Taxonomical study of Japanese Aulodrilus Bretscher (Annelida, Clitellata Tubificinae) with descriptions of two new species Author Ohtaka, Akifumi Faculty of Education, Hirosaki University, Hirosaki 036 - 8560, Japan text Zootaxa 2021 2021-04-08 4952 1 1 32 journal article 7377 10.11646/zootaxa.4952.1.1 3d9df3ba-adb5-46ec-9784-eb3a9853258b 1175-5326 4671489 1B8CC647-D100-4BFD-A054-F1D9F94274B3 Aulodrilus japonicus Yamaguchi , 1953 ( Figures 6 , 7 , 8 ) Aulodrilus japonicus Yamaguchi , 1953: 298 , fig 12m , pl VIII, figs 5–7. Aulodrilus japonicus Yamaguchi : Brinkhurst 1963: 70 ; Yamaguchi 1965: 542 ; Hrabě 1981: 70 , pl XI, figs 5–10; Liang & Xie 1997: 390, fig 5; Finogenova & Arkhipova 1994: 8 , figs 3, 6–10, 18; Timm & Všivkova 2007: 32 , fig 6. Ohtaka & Chen 2010: 105. Aulodrilus pluriseta (Piguet) : Brinkhurst 1971: 525 , fig 8.23J (in part); Wang & Liang 2001: 36 , fig. d, e. Material examined . Japan : 20 immature specimens, a pond in Wakkasakanai , Toyotomi Town , Hokkaido , 29 Oct. 1984 . 2 immature specimens, Shinoro-Shinkawa River , Sapporo , Hokkaido , 6 May 1983 . 128 mature and 500 immature specimens, Maruyama , Sapporo City , Hokkaido , 4, 19 Oct. , 30 Dec. 1983 ; 23 Apr. , 18 May , 2, 28 July , 15 Aug. 12 Oct. , 4 Nov. 1984 ; 19 Apr. 10 May , 20 June , 27 July , 11, 28 Aug. , 19 Sep. , 1985 . 6 immature specimens, Nishioka reservoir, Sapporo City , Hokkaido , 1 Sep. 1982 , 28 Apr. 1983 . 2 mature and 7 immature specimens, littoral Lake Shikotsu , Hokkaido , 30 May 1979 , coll. T . Ito . 2 immature specimens, littoral Lake O-numa, Nanae Town , Hokkaido , 9 May 1984 . 5 immature specimens, Mitake Park , Hirosaki City , Aomori Prefecture , 17 July 1992 . 3 immature specimens, a stream in Tokiwano , Hirosaki City , Aomori Prefecture , 15 May 2009 . 20 immature specimens, rice paddy in Sakamoto , Hirosaki City , Aomori Prefecture , 16 July , 25 Sep. 2011 ; 1 Sep. 2012 . 10 immature specimens, Osawa near Lake Tazawa , Senboku City , Akita Prefecture , 29 Sep. 2007 . 1 immature specimen, Ushiawari River on Mt. Chokai , Yuza Town , Yamagata Prefecture , 29 July 2015.1 immature specimen, a brook in Gobono , Obanazawa City , Yamagata Prefecture , 8 May 1984 . 1 immature specimen, a stream in Naganeyama hill, Obanazawa City , Yamagata Prefecture , 9 Aug. 1990 . 3 immature specimens, offshore Lake Onogawa , Kita-Shiobara Village , Fukushima Prefecture ( 2.5 m depth ), 9 July , 2010 . 1 immature specimen, offshore Lake Yunoko , Nikko City , Tochigi Prefecture ( 6 m in depth), 22 July 1988 , coll. T . Iwakuma . 3 immature specimens, offshore Lake Maru-numa , Katashina Village , Gunma Prefecture ( 16.3 m depth ), 21 Sep. 2009 . 6 immature specimens, Saikawa River , Sano City , Tochigi Prefecture , 10 Nov. 1980 . 3 immature specimens, River Takada , Tomioka City , Gunma Prefecture , 4 Apr. 1984 . 5 immature specimens, littoral Lake Kizaki , Omachi City , Nagano Prefecture ( 5.3 m depth ), 2 Aug. 2007 . 4 immature specimens, Tsuya River , Yoro Town , Gifu Prefecture , 9 June 2005 , coll. K. Tanida. 15 immature specimens, north basin of Lake Biwa ( 10–70 m deep, mud), 26 Jan. 1992 – 14 Feb. 1995 . 7 immature specimens, a marsh in Hayasaki , Nagahama City , Shiga Prefecture , 29 Aug. 2002 . 2 immature specimens, Mizorogaike Marsh , Kyoto City , Kyoto Prefecture , 1 Nov. 2004 , coll. Y. Murakami. 10 immature specimens, Kitafune Stream , Izumo City , Shimane Prefecture , 6 Nov. 1993 . 5 immature specimens, Rivers Kanna and Kesashi , Okinawa Is. , Okinawa Prefecture , 7, 8 Aug. 1990 , coll. M. Tsuchiya. Altogether 130 mature and 642 immature specimens from Japan. Taiwan : 1 immature specimen ( ESRI-OA0009 ), a pond in Minchien , Nantou County , 10 Sep. 2008 . U.K. : 1mature and 3 immature specimens, Bala Lake , N. Wales , 1962 (detailed collection data unknown), ( R . O. Brinkhurst collection) . Estonia : 25 immature specimens, aquarial culture at the Võrtsjärv Limnological Station , started in 2006 with specimens from the Emajõgi River , Tartu City , Estonia , coll. T . Timm . U.S.A. USNM 32648 , 1 immature specimen from Sonoma County , California , 18 Sep. 1962 , R .O. Brinkhurst collected and deposited as Aulodrilus pluriseta . 2 mature and 1 immature specimens, Santa Clara , California (exact locality unknown), 1 Apr. 2002 , coll. S. V . Fend . 10 immature specimens, a stream near McMinnville , Oregon , 10 May , 2001, coll. S. V . Fend . 3 immature specimens, Coeur d’Alene Lake , Idaho , 24 June 2004 , coll. J. Kuwabara (S. V . Fend collection) . 5 immature specimens, Sacra- mento– San Joaquin River Delta, California , Oct. 2003 , coll. W. Fields. 2 immature specimens, Cosumnes River , San Francisco Bay Delta, California (date and collector unknown) (S. V . Fend collection) . Description . The following description is based on the topotypic specimens from Maruyama, Sapporo, Japan . Mature and living state: length 28–35 mm , width 0.3–0.5 mm in anterior segments; up to 150 segments. Body anteriorly dark red; posteriorly somewhat yellowish. Prostomium conical, more or less pointed. No secondary annulations. Posterior part of body (consisting of up to 45 segments) without chaetae, and the posterior end of about 0.4 mm without septa, loosely packed with coelomocytes. FIGURE 6. Chaetae in Aulodrilus japonicus Yamaguchi from Maruyama, Sapporo, Japan. A , dorsal chaeta in VIII; B , ventral chaeta in IV; C , the same in X; D , distal end of dorsal chaeta in an anterior segment, ventral view; E , the same, dorsal view; F , SEM photomicrograph of ventral chaetae in an anterior segment; G , the same of dorsal chaeta in a mid-segment, dorsal view; H , the same, lateral view. Pharynx in II and III; thick walls ( 20–25 µm ) covered by a thin layer of pharyngeal glands. Chloragogen cells from posterior part of IV on, a thin tissue as far as VIII or IX, and then suddenly thickened. Intestine widens at X or XI. Contractile commissural vessels in VIII–IX. Dorsal vessel shifted ventrolaterally in X, located on the left side of ventral vessel. Nephridia from XI, elongate; ental part of narrow duct densely surrounded by large (up to 80 µm diameter) and spherical cells. Forming a loose and thick mud tube. Dorsal chaetal bundles consisting of hair and pectinate crotchets, both beginning in II. Hair chaetae smooth and slightly sigmoid, 4–7 per bundle, 90–207 µm long in anterior segments; 1–3 per bundle, 60–150 µm long in posterior ones. Dorsal crotchets ( Fig. 6A ) with distal nodulus, 5–9 per bundle, 76–110 µm long in anterior segments; 2–6 per bundle, 65–86 µm long in posterior ones; distal end with upper tooth split into 5–20 fine teeth which are arranged irregularly, and much thinner and shorter than single lower tooth ( Fig. 6D, E, G, H ). Ventral chaetae ( Fig. 6B, C ) bifid crotchets with distal nodulus, 8–13 per bundle, 75–112 µm long in anterior segments; 3–8 per bundle, 68–84 µm long in posterior segments; distal teeth parallel and lower tooth about twice longer and much thicker than upper one; one to several small teeth often occur laterally between upper and lower teeth ( Fig. 6F ). Distal parts of all dorsal and ventral crotchets with lateral expansions along the axis of chaeta. Ventral chaetae in spermathecal and penial segments of usual type , neither modified nor absent even in fully mature specimens. Clitellum more or less conspicuous, usually occupying from 2/3 IX to end of XI; ventral side flattened and slightly swollen laterally of male pores. Gonads and copulatory organs paired ( Fig. 7A ). Testes usually in VIII and IX, ovaries in X. In fully mature specimens, anterior pair of testes not as well developed as posterior testes and ovaries. Male funnels one pair on 9/10, large, 160 µm in diameter. Vasa deferentia about 600 µm long, winding and slightly stouter ectally than entally, connected with atrium apically. Atrium bean-shaped, 180–220 µm long, inner epithelium thick and glandular with basal nuclei ( Fig. 7B ). Prostate gland large, connected laterally with atrium through short and narrow stalk ( Fig. 7C ). Ejaculatory duct about 190 µm long, nearly as long as atrium, and swollen at middle ( Fig. 7B ). Penes short and conical, set in small depressed chambers, opening at lateral side of ventral chaetal bundle in X or rarely XI ( Fig. 8B ). Paired spermathecae usually in VIII and IX ( Fig. 7A ); anterior pair smaller than posterior one. Spermathecal ampullae globular or ovoid in shape. Spermathecal ducts short, well-marked off from ampullae, opening laterally at slightly behind anterior septa ( Fig. 8A ). Loose sperm masses present in spermathecal ampullae. Sperm sac usually in VIII–X. Egg sac restricted to ovarial segment. FIGURE 7. Aulodrilus japonicus Yamaguchi from Maruyama, Sapporo, Japan. A , parasagittal section of genital segments; B , longitudinal section of atrium and ejaculatory duct; C , cross section of atrium on the line of junction with prostate gland. Variation . Variations related to multiplication of spermathecae and to shift in the segmental position of genital organs were found in the present specimens as follows. Of 28 mature specimens from the type locality in Sapporo, 24 had two pairs of spermathecae, one in VIII and another one in IX, and one pair of male ducts in X ( Fig. 8C ). One specimen showed the same arrangement of genital organs, but lacked the spermatheca on the left side in VIII. Two specimens had a third pair of spermathecae in VII, in addition to those in VIII and IX ( Fig. 8D ). One specimen had paired spermathecae in VII, IX, and X and the male duct in XI. In all cases examined, anterior spermathecal ampullae were smaller than posterior ones. FIGURE 8. Location of genital organs in Aulodrilus japonicus Yamaguchi from Maruyama, Sapporo, Japan. A , cross section at the level of spermathecal pore in VIII; B , cross section at the level of male pore; C , horizontal section of genital segments of a specimen with two pairs of spermathecae; D , sagittal section of the genital region of a specimen with three pairs of spermathcae. Remarks . Since Yamaguchi (1953) described the present species based on immature specimens lacking genital organs except for gonads, the identity of this species has remained unclear for several decades ( Brinkhurst 1963 , 1971 ; Brinkhurst & Wetzel 1984 ). Brinkhurst (1971) once tentatively synonymized it with A. pluriseta (Piguet) . Hrabě (1981) described the male duct for the first time and regarded A. japonicus as a distinct species. Then Finogenova & Arkhipova (1994) , Liang & Xie (1997) , and Timm & Všivkova (2007) redescribed the species based on specimens from continental Eurasia. The newly obtained Japanese specimens, including topotypes listed above, agree well with the previous descriptions both in chaetal and genital structures. A. japonicus differs from A. pluriseta in the following respects (corresponding condition of latter species in parentheses): upper teeth multiple in dorsal crotchets (both dorsal and ventral crotchets mostly bifid); vasa deferentia about three times longer than atria (slightly longer than atria); male ejaculatory ducts long, as long as atria (much shorter than atria); spermathecal ampullae ovoid, well distinguished from ducts (cylindrical and not well marked off from the ducts); wide midgut begins either in X or XI (VIII or IX); very thick chloragogen tissue appears in one segment before the beginning of midgut (chloragogen tissue thin throughout). Results of this examination confirmed that all specimens listed above have multiple upper teeth in the dorsal chaetae. The irregularly arranged, multiple upper teeth in the dorsal chaetae of A. japonicus are unique in oligochaetes, whereas such a condition is common in hooded hooks of capitellid polychaetes (e.g., Yabe & Mawatari 1998 ; Tomioka et al . 2016 ). Additional small teeth were often found in ventral chaetae on the lateral sides on the base of teeth branch in the SEM observation of topotypic specimens ( Fig. 6F ). Finogenova & Arkhipova (1994) presented this structure on Neva estuary specimens from western Russia . All mature Japanese specimens that were examined had more than one pair of spermathecae. Two pairs of spermathecae in VIII and IX are also confirmed in the Bala Lake specimen from northern Wales and in a Santa Clara specimen from North America. Multiple pairs of spermathecae, in VIII and IX and occasionally also in VI, were described for Czech material ( Hrabě 1981 ) and for Chinese specimens ( Liang & Xie 1997 ). Multiple pairs of spermathecae therefore appear to be the normal condition in A. japonicus . The long ejaculatory duct with a middle swelling is also unique in the genus. Gonads were found in VIII, IX, and X in the present specimens, as Yamaguchi (1953) described. In fully mature worms, gonads of IX (testes) and X (ovaries) were well developed, although those in VIII (testes) were rudimentary. The rudimentary testes were much smaller and without corresponding efferent ducts. They are thought to be functionless as in A. pluriseta ( Naidu 1965 ) , A. remex Stephenson, 1923 ( Aiyer 1929 ) , (a synonym of A. pigueti ), and A. pigueti (present study). Distribution . Widespread. This species has been confused with A. pluriseta . For example, A. pluriseta of Wang & Liang (2001) should be ascribed to A. japonicus . USNM 32648, a California specimen registered as A. pluriseta , is confirmed to be A. japonicus in the present study. This is a common tubificine, at least in Japanese waters. Periodic samplings at a small, shallow pond in Maruyama, Sapporo ( type locality) revealed that mature individuals of the present species appeared—in a low proportion (maximum 10%)—only during summer when water temperature was above15 °C (Ohtaka, unpublished data). Van den Hoek & Verdonschot (2005) also noted that mature specimens of A. japonicus were found only in July in the Netherlands .