscis from a small burrow opening to specimen, it was found in the museum of Tohoku Univer- the sand flat surface in order to collect sediments contain- sity with the label “Ikeda taenioides (IK), Onomichi, Seto ing food particles (Ikeda 1901, 1904, Goto et al. 2017). March 22, 1931 H. Okada” by Prof. T. Nishikawa (T. Nishi- Ikeda taenioides has been reported around the Japanese Is- kawa, personal communication). We interpret that this la- lands, from the northern end of Honshu Island to the south- bel means that the specimen was collected by H. Okada in ern end of the Kyushu Island or to the Amami-Ohshima Is- Onomichi Bay, the Seto Inland Sea, on March 22, 1931. To land (see review in Oshiro et al. 2020). However, except for the best of our knowledge, these are all records of the col- old records from Moroiso (Ikeda 1901, 1904, 1907, Fuchita lection of I. taenioides specimens with their trunks. How- 1902) and Onomichi Bay (Sato 1934), all of these previous- ever, most of the specimens were lost. Only two specimens ly mentioned records are based on the observation or col- of I. taenioides have been located at the present: one was lection of the proboscis that is extended from the burrows. deposited at the University of Tokyo, corresponding to the This is because the trunk of I. taenioides always stays one collected by Dr. Ikeda on December 24, 1901, and within a deep part of the burrows and is thus extremely examined in Nishikawa (2002), and the other was depos- difficult to dig up. ited at Tohoku University, which was photographed in Sato Dr. Iwaji Ikeda collected two specimens with the trunk (1934). To understand the biology and morphology of this at Moroiso Bay, near Misaki Marine Station, University enigmatic worm species, further examination of new spec- of Tokyo, in Kanagawa, at night low tide on November 14, imens with the trunk is required. 1901, with his colleagues, which was the first collection In this study, we succeeded in collecting two new speci- of whole I. taenioides (Ikeda, 1901). According to Ikeda mens of I. taenioides with the trunk using a yabby pump in (1907), he described I. taenioides based on six specimens the intertidal sand flats in the Seto Inland Sea, Japan. This with trunks, which were collected in Moroiso Bay during is the first sampling of the main bodies of I. taenioides in a stay between October and November in 1901. We assume 88 years after the last one in Onomichi Bay. We assessed that these contained two specimens collected on Novem- the body color and morphological characteristics of the ber 14, 1901. Furthermore, Dr. Ikeda collected two more specimens. specimens of the full body of I. taenioides on December 24, 1901 (Fuchita 1902), one of which is probably the same Materials and Methods as the specimen examined in Nishikawa (2002). Taken to- gether, Dr. Ikeda collected at least eight specimens of the Sampling (nearly) full body of I. taenioides from November to De- cember in 1901. In addition, Sato (1934) reported the oc- Ikeda taenioides was collected from the tidal flat in Fig. 1. Sampling localities of Ikeda taenioides in this study, along with its previous sampling records in Japan. Filled and open circles indicate the sampling localities of this study (A: Ohmishima, B: Hachi) and the previous sampling records [1: Ikeda (1904, 1907), 2: Satô (1931), 3: Sato (1934), 4: Satô (1937), 5: Komai (1949), 6: Tanita et al. (1956), 7: Honma (1968), 8: Dewa (2006), 9: Nishikawa (2012), 10: Goto et al. (2013), 11: Biodiversity Center of Japan, Nature Conservation Bureau, Ministry of the Environment of Japan (2016), 12: Goto et al. (2017), 13: Oshiro et al. (2020).] Main bodies of Ikeda taenioides 157 Fig. 2. Living individuals of Ikeda taenioides and its habitat. (A) An intertidal flat of Ohmishima Island and field gear (a yabby pump and sieve). (B) A proboscis and trunk of the specimen of I. taenioides collected at Ohmishima Island (specimen ID: #1). (C, D) Close-up of the trunk and the proximal part of the proboscis (#1). (E) A trunk of the specimen collected at Hachi (specimen ID: #2). (F) Gonoducts exposed to outside of the trunk (#2). (G) Posterior end of the trunk (#2). (H) A fecal pellet expelled from specimen #1. Scale bars: 5 cm (B), 3 cm (C, E), 5 mm (D, F, G), 1 mm (H). 158 R. Goto et al. western Ohmishima Island (hereafter referred to as Ohmi- ers [LCO1490 and HCO2198 (Folmer et al. 1994); 10 µM shima; 34°13′30″N, 132°59′22″E; Figs. 1A, 2A), Imabari, each], 2.5 µL of 10x Taq Buffer, 2.0 µL of dNTP Mixture, Ehime Prefecture on June 16, 2019, and from the Hachi 0.13 µL of TaKaRa ExTaq polymerase (TaKaRa, Otsu, tidal flat located at the mouth of the Kamo River (hereafter Japan), 2.5 µL of template DNA and 17.5 µL of distilled referred to as Hachi; 34°19′31″N, 132°54′00″E; Fig. 1B), water. Thermal cycling was performed with an initial de- Takehara, Hiroshima Prefecture on February 12, 2020. We naturation for 3 min at 94°C followed by 30 cycles of 30 s used a bait pump which was 5 cm in diameter and 75 cm at 94°C, 30 s at 42°C, and 2 min at 72°C, with a final 3 min in length (Poseidon 750 mm yabby pump; see Fig.
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