INTRODUCTION

The genus BelbollaAndrássy, 1973 is characterized by the presence or absence of ocelli, presence of a large and narrow buccal cavity divided into two parts by a sclerotized transverse band, the presence of three teeth, of which one ventrosubdorsal is the largest, and the presence of a series of bulb-like muscular oesophageal swellings (4 to 10) in the posterior section of pharynx, which is the most important diagnostic characteristic of the genus within the family Enchelidiidae Filipjev, 1928 (Smol et al. 2014). So far, the genus Belbolla contains 15 valid species found from various marine habitats (Huang and Zhang 2005;Nasira et al. 2014;Gagarin and Thanh 2016;Gagarin and Tu 2016). Of these, four species of the genus Belbolla have been previously described around the Korean waters, i.e. B. zhangiGuo and Warwick, 2001 from the Bohai Sea, China and B. huanghaiensisHuang and Zhang, 2005, B. stenocephalumHuang and Zhang, 2005 and B. warwickiHuang and Zhang, 2005 from the Yellow Sea, China.

During a continuous ecological investigation on the biodiversity of the free-living marine nematofauna around the East Sea, Korea, one Belbolla nematode species was obtained from the washings of coarse sediments from a shallow subtidal benthic interstitial environment. Present paper deals with a new species of the genus Belbolla based on morphological study using a differential interference contrast (DIC) microscope. The new species is described and illustrated herein as Belbolla wonkimi sp. nov., and we discuss its taxonomic relationships with other valid species of the genus. This is the first taxonomic report of the genus Belbolla from the East Sea, Korea.

MATERIALS AND METHODS

Sampling of specimens

The marine nematodes were obtained from the washings of subtidal sediments, which were collected at a depth of 104 m using Smith McIntyre grab (OSIL, UK) at Gangneung on the eastern coast of Korea.

Sample processing and preparation of specimens

Meiobenthos were roughly separated from the sediments by decantation methods using a 67 μm mesh sieve in the survey field after freshwater rinsing for less than a few minutes to reduce the attachment from the sediments (Kristensen 1989), and then fixed in 4% neutralized formalin in sea water. After the initial sampling, meiobenthos were extracted once again from the rough samples using the Ludox flotation method (Burgess 2001) in the laboratory, and the concentrated samples were subsequently fixed in 4% neutralized formalin solution. The marine nematodes were picked up under a high magnification of dissecting microscope (Leica M205 C; Leica Microsystems, Germany). Specimens for morphological observation under a light microscope were dehydrated through a graded series of glycerin according to Seinhorst (1959) and mounted on a HS slide (Shirayama et al. 1993). The mounted nematodes were examined and photographed using an Olympus BX53 microscope equipped with an Olympus DP26 digital camera (Olympus, Japan). All drawings and measurements were made with the aid of a camera lucida.

Terminology and abbreviations

The terminology used for the description and measurements was followed by Huang and Zhang (2005). Abbreviations used in the text are as follows: a=body length divided by maximum body diameter; a.b.d.=anal body diameter; b=body length divided by oesophagus length; c=body length divided by tail length; c.d.=corresponding body diameter.

SYSTEMATIC ACCOUNTS

Phylum Nematoda Potts, 1932

Class Enoplea Inglis, 1983

Order Enoplida Filipjev, 1929

Family Enchelidiidae Filipjev, 1918

Genus BelbollaAndrássy, 1973

Type species

Belbolla tenuidens (Cobb, 1920) Andrássy, 1973

Valid species of the genus Belbolla

B. asupplementataJuario, 1974

B. californica (Allgén, 1951) Andrássy, 1973

B. gallanachmorae (Inglis, 1961) Andrássy, 1973

B. gracilis Gagarin and Thanh, 2016

B. heptabulba (Timm, 1961) Andrássy, 1973

B. huanghaiensisHuang and Zhang, 2005

B. intarmaBelogurov and Belogurova, 1980

B. longispiculataNasira, Shahina and Shamin, 2014

B. stenocephalumHuang and Zhang, 2005

B. sundaensis (Micoletzky, 1930) Andrássy, 1973

B. teissieri (Luc and Coninck, 1959) Andrássy, 1973

B. tenuidens (Cobb, 1920) Andrássy, 1973

B. vietnamica Gagarin and Tu, 2016

B. warwickiHuang and Zhang, 2005

B. zhangiGuo and Warwick, 2001

Belbolla wonkimi sp. nov. (Figs. 1, 2; Table 1)

Type material. Holotype male (NA00156498), in glycerin on HS slide, from Sacheon-myeon, 17 April 2018 (leg. H Lee, HG Kim and HJ Lee) was deposited in the nematode collection at the specimen conservation room of the Marine Biodiversity Institute of Korea (MABIK), Seochun, Korea. Two paratype males (KIOST NEM-1-2341, KIOST NEM-1-2342), mounted on HS slides, was deposited in the nematode collection at the specimen conservation room of the Bio-Resources Bank of Marine Nematodes (BRBNM), East Sea Research Institute, Korea Institute of Ocean Science & Technology (KIOST), Korea.

Etymology. The proposed specific name wonkimi is named after Prof. Won Kim of the School of Biological Sciences at Seoul National University, in recognition of his excellent mentoring during the first author’s PhD research course (H. S. Rho).

Type locality. Subtidal zone of Sacheon-myeon (37° 44ʹ16ʺN, 128°59ʹ05ʺE), Gangneung-si, Gangwon-do, Republic of Korea.

Habitat. Subtidal sediments with tiny shell gravels and detritus collected at a depth of 104 m.

Measurements. See Table 1 for measurements and morphometrics.

Diagnosis. Body relatively long (3,263-3,396 μm in males); ocelli absent; nine well-developed oesophageal bulbs in the posterior section of pharynx; well developed two winged precloacal supplements; triangle-shaped gubernacular apophysis short and thick.

Description. Male (Holotype). Body comparatively long (3,328 μm), slender; anterior body region outstretched anteriorly and strongly tapered anteriorly from mid oesophagus to cephalic region; posterior body region often slightly curved ventrally in fixed specimen (Figs. 1C, 2A). Head diameter 15 μm distinctly narrowed. Body at level of end of posterior pharyngeal region 6.1 times as wide as head region width. Body cuticle, smooth, no lateral differentiation. Anterior parts of head around cephalic setae, separated with slight constriction (Figs. 1A, 2B). Lip region not extruded in fixed specimen. Six short, thin labial setae on lip region arranged in one circle. Inner labial setae not observed. Ten cephalic setae (11 μm long) inserted at level of amphideal fovea and arranged in one circle. Maximum body width 101 μm. Buccal cavity wide (10 μm) with thick wall 1.7 times as long (17 μm) as wide. Buccal cavity with one large right dorsolateral tooth and two less prominent teeth, which are composed of dorsal and left ventrolateral in position (Fig. 1A). Buccal cavity large and wide and separated into two buccal chambers by a cuticular ring, which is smooth with no denticles. Amphideal fovea located at level of stoma. Ocelli absent. Several cervical setae, 25 μm in length. Oesophagus muscular and expands gradually and evenly, 796 μm long and posteriorly modified into nine oesophageal bulbs (length of oesophageal bulb 395 μm) (Figs. 1B, 2E). Oesophagus corresponding diameter 91 μm. Nerve ring 374 μm from anterior end with 72 μm corresponding body diameter and at 46.9% of oesophagus length. Cardia short, conoid. Male diorchic, testis opposed and outstretched, located left or right of intestine. Spicules long (115 μm long or 1.6 times as long as a.b.d.) and cylin-drical, strongly arcuated ventrally with rounded open head and blunt distal end; proximal end slightly cephalated (Figs. 1D, 2D). Gubernaculum small and wide, 18 μm long with triangle-shaped apophysis. Two winged precloacal supplements strongly developed; anterior precloacal supplement 543 μm lies from cloacal opening and posterior precloacal supplement lies 350 μm from cloacal opening (Figs. 1C, 2C). Tail long and slender, conico-cylindrical, 299 μm long, 4.3 times anal body diameter, tapering with distal third cylindrical and with slightly swollen tip with three minute terminal setae (Figs. 1C, 2F).

Female. Unknown.

Remarks. The genus BelbollaAndrássy, 1973 was first erected as Bolbella by Cobb (1920) based on Bobella tenuidensCobb, 1920 as a type species of the genus (Andrássy 1973), and classified within the family Enchelidiidae Filipjev, 1928 belongs to the order Enoplida Filipjev, 1929 based on the following combination of characteristics: the presence or absence of ocelli, the presence of a large and narrow buccal cavity divided into two parts by a sclerotized transverse band, the presence of three teeth, of which one ventrosubdorsal is the largest, and the presence of a series of bulb-like muscular oesophageal swellings (4 to 10) in the posterior section of pharynx, which is the most remarkable taxonomic key character of the genus within the family Enchelidiidae (Smol et al. 2014). So far, 15 species within the genus Belbolla have been described previously from various localities of the intertidal and shallow subtidal habitats in oceans all over the world (Huang and Zhang 2005;Nasira et al. 2014;Gagarin and Thanh 2016;Gagarin and Tu 2016) (Table 3). Belbolla can be artificially subdivided into two groups on the basis of the number of oesophageal bulb, as adopted in the keys by Belogurov and Belogurova (1980) and Huang and Zhang (2005) (Table 2). The first group is characterized by having four, seven or eight oesophageal bulbs in male, and comprises 13 recorded species: B. asupplementata, B. californica, B. gallanachmorae, B. gracilis, B. heptabulba, B. longispiculata, B. stenocephalum, B. sundaensis, B. teissieri, B. tenuidens, B. vietnamica, B. warwicki, and B. zhangi. On the other hand, the second group is characterized by having nine oesophageal bulbs, and includes the remaining two species (B. huanghaiensis and B. intarma), with the present new species. Belbolla wonkimi sp. nov. is characterized by the following combination of characteristics: (1) relatively long body (3,263-3,396 μm); (2) the absence of ocelli; (3) nine oesophageal bulbs in the posterior pharynx; (4) well developed two winged precloacal supplements; (5) longer spicule length (115-130 μm, 1.6-1.8 a.b.d. long); and (6) triangle-shaped shorter gubernacular apophysis length (17-18 μm). In having the nine muscular oesophageal bulbs in the pharynx, which is the most remarkable diagnostic characteristic of the genus, Belbolla wonkimi sp. nov. is very similar to B. huanghaiensis and B. intarma among the congeners. However, the new species differs from B. huanghaiensis by: (1) the shape of gubernacular apophysis (triangle-shaped vs. long dorso-caudally directed); (2) the very shorter gubernacular apophysis (17-18 μm vs. 45-60 μm); (3) the relatively longer tail in male (265-299 μm vs. 230-252 μm); (4) distance of the posterior precloacal supplement from cloacal opening in male (350-385 μm vs. 210-255 μm); and (5) distance between precloacal supplements in male (189-193 μm vs. 115-140 μm). Belbolla wonkimi sp. nov. can be also easily distinguished from B. intarma by the relatively longer tail in male (265-299 μm vs. 215 μm), and the shape and relative length of spicules (smooth on the distal end of spicules, 115-130 μm vs. hook on the distal end of spicule, 110 μm).