Lumbricillus antarcticus, STEPHENSON, 1932

Klinth, Mårten J., Rota, Emilia, Martinsson, Svante, Prantoni, Alessandro L. & Erséus, Christer, 2022, New insights into the systematics of Lumbricillus and Marionina (Clitellata: Enchytraeidae) inferred from Southern Hemisphere samples, including three new species, Zoological Journal of the Linnean Society 194 (4), pp. 1103-1133 : 1111-1114

LUMBRICILLUS ANTARCTICUS STEPHENSON, 1932

( FIGS 3 , 4A–C )

Lumbricillus antarcticus Stephenson, 1932: 256–257 , fig. 8.

Lumbricillus sp. 2 – Prantoni et al., 2018 (confirmed by comparison of COI data).

Lumbricillus cf. antarcticus – Lee et al., 2019: 4–5, fig. 4.

Type material: BMNH 1933.2.23.899–900, two mature sectioned specimens (studied), BMNH 1931.06.23.89/90 (in alcohol, not studied). Syntypes. Loc. Wilson Harbour, South Georgia. Leg. ‘Discovery’ 1925–1927 ( Stephenson, 1932), see Boros & Sherlock (2010).

Type locality: Wilson Harbour , South Georgia Island. According to Stephenson (1932), the sample was labelled as ‘moss dwellers’, but the sampling station was listed as ‘hauled’ from 15–45 and 26–83 m using a beam trawl .

New material examined: SMNH 198144–198147 ( CE 12479–CE12482), four mature specimens collected intertidally in 2010 from South Georgia Island, and SMNH 198148 ( CE 34641) and SMNH 198149 ( CE 34643), two mature specimens collected in 2015 from algae on intertidal rocks at Snow Island (South Shetland Islands, Antarctica). All new specimens are mounted on slides and serve as vouchers of genetic data. For details on collection and GenBank accession numbers for COI barcodes (and other genes for some specimens), see Table 1 and the Supporting Information ( Table S1 ).

Diagnosis: This species, now differentiated by a unique COI barcode, is a member of the L. lineatus group, meaning that it has testis sacs forming clubshaped lobes arranged in a fan shape, and spindleshaped spermathecae. It can be distinguished from other L. lineatus group members by combining: (1) short sperm funnel, 1.0–1.5 times longer than wide; (2) spermatheca that widens gradually from the ectal pore, to be widest midway or two-thirds in and gradually tapers towards the oesophagus, where it connects to the latter; and (3) the geographical range, in that it is known only from the Subantarctic Islands and Antarctic Peninsula.

Description: Length of first 20–26 segments is 3.1– 7.1 mm (fixed, amputated specimens); first 15 segments 2.0– 4.3 mm long; width at clitellum is 0.45–0.67 mm. Chaetae sigmoid ( Fig. 3A ). Upper bundles dorsolateral (above the lateral line but closer to it than the ventral bundles), with (three) four to six (eight) chaetae anterior to clitellum, and three to six (eight) chaetae in postclitellar segments, at least to XXVI. Ventral bundles with (four) six to eight (ten) chaetae anterior to clitellum, and (four) five to seven (nine) chaetae posteriorly. Longest measured chaetae of each worm 70–85 µm long, ~3–5 µm wide. Epidermis loosely covered with rows of pale gland cells. Clitellum with reticulate pattern of gland cells, extending over XII–XIII, absent ventrally.

Coelomocytes numerous, 15–20 µm long; round, oval or spindle shaped; granulated with distinct nucleus. Paired pharyngeal glands ( Fig. 3B ) in IV, V and VI; each pair converging dorsally, but connections not discernible. Dorsal vessel originating in XIII, with peristomial bifurcation. Nephridia ( Fig. 3C ) ~85– 110 µm long, observed in 7/8–9/10 and postclitellar segments. Anteseptale small, consisting of funnel only. Postseptale oval, tapering into posteroventral efferent duct. Brain with posterior incision.

Male genitalia paired ( Figs 3D , 4C ). Testes originating in anterior of XI, with testis sacs forming regular club-shaped lobes extending forwards into IX, sometimes VIII. Sperm funnels in XI, 175–250 µm long, 150–235 µm wide, making them about as long as wide or 1.5 times longer than wide; funnels tapering towards vasa deferentia. Most of vasa irregularly coiled in and confined to XII, 15–20 µm wide. Penial bulbs round, 100–140 µm in diameter. Ovaries in XII. One to three mature eggs present at a time.

Spermathecae ( Figs 3E, F , 4A, B ) in V, spindle shaped, with short ectal duct covered in musculature and rapidly widening into ampulla. Ampulla with midway bend dividing it into two sections; ectal part slightly narrower than ental part; ental part connecting with oesophagus. Sperm in lumen of entire ampulla; heads of spermatozoa embedded in wall of ampulla; more concentrated in the ental part. Spermathecae 270–390 µm long, 25–35 µm wide at the ectal duct, 75–115 µm wide at widest part of ampulla. Gland cells surrounding ectal duct, forming compact mass 100–145 µm in diameter at its widest part. Midventral subneural glands observed in XIII–XIV( XV), 75–130, 85–130 and 55–95 µm long, respectively.

Geographical distribution and habitat: Stephenson (1932) originally described this species from South Georgia Island, which is where most material comes from, in addition to two specimens that came from Snow Island (South Shetland Islands) near the Antarctic Peninsula, not far from King George Island, from where it was reported from a tidal pool by Lee et al. (2019). It should be noted that Stephenson’s material was labelled as ‘moss dwellers’ and was sampled (‘hauled’) from 15–45 and 26–83 m using a beam trawl. The species is also reported in the literature from Heard Island, the Kerguelen Islands, Macquarie Island and the South Orkney Islands, where the samples from Macquarie Island were from freshwater ( Dartnall et al., 2005), but we have not been able to confirm these reports by comparing morphology or genetic data.

Remarks: Our specimens, sampled from the intertidal zone on South Georgia Island and Snow Island, agree with the original description, particularly in the short sperm funnels, but they have on average more chaetae per bundle, the penial bulbs are smaller, and the spermathecal ampullae of our specimens are widest in their ental portion rather than ectally as in the illustration by Stephenson (1932: fig. 8). In these respects, our specimens are similar to those of Lee et al. (2019), who motivated the uncertain identification L. cf. antarcticus owing to these differences. However, in Stephenson’s sectioned specimens, the penial bulbs are of the same size as in our material, and the proportions of the spermathecae also agree, making us confident that our specimens and those of Lee and Stephenson are conspecific. In his publication, Stephenson also recorded L. lineatus from South Georgia and considered it close to L. antarcticus , but distinguished by the much longer sperm funnels; five to ten times as long as wide for L. lineatus against 1.25 times as long as wide for L. antarcticus (matching the sperm funnels of our specimens). The short sperm funnels seem to distinguish L. antarcticus from most other species in the L. lineatus group. There are a few species from the Northern Hemisphere with sperm funnels only 1.5 times longer than wide: Lumbricillus alaricus Shurova, 1974 from the Kurile Islands, Lumbricillus fennicus Nurminen, 1964 from northern Europe, Lumbricillus parabolus Shurova, 1978 from the eastern coast of Kamchatka and L. rubidus from east Murmansk (Barents Sea). Lumbricillus antarcticus does not have the lobed sperm funnels of L. fennicus or L. parabolus and lacks the ‘muscular bulb’ surrounding the spermathecal ectal duct in L. rubidus . The brief description of L. alaricus is similar to that of L. antarcticus , but with fewer chaetae on average and a smaller ectal gland on the spermathecae. All four mentioned species are separated from L. antarcticus by huge geographical distances, and L. fennicus and L. rubidus were both included in the phylogeny and were not found to be related closely to L. antarcticus .

The following three Lumbricillus species, all described from the South Shetland Islands in the Subantarctic, are similar to L. antarcticus and have only slightly longer sperm funnels (two to three times longer than wide). The first, Lumbricillus sejongensis Lee et al., 2019 , has spermathecae with less distinct transition from ectal duct to ampulla, and a more inflated ampulla than L. antarcticus . The two other candidates, Lumbricillus incisus Wang & Liang, 1997 and Lumbricillus healyae Rodriguez & Rico, 2008 , have both been found in freshwater and are morphologically similar to one another. Lumbricillus incisus has fewer chaetae per bundle and has penial bulbs with a midway constriction, separating it from L. antarcticus . Lumbricillus healyae is described as having sacshaped spermathecal ampullae attaching directly to the oesophagus without tapering into an ental duct, whereas we consider those of L. antarcticus to be more spindle shaped and to taper into an ental duct. However, this shape can be influenced by the extension or contraction of the worm [compare our Fig. 3E, F , in addition to Rodriguez & Rico’s (2008) figs 3c and 4e, f for L. healyae ; our Fig. 3F is similar to their fig. 4f]. Nevertheless, L. antarcticus can be distinguished from L. healyae by not having strong dorsoventral muscle strands surrounding the penial bulbs (described as possibly unique for that species) and shorter sperm funnels, as mentioned earlier.

Finally, the closest species to L. antarcticus , both morphologically and genetically, is the new species L. nivalis , which we describe below. A comparison between these two species can be found under the Remarks section of this new species.

Figures

Figure 3. Lumbricillus antarcticus. A, chaetal bundle (CE12480). B, anterior part of body (CE12479). C, nephridium (CE12480). D, genitalia (CE12479). E, F, spermathecae (CE12479 and CE34641). Abbreviations are defined under ‘Taxonomy’. Scale bars: 100 μm.

Figure 4. Lumbricillus antarcticus and Marionina colpites. A–C, L. antarcticus, sectioned specimen BMNH 1933.2.23.899. A, B, spermatheca. C, genitalia. D–F, M. colpites. D, male pore and associated glands (BMNH 1933.2.23.888). E, F, spermatheca (BMNH 1933.2.23.886 and BMNH 1933.2.23.888). Abbreviations are defined under ‘Taxonomy’. Scale bars: 100 μm.