Tasserkidrilus tubifex

Timm, Tarmo, 2006, A Nearctic tubificid Varichaetadrilus harmani (Loden) n. comb. in a Dutch wetland, with remarks on Tubifex tubifex (Müller) (Annelida: Oligochaeta), Zootaxa 1281, pp. 21-39 : 32-37

Tubifex tubifex (Müller, 1774)

( Figs 4–6 )

Lumbricus tubifex: Müller (1774) , 27.

Tubifex tubifex : Brinkhurst (1971), 453–456, Figs 8A–D. Tubifex tubifex : Holmquist (1983), 189–192, Figs 1–3 .

Description of new material

Full­grown preserved individuals from Korenburgerveen, described in this study, were 9–20 mm long and consisted of up to 100 segments (but of only 39–90 segments when having a tail regenerate or a growth zone). They were 0.5–0.8 mm wide in the genital segments, tapering anteriorly, and only 0.3 mm wide in the tail.

Prostomium bluntly conical, separated with furrow. Intersegmental furrows shallow, without additional rings. Body wall smooth and transparent ( Fig. 4 ).

In anterior dorsal bundles 2–4 smooth, 400–500 μm long hair chaetae (finely barbed when studied with immersion); and 4–5 pectinates, 100–125 μm long ( Fig. 5 E–G). In anterior ventral bundles 3–4 bifids, 100–140 μm long (but only 55–90 μm in II). The latter are thinner (3 μm) and with much longer upper tooth in II–III ( Fig. 5 A); and thicker (up to 6 μm) in subsequent segments, with teeth becoming gradually equal in length (the upper one remaining thinner; Fig. 5 B). Beginning from VII, ventral bifids are 5–7 μm thick, strongly curved, with thick and bent lower tooth, and short and thin upper one ( Fig. 5 C). Similar robust, curved crotchets, 100–125 μm long, occuring by two in postclitellar segments, both in dorsal and ventral bundles ( Fig. 5 D); those in dorsal bundles sometimes accompanied with 1–2 short (about 200 μm) hair chaetae. Four unmodified crotchets in ventral bundles of X, and two in XI.

Clitellum in XI–XII, 20–35 μm thick; the ventral side of XI flat or slightly concave, forming thick ventrolateral folds. Male pores near ventral chaetae in XI ( Fig. 4 ); immediately before them, an unpaired median spot with thinner epithelium ( Fig. 6 A,B). Spermathecal pores occurring laterally between ventral and dorsal chaetae, and nearer to dorsal chaetae ( Fig. 4 ). One abnormal specimen, lacking spermathecae, displayed unpaired median pore in 10/11.

Ventral nerve ganglia with large lateral appendages in some anterior segments (III–V and III–IX in two cross­sectioned specimens, respectively). Pharynx in III with dorsally folded wall; pharyngeal glands sitting on these folds, and also surrounding oesophagus up to V. Chloragogen tissue on oesophagus beginning in VI; intestine dilating in VIII or IX but equipped with blood sinus always from VIII. Transversal blood vessels forming loops in the body cavity in III–X (XI), except VIII in which they have turned into short, thickwalled “hearts”, 20–50 μm wide including their chloragogen cover. The first nephridia seen either in VII or VIII. No coelomocytes.

Testes in X, small or even not visible in sections; sperm scarce in sperm sacs in XI–XIII. Male funnels either funnel­ or sac­like. Vasa deferentia long, forming many loops in egg sacs up to XIII or XIV, appearing annulate owing to presence of orbicular epithelial cells throughout length, bipartite ( Fig. 4 , 5 I,J,L, 6B,C). Their proximal portion is 21–30 μm wide, with 5 μm thick internally ciliated wall, annulate on both sides. The distal portion is wider (30–50 μm), without cilia, its 12–14 μm thick wall being internally annulate but externally smooth.

Atria in XI evidently about 500 μm long, their main portion tubular, winding, and about 50 μm wide; tapering distally to 33 – 40 μm. The proximal portion sometimes reaching XII, 60–110 μm wide, asymmetrically comma­shaped, receiving vas deferens apically, and the short stem of large prostata subapically. Atria covered with a transversally striped muscular layer 3–7 μm thick; a thinner (2 μm) muscular layer covers also the 12 μm wide stem of prostata. Atrial epithelium 5–14 μm thick, columnar in the proximal portion but with longitudinally extending cells in the distal region, ciliated ( Fig. 4 , 5 K, 6A–C).

Penial sacs about 150 μm high and 100 μm wide, barrel­shaped, internally folded ( Fig. 6 A,B). Penes soft, up to 160 μm long; sometimes their tip can be externally visible in male pore. The middle portion of penis, 54 μm wide, shows a ring of thicker (14 μm) epithelium, covered with slightly thickened, verrucose cuticle ( Fig. 5 L, 6B).

Large ovaries in XI. Egg sacs can reach XV or XVI; one specimen displayed also a single egg in X. Female funnels not studied.

Spermathecae present in only three of the eight mature specimens. Spermathecal ampulla rounded, about 450 μm wide, thin­walled, and containing very long vermiform spermatozeugmata up to 70 μm wide in their thickest, and 28 ìm in the narrower portion. Well­separated, soft­walled spermathecal duct longer than ampulla (560 μm), and 40–60 μm wide ( Fig. 5 H).

Comparison of Varichaetadrilus harmani and Tubifex tubifex

T. tubifex from Korenburgerveen represents a large phenotype with particularly thick and curved posterior crotchets (with a very robust lower tooth and a gradually diminishing upper tooth) almost alike those in Psammoryctes spp. V. h a r m a n i can be easily confused with T. tubifex owing to the similar appearance of the posterior crotchets ( Fig. 2 D,G, 5D), as well as the anterior dorsal hair and pectinate chaetae ( Fig. 2 E,F, 5E,F). The similarity extends also to sexually mature individuals that have longitudinal, ventrolateral folds along the edge of the concave ventral surface of the clitellar segments in both taxa. However, these folds are less pronounced in T. tubifex than in V. harmani . In V. harmani their anterior ends reach the spermathecal pores in X but do not extend this far in T. tubifex ( Fig. 1 A, 3B, 4).

The ordinary ventral chaetae in the segments containing the spermathecal and male pores complete the similarity. The shape of the anteriormost preclitellar ventral chaetae in T. tubifex is different from those in V. harmani . In T. tubifex they show a distinctly longer upper tooth, gradually levelling towards the genital segments ( Fig. 5 A–C); in V. h a r m a n i, the teeth are equally long in all anterior ventrals ( Fig. 2 A–C). T. tubifex is a somewhat thicker worm; consequently, its bifid and pectinate chaetae are somewhat larger than those of V. harmani (at least, this was observed in the material from Korenburgerveen). The hair chaetae are relatively longer and thinner in V. h a r m a n i than in T. tubifex .

A good character that can be used to distinguish these two species from one another (but not always noticed in identification process) is the beginning of the intestine: in IX or more posteriorly, at least if the anterior end has not recently regenerated, in V. harmani ( Fig. 1 A,D, 4), but in VIII in T. tubifex , like in most other tubificids ( Fig. 4 ). The position of the “hearts” (in VIII in T. tubifex , and in IX in V. harmani , Fig. 3 A,B) is another somatic difference, although this is not easily visible in whole mounts.

Short penial sheaths with a characteristic shape are distinct in whole­mounted V. harmani ( Fig. 1 A, 2H). The thickened, verrucose cuticle ring on the thickened penial epithelium of T. tubifex (apparently protrusible with the proximal portion of the penis, Fig. 5 L) has also been named penial sheath [e.g., by Brinkhurst (1965, 1971, 1986)], thus causing some confusion. This cuticle ring, although morphologically homologous with a penial sheath, is seldom discernible in whole mounts with glycerine or Canada balsam, unlike in whole mounts with Amman’s lactophenol used by Brinkhurst. Holmquist (1983) denied presence of any penial sheath in T. tubifex , although accepting the occasional presence of granulated cuticle on the penis. This formation should also not be confused with the sheath­like basal membrane of the penial epithelium, described by Holmquist (1978) in Haber speciosus (Hrabĕ, 1931) , and by Baker (1982) in Potamothrix hammoniensis (Michaelsen, 1901) .

The transversally striped appearance is highly characteristic of the thin and winding, bipartite vasa deferentia of T. tubifex , often reaching the postclitellar segments together with the egg sac. In V. harmani , a similar striped appearance is characteristic of the much wider tubulate atria confined to XI and XII while the vasa deferentia do not form any postclitellar loops.

Reproduction by architomy (fragmentation) is prevalent in V. harmani , but does not occur in T. tubifex .

Figures

FIGURE 1. Varichaetadrilus harmani. A, forebody of mature individual. B, C, regenerating anterior ends. D, forebody of immature individual. Scale bar 200 µm.

FIGURE 2. Varichaetadrilus harmani. A – D, ventral chaetae: A, from II, B, from IV, C, from IX, D, from XV. E – G, dorsal chaetae: E, from V, F, from VII, G, from XV. H, penial sheath. I, spermatheca with spermatozeugmata (extracted from body, with uncomplete duct). Scale bars: A – H 20 µm, I 50 µm.

FIGURE 3. Varichaetadrilus harmani, cross sections from genital region. A, end of IX (below) and beginning of X (above). B, X. C and D, XI. Scale bar 50 µm.

FIGURE 4. Tubifex tubifex, forebody of mature individual. Scale bar 200 µm.

FIGURE 5. Tubifex tubifex. A – D, ventral chaetae: A, from II, B, from IV, C, from midbody, D, from tail region. E – G, dorsal chaetae: E, from III, F, from V, G, from midbody. H, spermatheca (partially extracted from body). I – K, cross sections of male duct. I, proximal portion of vas deferens, J, distal portion of vas deferens, K, distal portion of atrium. L, penial apparatus and a stretch of proximal portion of vas deferens in a whole mount. Scale bars: A – G 20 µm, H 200 µm, I – L 50 µm.

FIGURE 6. Tubifex tubifex, cross sections from genital region. A, anterior portion of XI. B, median portion of XI, with penial sacs. C, posterior portion of XI, with atrial ampullae and prostates. Scale bar 50 µm.