Lumbricillus lineatus ( Mueller , 1774)

Klinth, Marten J., Rota, Emilia & Erseus, Christer, 2017, Taxonomy of North European Lumbricillus (Clitellata, Enchytraeidae), ZooKeys 703, pp. 15-96 : 20-22

Lumbricillus lineatus ( Mueller, 1774) Figs 2, 3A

Lumbricus lineatus Müller, 1774: p. 29.

Lumbricillus lineatus ; Erséus et al. 1999; Erséus et al. 2010; Klinth et al. 2017.

Pachydrilus claparedeanus Ditlevsen, 1904: pp. 431-435, figs 28 a–b.

Lumbricillus agilis Moore, 1905: pp. 395-397, pl. XXXIII, figs 23-28.

Lumbricillus lineatus partim; Michaelsen 1900: p. 80; Welch 1917: pp. 123-130; Nielsen and Christensen 1959: pp. 100-102, figs 109-112.

" Lumbricillus lineatus L2"; BOLD (unpublished records)

Non Pachydrilus lineatus ; sensu Backlund 1947: pp. 3-5, figs 1-2 (see Lumbricillus latithecatus sp. n. below).

Type material (neotype).

Lumbricillus lineatus was described long before reference to types had become common practice and there is no remaining original material ("Typus amissus" in Nomenclatura Oligochaetologica). We designate SMNH Type-8931 [former SMNH 152751] (CE1894) as a neotype of this species. It is a whole-mounted voucher of a sexually mature and DNA-barcoded worm (COI barcode is KU894040 in NCBI/GenBank; Klinth et al. 2017) from the Baltic Sea, Öland, Mörbylånga, Skärlöv fishing harbor, on beach with mixed shelly sand, pebbles and organic material, 56.4241 N, 16.5815 E, collected 10 June 2006 by Lisa Matamoros, Sweden. Our decision to designate this neotype is further discussed in Remarks below.

Other material examined.

SMNH 152742 (CE1640), one mature specimen from Sweden; SMNH 152744 (CE1694), one mature avesiculate triploid specimen from Spain; ZMBN 107872 (CE12043), ZMBN 107875 (CE21688), ZMBN 107879 (CE22604) & ZMBN 107880 (CE22605), four mature specimens from Norway; ZMBN 107878 (CE21986), one mature avesiculate triploid specimen from Norway. For information on collection localities and GenBank accession numbers for COI barcodes see Appendix 1.

Description.

Orange, red or pink worms. Length (fixed worms) more than 2.2-5.5 mm (amputated specimens), first 15 segments 2.1-2.8 mm long, width at clitellum 0.45-0.75 mm. More than 14-38 segments. Chaetae sigmoid (Fig. 2A). Upper bundles dorsolateral, with 3-6 chaetae anterior to clitellum, 3-7 chaetae in postclitellar segments. Ventral bundles with 4-8 chaetae anterior to clitellum, 3-7(8) chaetae posteriorly. Each worm’s longest measured chaetae 50-75 µm long, about 3-5 µm wide. Clitellum extending over XII– 1/2XIII/XIII. Head pore not observed.

Coelomocytes, in some specimens numerous, 10-20 µm long, round, oval or spindle-shaped, granulated with distinct nucleus. Paired pharyngeal glands present in IV, V and VI; each pair converging dorsally (Fig. 2B). Dorsal vessel originating in XII–XIV. Nephridia observed in VIII–X and XIII–XX, about 85-110 µm long. Anteseptale small, consisting of funnel only. Postseptale oval, tapering into posteroventral efferent duct. Brain with posterior incision.

Male genitalia paired (Fig. 2D). Testes originating in XI, extending forwards into X, sometimes IX, with testis sacs forming regular club-shaped lobes, except in two “avesiculate” specimens (SMNH 152744 and ZMBN 107878) which have atrophic testes. Sperm funnels in XI, 215-420 µm long, 125-185 µm wide, making them about 1.5-2.5 times longer than wide, funnels tapering towards vasa deferentia. Most of vasa irregularly coiled in XII, 15-20 µm wide. Penial bulbs round, 65-140 µm in diameter. Ovaries in XII. One to six mature eggs present at a time.

Spermathecae (Figs 2C, 3A) in V, spindle-shaped, without distinct ampulla. Ectal duct very short, widening into ampulla. Ampulla with constriction midway dividing it into sections, ectal part narrow, ental part wider, sometimes circular, connecting with oesophagus. Sperm in lumen of ectal part of ampulla, heads of spermatozoa embedded in wall of ental part of ampulla, forming aggregates. Spermathecae 220-275 µm long, 60-125 µm wide at widest part of ampulla. Gland cells surrounding ectal duct at pore, forming compact mass, glandular body 80-150 µm in diameter at its widest part. Two midventral subneural glands in XIII–XIV, 60-110 µm and 60-95 µm long, respectively.

Details of neotype.

Length 3.3 mm (amputated specimen), first 15 segments 2.4 mm long, width at clitellum 0.45 mm. 20 segments. Dorsal bundles with 4-6 chaetae anterior to clitellum, 3-4 chaetae in postclitellar segments. Ventral bundles with 6-8 chaetae anterior to clitellum, 3-5 chaetae posteriorly. Longest chaetae 50 µm, about 3 µm wide. Clitellum extending over XII–XIII.

Coelomocytes 15 µm long. Dorsal vessel originating in XIII. Nephridia observed in VIII–X and XIII–XX, about 110 µm long.

Testes originating in XI, extending forwards into X. Sperm funnels folded, length and width unclear. Vasa deferentia 15 µm wide. Penial bulbs 115 µm in diameter. No mature eggs observed.

Spermathecae (Fig. 2C) 270 µm long, 120 µm wide at widest part of ampulla. Glandular body at ectal pore 115 µm in diameter at its widest part. No midventral subneural glands observed.

Geographical distribution including BOLD data.

Genetically identified from the Netherlands, Norway, Spain and Sweden; also recognized from Canada (BIN-numbers BOLD:AAF9630 & BOLD:ACV7068). This species has historically been widely reported from Europe and North America, and even from the southern hemisphere ( Stephenson 1932b).

Remarks.

Lumbricillus lineatus , possibly the first ever described enchytraeid, has an interesting history and was for a long time poorly defined as a species. It was given the name Lumbricus lineatus by Müller (1774) who described it as abundant on the shores of the Baltic Sea. Müller classified the worm under “Setosa”, and gave a brief description of its circulatory system and short protruding chaetae. In the same work, he refers to a worm that he previously described ( Müller 1771), which he found on sandy shores of the Baltic and particularly among the rotting seaweed by the ramparts of Copenhagen, where he did most of his work. However, he classified that worm in Gordius , referred to it as a Faden Wurm (nematode) said to lack any segments or ring, and he failed to mention anything about chaetae. It is therefore difficult to say if Müller simply missed those characters or if the worm from 1771 was something different. Nevertheless, as Müller worked with live material, it is most plausible that the type locality for the first described Lumbricillus lineatus is around Copenhagen. Unfortunately, we do not have any specimens from Copenhagen, but we have found that our molecularly defined L. lineatus is common throughout the Baltic Sea. For the sake of finally defining the true L. lineatus and connecting it to a molecular profile, we decided to designate one of our specimens from Öland in the Baltic Sea as a neotype.

The specimens of L. lineatus in this study were smaller than the ones in the re-description by Nielsen and Christensen (1959) and the sperm funnels were shorter in relation to their length. However, the shape of the spermathecae, number of chaetae and segments conformed well with these authors’ description. Furthermore, both the vesiculate and avesiculate forms of the species were observed, as has previously been noted to occur in L. lineatus ( Nielsen and Christensen 1959, Christensen 1961), further supporting the designation of a neotype from our material. Christensen and O’Connor (1958) were the first to describe diploid vesiculate and triploid avesiculate forms of L. lineatus and their intriguing life histories (see also Christensen 1960). While the diploid form has normal gametogenesis and is amphimictic, the triploid form is dependent on copulation with the diploid form, which acts as sperm donor, to produce offspring. Furthermore, the sperm from the diploid form does merely activate the egg of the triploid individual, without fertilizing it. Instead, oogenesis in the triploid cytotype follows a peculiar pattern of chromosome divisions and mergings that results ultimately in the restoration of triploid nuclei. The relationship between the two forms has been described as an obligatory co-existence ( Christensen 1960). To further complicate things, tetra- and pentaploids have also been observed within L. lineatus . The tetra- and pentaploids have testis sacs that are smaller than those of diploids but larger than those of triploids. Furthermore, the sperm funnels are smaller in tetra- pentaploids than in di- and triploids. Apparently, the testes sacs of tetra- and pentaploids sometimes produce sperm which can activate the eggs of all polyploid forms ( Christensen et al. 1978). Unfortunately, we did not determine the ploidy level of our sampled specimens, but we did not observe any genetic distinction between the vesiculate and avesiculate forms, neither in COI nor in ITS sequences (Klinth at al. 2017).

Lumbricillus lineatus is morphologically most similar to L. verrucosus and L. latithecatus sp. n. (compare spermathecae in Fig. 3 and see Remarks for these species), but also superficially similar to the other members of the group we have chosen to call the linaetus group. Genetically it is closely related to L. rutilus Welch, 1914 and L. latithecatus sp. n. ( Klinth et al. 2017; where L. latithecatus is called L. sp. E) (Fig. 1).