Octodrilus complanatus (Dugès, 1828)

Marchán, Daniel F., Piris, Alberto, Tilikj, Natasha, Mautuit, Alejandro Martínez Navarro Ambre, Kutuzovic, Davorka Hackenberger, Decaëns, Tibaud, Novo, Marta & Csuzdi, Csaba, 2025, Mediterranean conquerors: neotypification and phylogeography of the widely distributed earthworms Aporrectodea trapezoides and Octodrilus complanatus (Lumbricidae: Crassiclitellata), Zoological Journal of the Linnean Society 203 (3) : -

Octodrilus complanatus (Dugès, 1828)

Synonymy

Lumbricus complanatus Dugès 1828: 289 .

Octolasium complanatum —Reynolds and Cook 1976: 89. Octodrilus complanatus —Zicsi and Michalis 1981: 256.—Easton 1983: 483.—Pavliček et al. 2003: 457.—Csuzdi et al. 2006: 24.

Neotype

Clitellate specimen. France, Occitanie , Hérault , Montpellier , Jardin des Plantes (Botanical Garden) 43.615ºN, 3.871ºE. 12 June 2022. Collectors: Ambre Mautuit, Alan vergnes, Mathias Brand, Louise Eydoux, Jerome Cortet, Annick Lucas, Sandra Barantal, and Quilina Laffranchi. Deposited in Musée national d’Histoire naturelle (Paris). BOLD sample ID: EW-AM-0004.

Additional material

Two clitellates and two juveniles, France, Occitanie, Hérault, Montpellier, Jardin des Plantes (Botanical Garden) 43.615ºN, 3.871ºE. 12 June 2022. Collectors: Ambre Mautuit, Alan vergnes, Mathias Brand, Louise Eydoux, Jerome Cortet, Annick Lucas, Sandra Barantal, and Quilina Laffranchi. Deposited in Musée national d’Histoire naturelle (Paris). BOLD sample IDs: EW-AM-0003, EW-AM-0093, EW-AM-0149, and EW-AM-0259.

Description of neotype

Eoternal morphology: Body pigmentation absent in ethanol-fixed specimen ( Fig. 5). Length (fixed specimen) 9.3 cm; body cylindrical in cross-section, flatened tail; number of segments 187. Weight (fixed specimen): 4.57 g. Prostomium epilobous, closed. Transverse furrows from segment 10. First dorsal pore at intersegmental furrow 12/13. Nephridial pores aligned close to b. Spermathecal pores at intersegmental furrows 6/7–12/ 13 in c. Male pores in segment 15, punctiform without porophore. Female pores in the middle of segment 14 above b, moderately sized. Clitellum saddle-shaped in segments 28–37. Linear tubercula pubertatis in segments 28–39. Chaetae separate, aa 2, ab 1, bc 0.75, cd 0.5, and dd 4.5.

Internal anatomy: Septa 6/7–13/14 thickened. Lateral hearts in segments 7–11. Calciferous glands in segments 1/2 10–14, with paired diverticula in 10. Crop in segments 15–16, gizzard in segments 17–18. Typhlosole pennate (composed of transverse folds resembling ribs) ( Fig. 5). Male sexual system holandric; testes and funnels enclosed in suboesophageal testes sacs in segments 10 and 11. Four pairs of reniform seminal vesicles in segments 9, 10, 11, and 12, with the later two pairs being larger. Ovaries and female funnels in segment 13; ovarian receptacles (ovisacs) in segment 14. Seven pairs of large, globular spermathecae in segments 6–12. Nephridial bladders ocarina-shaped (sensu Csuzdi and Zicsi 2003).

Variability shown by additional material: Length (fixed specimens): 8.4–10.9 cm. Number of segments: 125–190. Weight (fixed specimens): 3.63–4.70 g. First dorsal pore 11/12–12/13. Clitellum 28–37 or (1/ N 28) 29–37. Number of spermathecae can be uneven in both halves of the animal; specimen EW-AM-0003 showed seven spermathecae in one side and eight in the other (placed in intersegment 5/6), whereas specimen EW-AM-0093 showed six spermathecae in one side (intersegments 7/8– 11/12) and five spermathecae in the other side (intersegments 7/8–12/13).

Remarks Specimens belonging to the same clade as the neotype (thus considered Octodrilus complanatus s.s.) inhabit Spain, France (including Corsica), Italy (including Sicily), and Cyprus.

Two species-level, cryptic lineages exist within Octodrilus complanatus s.l. ( Figs 1, 2; Csuzdi et al. 2018). Tey inhabit northeastern Italy (Friuli and Veneto)– Slovenia – Croatia and Croatia, respectively. Further studies that could detect morphological or ecological differences should lead to their description as independent species.

Phylogeographical and ecological implications Although the redefined Aporrectodea trapezoides and Octodrilus complanatus share some aspects of their phylogeography and biogeography, they showed some remarkable differences.

For instance, Aporrectodea trapezoides showed only a widely distributed invasive haplotype (the clone 1 of Fernández et al. 2012), with all the other haplotypes being geographically restricted. Meanwhile, Octodrilus complanatus showed four different haplotypes shared between different countries, but none of them could be defined as widespread invasive. Tis leads to introduced/non-native populations of Aporrectodea trapezoides around the world being extremely genetically homogeneous, whereas populations of Octodrilus complanatus outside of their putative native range ( Italy) show remarkable genetic diversity. Tis could explain, in part, the success of Octodrilus complanatus as a colonizer although it lacks the innate advantages of Aporrectodea trapezoides (a polyploid, parthenogenetic species).

High genetic diversity in introduced or non-native populations is usually atributed to multiple introductions ( Roman and Darling 2007). In the case of Octodrilus complanatus , its apparent geographical origin in central Italy and its abundance in vineyards ( Gavinelli et al. 2018), in addition to most of its range being restricted to countries surrounding the Mediterranean Sea, suggest that it could have been dispersed passively by the Romans. Te importance of the Roman Empire in the introduction of plant species of agricultural or culinary value is well documented ( Peña-Chocarro et al 2019), with a special emphasis on grape, because viticulture had a central role in their socioeconomical structuring ( Stubert et al. 2020). Te intense trade between Italy and the provinces during roughly six centuries would have provided numerous chances for earthworms to be transported to new territories as cocoons, juveniles, or adult specimens within soil or atached to roots of seedlings. Tis could also explain, in part, the different phylogeographical patern of Aporrectodea trapezoides ; given that their evolutionary origin appears to be closer to the Iberian Peninsula, their genetically diverse populations would not have been in the centre of such a trade network. Te role of past civilizations in the dispersal and distribution of earthworm species has hardly been explored (but see Cunha et al. 2016), but it has a strong potential to explain the phylogeography of highly diverse, widely distributed species, such as Aporrectodea rosea s.l. Savigny, 1826, Eiseniella tetraedra Savigny, 1826 , or the Octolasion cyaneum Savigny, 1826 / lacteum Örley, 1881 species complex (among many others).

Different ecological preferences have already been found for species-level lineages in earthworms ( Spurgeon et al. 2016). Tis not only helps with their delimitation, but it can also provide explanations for their current distribution, success as colonizers, and response to environmental changes. Further sampling and barcoding for populations belonging to Octodrilus complanatus s.l. and Aporrectodea trapezoides s.l. (i.e. including Aporrectodea trapezoides s.s. and Aporrectodea borelii ) would allow their citations to be assigned to the correct lineage, obtaining more accurate predictions than the ones provided by studies lumping them together ( Zeiss et al. 2024).