Aulodrilus pigueti Kowalewski, 1914

Ohtaka, Akifumi, 2021, Taxonomical study of Japanese Aulodrilus Bretscher (Annelida, Clitellata Tubificinae) with descriptions of two new species, Zootaxa 4952 (1), pp. 1-32 : 18-21

Aulodrilus pigueti Kowalewski, 1914

( Figures 13 , 14 )

Aulodrilus pigueti Kowalewski, 1914: 625 , fig 12.

Aulodrilus pigueti Kowalewski : Hrabě 1981: 72, pl 11, figs 16–21, pl 12, figs 1–6; Brinkhurst et al. 1990: 908, fig. 2A; Finogenova & Arkhipova 1994: 13, figs 14–17; Pinder & Brinkhurst 2000: 46; Arslan & Sahin 2003: 278, fig 4.

Aulodrilus remex Stephenson, 1921: 753 , pl XXVIII, figs. 2–6; 1923: 107, figs 42–45; Aiyer 1929: 81, pl VI, figs 1–10; Naidu 1965: 470, fig 3a–e.

Aulodrilus kashi Mehra, 1922: 946 , figs 1–11; Stephenson 1923: 509.

Aulodrilus prothecatus Chen, 1940: 68 , fig 22.

Aulodrilus tchadensis Lauzanne, 1968: 102 , figs 12–13.

Material examined. Japan: 5 immature specimens, offshore O-numa, Nanae Town , Hokkaido (10–12 m depth), 1 June 2008 . 3 immature specimens, rice paddy in Iwaihana, Hachimantai City , Iwate Prefecture, 15 July 2007 . 3 immature specimens, offshore Lake Izunma, Tome City , Miyagi Prefecture (1.5 m depth), 7 June 2008 . 1 immature specimen, Kabukuri-numa Marsh, Tome City , Miyagi Prefecture, 7 June 2008 . 3 mature specimens, Nikatsutsumi reservoir, Maki Town , Niigata Prefecture, 7 Oct. 1982 . 1 immature specimen, a stream in Saitama City , Saitama Prefecture, Aug. 2005 , coll. T. Torii . 2 immature specimens, littoral Lake Hinuma , Ibaraki prefecture, 9 Aug. 1982, coll. H. Morino. 4 mature and 178 immature specimens, offshore Lake Kitaura, Ibaraki Prefecture (6 m depth), 3 July , 9 Aug. 1980 , 20 Jan., 20 May, 22 June , 16 July , 26 Aug. , 29 Sep. , 21 Oct. , 19, 26 Nov. , 24 Dec. 1982 ; 24 June, 14 Feb., 15 Mar. , 14 Apr. , 17 May , 25 June , 14 July , 19 Aug. 1983 ; 20 Jan., 14 June, 16 July , 17 Aug. , 14 Sep. 1984; 17 June 1985 . 4 immature specimens, Mizuhara, Lake Kitaura , Ibaraki Prefecture, 11 Dec. 1980; 9 June 1981 . 5 immature specimens, offshore Lake Kasumigaura , 9 Aug. 1983, 9 Feb. 2011 . 3 mature and 2 immature specimens, offshore Lake Suwa , Nagano Prefecture (5.5 m depth), 18 Oct. 1980; 9 Aug. 2006, coll. H. Fukuhara. 2 immature specimens, Lake Kahoku-gata , Ishikawa Prefecture, 11 Aug. 1999, coll. M. Nishino. 3 immature specimens, Yamanoshita Bay, south basin of Lake Biwa, Otsu City , Shiga Prefecture, 3 Oct. 1992 . 2 immature specimens, Mizorogaike Marsh, Kyoto City , Kyoto Prefecture, 1 Nov. 2004, coll. Y. Murakami. 1 immature specimen, River Kitafune, Hirata City , Shimane Prefecture, 6 Nov. 1993 . Littoral Lake Ikeda, Ibusuki City , Kagoshima Prefecture (10 m depth), 15 July 1998 . Altogether 10 mature and 112 immature specimens from Japan. U.S.A. : 16 immature specimens, Coeur d’Alene Lake , Idaho, 24 June 2004, coll. K. Kuwabara (S. V. Fend collection) . 2 immature specimens, Cosumnes River, San Francisco Bay Delta, California, (date and collector unknown) (S. V. Fend collection) .

Description. Description of Japanese specimens in mature and preserved states: 6–9 mm length, about 0.25 mm width in anterior segments; up to 62 segments. Posterior 1/5–1/7 of body without chaetae and unsegmented, with numerous transverse wrinkles. Prostomium bluntly conical. Pharynx covered by a thin layer of pharyngeal glands. Intestine suddenly widens in VII. Chloragogen cells on gut from VI or VII on. Transverse vessels forming complicated loops in I–VI. Forming a mud tube with mucus and foreign matter.

Dorsal chaetal bundles consist of hairs and bifid or oar-shaped chaetae. Dorsal hairs smooth and slightly sigmoid, beginning in III or IV in immature specimens but in III in mature ones: 2–8 per bundle, 70–125 µm long. Dorsal crotchets in anterior segments ( Fig. 13A,B ) 6–11 per bundle, 46–80 µm long, with distal nodulus and with upper tooth shorter and thinner than lower one; replaced by 4–8 oar-shaped chaetae ( Fig. 13C,D,G–K ) from VII to X on. Oar-shaped chaetae 50–82 µm long. Distal, oar-shaped part 4.1–5.7 µm wide; chaeta with nodulus at 1/3 from distal end, bent backward slightly at 1/4 from distal end ( Fig. 13D ). The distal part rounded and slightly concave with a swollen edge ( Fig. 13C,J,K ). Ventral chaetae ( Fig. 13E ) all bifid crotchets with nodulus at 1/3 from distal end and with parallel teeth, with upper tooth about 2/3 times longer and much thinner than lower one; 8–12 per bundle, 53–70 µm long in anterior segments, 4–7 per bundle and 46–60 µm long in posterior ones. Penial chaetae ( Fig. 13F ) in VII when mature; 1–3 per bundle (usually 2), 130–158 µm long, much larger than other, somatic crotchets. Distal end hollow and spoon-shaped.

Clitellum ( Fig. 14A ) in 1/2 VI–VIII, conspicuous, except around male pores. Paired testes at V and VI, with former pair smaller than the latter one. Paired ovaries in VII. Male funnels large, about 90 µm in diameter. Vasa deferentia ( Fig. 14A ) about 140 µm long, 20 µm wide, not winding, somewhat thinner near atria; connected with atria apically. Atria globular or ovoid in shape, 90 µm long and 70 µm wide, with thick and glandular inner epithelium ( Fig. 14D ). Prostate glands solid, slightly smaller than atria, connected through short stalk at lateral sides of atria. Penes conical and as large as atrium when protruding, consisting of non-glandular, loose tissues and thin inner and outer epithelia, opening into large ventromedian male bursa at middle of VII ( Fig. 14C,E ). Large penial chaetophores ( Fig. 14A, F ), 80 µm long, 70 µm wide, located posterior to penes in VII, consisting of a layer of tall glandular cells surrounding penial chaetae and thin muscular coverings; opening into posterior side of male bursa. Accessory glands formed by several clusters of glandular cap cells attached to dorsal side of the penial chaetophore ( Fig. 14A ). Female funnel small and thin. Sperm sac restricted to VII, ovisac in VII and VIII. Spermatheca in VI ( Fig. 14A ); ampulla large and globular or ovoid, and duct well marked off from ampulla, opening at chaetal line in VI ventrolaterally ( Fig. 14B ). Sperm diffuse in spermathecal ampulla.

Remarks. Oar-shaped chaetae in dorsal bundles usually begin to appear in VII or VIII, and they completely replace bifid crotchets from VIII–XI on. Therefore, some 'transitional' chaetal bundles in VII–X have both bifid and oar-shaped chaetae, and occasionally their intermediates ( Figs. 13G–I ), in addition to hair chaetae. Replacement of bifid chaetae by oar-shaped chaetae proceeds from medial to lateral in each chaetal bundle. Paired testes were observed in V and VI in all mature specimens examined. Because segment V had no efferent duct, the testes of this segment are thought to be functionless. Large penes and glandular cap cells on penial chaetophores found in the present specimens agree well with earlier descriptions of this species ( Kowalewski 1914; Ohtaka & Usman, 1997).

Several Aulodrilus species with oar-shaped chaetae in dorsal bundles have been described. Among them, A. remex Stephenson, 1921 , A. kashi Mehra, 1922 , A. prothecatus Chen, 1940 and A. tchadensis Lauzanne, 1968 have been regarded as junior synonyms of A. pigueti by several authors ( Chekanovskaya 1962; Brinkhurst 1963, 1971; Brinkhurst et al. 1990; Finogenova & Arkhipova 1994; Ohtaka & Usman 1997). They share rounded oar-shaped chaetae in dorsal bundles, ovoid or bean-shaped atria, penes set in a median male bursa, and spoon-shaped penial chaetae. Cap cells on penial chaetophores are also found in the descriptions of A. remex by Aiyer (1929) and A. prothecatus by Chen (1940). A sightly swollen edge and concavity in the oar-shaped portion found in the Japanese specimens of A. pigueti were also confirmed in SEM micrographs of Russian specimens by Finogenova & Arkhipova (1994) and those of Indonesian specimens by Ohtaka & Usman (1997). Chen (1940) and Aiyer (1929) described no true penes, but instead described atrial ducts winding in large penial sacs for A. prothecatus and A. remex , respectively. Hrabě (1981) also described the atrium as ending in a very small penis, which extends into a long outlet duct in A. pigueti . These atrial ducts should be everted and protruded, forming the large pseudopenes found in the present study.

Aulodrilus acutus Ohtaka & Usman, 1997 has tapering oar-shaped chaetae in dorsal bundles. This species resembles A. pigueti in having a median male bursa and globular atrium, but it differs from A. pigueti in lacking penial chaetae.

Distribution. A. pigueti is cosmopolitan ( Brinkhurst 1971). In Japan, this species has been widespread in mesoeutrophic lakes as well as paddy fields ( Ohtaka 2014; 2018b). Aulodrilus pigueti and its relatives are common in Southeast Asia and the south Asian region ( Stephenson 1921; Mehra 1922; Ohtaka & Usman 1997; Ohtaka 2018a). Although no molecular approach has been used in the taxonomy and phylogeny of the nominal A. pigueti and its related taxa, it is probable that there are multiple lineages within the species.

Figures

FIGURE 13. Chaetae of Aulodrilus pigueti Kowalewski from Lake Kitaura, Japan. A, dorsal crotchet in II; B, the same in V; C, oar-shaped chaeta in VII, frontal view; D, the same, lateral view; E, ventral chaeta in VIII; F, penial chaeta; G–I, variation of oar-shaped chaetae, distal ends; J, SEM photomicrograph of frontal view of left side of dorsal chaetal bundle in X; K, SEM photomicrograph of lateral view of dorsal chaetal bundle in a mid-segment.

FIGURE 14. Genital organs of Aulodrilus pigueti Kowalewski from Niigata, Japan. A, parasagittal section of genital segments; B, cross section at the spermathecal pores in VI; C, the same at the male pores in VII; D, longitudinal section of atrium with prostate; E, longitudinal section of penis in male bursa; F, longitudinal section of chaetophore with penial chaetae.