Enchytraeus moebii ( Michaelsen, 1885 )

Erséus, Christer, Klinth, Mårten J., Rota, Emilia, De Wit, Pierre, Gustafsson, Daniel R. & Martinsson, Svante, 2019, The popular model annelid Enchytraeus albidus is only one species in a complex of seashore white worms (Clitellata, Enchytraeidae), Organisms Diversity & Evolution (New York, N. Y.) 19 (2), pp. 105-133 : 123-124

Enchytraeus moebii ( Michaelsen, 1885) ( Figs. 9–10 )

Archenchytraeus möbii Michaelsen, 1885: pp. 237–239 .

Enchytraeus möbii ; Michaelsen 1886: pp. 1–52, pl. I, figs. 1–16, pl. II, figs. 1–7, pl. III, figs. 1–10.

E. albidus partim; Nielsen and Christensen 1959: pp. 91– 92, figs. 95–100.

E. albidus B clade A^; Erséus and Gustafsson 2009.

E. albidus ; Christensen and Glenner 2010: table 1.

E. albidus B EA-DK^; Arslan et al. 2018.

Material examined SMNH 172878–172880 ( CE965 , CE972, and CE973 ) , SMNH 172883 ( CE2789 ) , and SNHM 172885 ( CE2966 ) , 5 specimens from Swedish seashores ; SMNH 172876 ( CE1686 ) , 1 specimen from algal compost in Galicia, Spain. All specimens sexually mature and COI barcoded. For more details, including GenBank accession numbers for genetic data, see Table 1 .

Diagnosis Several chaetal bundles with more than three chaetae; sperm funnels 1.5–3.5 times longer than wide; vasa deferentia with uniform cell wall thickness; penial bulbs larger than accessory glands; spermathecae without diverticula.

External characters Color white. Length of first 17–35 segments,> 3–9 mm (fixed, amputated specimens); first 12 segments (anterior end to clitellum) 2.3–3.8 mm long; width at clitellum 0.43–0.89 mm. Chaetae straight or slightly curved. Lateral bundles with 3–4 chaetae anterior to clitellum, 2 in XII, 2–3 chaetae in postclitellar segments. Ventral bundles with 3–4(5) chaetae anterior to clitellum, missing in XII, 2–3 chaetae in postclitellar segments. Chaetae longest in ventral bundles anterior and posterior to XII, measuring 60–120 by 5– 8 μm. Clitellum extending over XII–½XIII or –¾XIII. Head pore not observed. Epidermis with transverse rows of gland cells.

Internal characters Coelomocytes numerous, 10–15 μm long, round, oval, or spindle-shaped, granulated and with distinct nucleus. Paired pharyngeal glands present in IV, V, and VI. All pairs with secondary lobes, first and second pairs possibly with narrow dorsal connection, third pair not connected. Esophageal appendages (peptonephridia) extending from dorsal wall of esophagus in III. Dorsal vessel seemingly originating in XIV or XV. Nephridia in 6/7–9/10 and from 13/14 to 21/22 at least, about 80 μm long, anteseptale consisting of funnel only, postseptale elongate ovoid, with efferent duct originating posteroventrally. Brain posterior margin straight or slightly indented.

Male genitalia paired. Testes in XI, paired, each enclosed in a sac and extending forwards into X. Sperm funnels in XI, 295–420 μm long, 120–265 μm wide at the widest point, making them about 1.5–3.5 times longer than wide, funnels tapering towards vasa deferentia. Vasa irregularly coiled in XII– XVI, of about uniform width (20–25 μm) throughout, with 2.5–5 μm thick wall. Vasa ciliated, without conspicuous musculature. Vasa seemingly not penetrating penial bulbs. Ventral surface of XII with invaginations creating two recesses with overhanging lips. Penial bulbs compact, round, 110– 180 μm in diameter, sheathed with muscles, and surrounded by accessory glands much smaller in size ( Fig. 9a ). Ovaries in XII. About one to five mature eggs present at a time.

Spermathecae in V. Ectal pore at lateral line or just above. Ectal duct short to moderately long, covered with gland cells and abruptly widening into sac-like ampulla ( Fig. 9b–c ). Ampulla usually rounded, ental connection with esophagus uncertain, no observed diverticulum. Sperm in lumen of ampulla and sometimes in ectal duct; heads of spermatozoa embedded in wall of ental part of ampulla, forming aggregates. Spermathecae 205–225 μm long, 80–90 μm wide at widest part of ampulla. Gland cells surrounding ectal duct, forming compact mass 80–125 μm in diameter at its widest part; glands seemingly extending along entire duct (but see Fig. 10 , and B Remarks^). No obvious midventral subneural glands observed.

Remarks Our specimens agree for the most part with Michaelsen’ s extended description of E. moebii (1886), but they have on average fewer chaetae per bundle and sometimes shorter sperm funnels. Our material is identified as this species primarily based on the combination of penial bulbs being larger than the accessory glands, and spermathecae having duct and ampulla of equal length but without diverticula. Obviously using sectioned material, Michaelsen (1886) illustrated a short inner part of the spermathecal duct as being devoid of gland cells ( Fig. 10 ). This could not be discerned in our slide-mounted specimens, but it may be a general feature of this taxon.

E. moebii was synonymized with E. albidus by Nielsen and Christensen (1959), but the molecular data in this study support considering the two as separate species. Furthermore, unlike E. moebii , E. albidus s. str. has penial bulbs of about the same size as the accessory glands, sperm funnels quite elongate in relation to their width, and spermathecae with diverticula, making it possible to distinguish these two species morphologically.

E. moebii is morphologically most similar to E. albellus sp. nov. (described below), and these two species do not seem to be distinguishable with regard to chaetal size and number, or sperm funnel proportions ( Table 3 ). Both species have penial bulbs that are much larger than the surrounding accessory glands (compare Figs. 9a , 10 , and 11d). However, the spermathecae of E. moebii lack diverticula, whereas those of E. albellus usually have at least one dorsal diverticulum. Furthermore, the vasa deferentia of E. moebii have rather uniform width and wall thickness, whereas the middle portion of the E. albellus vasa is wider and has thicker walls than the ental and ectal portions. The dimensional contrasts between the different sections of the vasa deferentia are even more prominent in our specimens of E. cf. krumbachi (described below), which also makes the latter species distinguishable from E. moebii .

E. moebii was originally described from decomposing seaweed in the Kiel Bay, Baltic Sea. Our specimens were partly from the Baltic Sea (sites around the island of Öland), but we also found the same lineage along a long stretch of the North- East Atlantic coast. We have decided not to designate any neotype for this species as we do not have material from the type locality.

Geographical distribution of genetically verified specimens Norway (including a BOLD record from Oslofjorden , NOENC236-15 ) , Sweden, and Spain in the present study; also recognized from Denmark (GenBank GU 453370; see Christensen and Glenner 2010). This species is represented in BOLD by BIN: AAM5959. The type locality is on the Baltic coast of Germany.

Habitat Seashores and salt marshes, but also in the intertidal zone; typically in decomposing seaweed and algae.

Figures

Fig. 9 Enchytraeus moebii a male copulatory apparatus. b–c Spermathecae. ag accessory glands, ed ectal duct, eg ectal gland, mu musculature, pb penial bulb, sa spermathecal ampulla, sm sperm, vd vas deferens. Scale bar 100 μm

Fig. 10 Enchytraeus moebii 3 male apparatus and 7 spermatheca; from Michaelsen (1886; pl. II figs. 3., 7.)