Helix borealis, sensu Neubert, 2014

Korábek, Ondřej, Kosová, Tereza, Dolejš, Petr, Petrusek, Adam, Neubert, Eike & Juřičková, Lucie, 2021, Geographic isolation and human-assisted dispersal in land snails: a Mediterranean story of Helix borealis and its relatives (Gastropoda: Stylommatophora: Helicidae), Zoological Journal of the Linnean Society 193 (4), pp. 1310-1335 : 1332-1335

APPENDIX 2.

SYSTEMATICS, DISTRIBUTION, VARIABILITY AND ECOLOGY OF HELIX BOREALIS

Helix borealis is generally poorly known, including conchological variability and its potential taxonomic significance. Most of the published accounts are in taxonomic compilations, often repeating earlier information, supplemented by faunistic data (see below for an overview of the literature). The biology and ecology of this taxon has been mostly neglected. Notable exceptions to this pattern are Hesse (1920), providing information on soft body morphology, and Welter-Schultes (1998a), who discussed its phenology and past distribution in Crete and on nearby islands. Kobelt (1895) distinguished, besides typical H. borealis , two more Greek taxa currently considered its synonyms. According to his description, Helix thiesseana Kobelt, 1878 , described from Evvia, should have a more globular shell with darker palatal callus than the nominotypical form and almost missing spiral sculpture. The name H. thiesseana has been sometimes used not only for populations from Evvia, but also for individuals with darker apertures from the Peloponnese peninsula. Helix aetolica Kobelt, 1892 from Aetolia, western Greece (name invalid due to primary homonymy), should be larger with broader shell, darker coloration and less developed spiral sculpture than the nominotypical subspecies. The Turkish populations were never formally described.

SYNONYMY OF HELIX BOREALIS

Helix cincta – d’Audebard de Férussac AEJPJF, 1821– 1822: 29 (quarto edition) [partim: La Gréce, l’Archipel; l’ile de Zante]

Helix cincta – Deshayes, 1835: 160 [partim: de Morée]

Helix ambigua Mousson, 1859: 15 , non Helix ambigua Linnaeus, 1758 (presently Fossarus ambiguus ) [de la Grèce et de la Thessalie …de Corfou et de Céfalonie se retrouve avec toutes ses particularités sur toute la côte de l’Epire, tant à Sayades qua’à Prevesa]

Helix ambigua var. borealis Mousson, 1859: 16 [Ile de Corfou…das les broussailles des rochers de la citadelle]

Helix cyrtolena Bourguignat, 1860: 165 [nom. nov. for Helix ambigua Mousson, 1859 ]

Helix (Pomatia) Thiesseana Kobelt, 1878: 320 [bei Chalcis auf Euböa]

Helix Thiesseana – Kobelt W, 1879–80: 1, pl. 179, figs 1805–1806 [bei Chalcis auf Euböa]

Helix cincta – Westerlund & Blanc, 1879: 79 [Pylos à Navarin, Pyrgos en Elide et dans l’Arcadie]

Helix cincta Var. ambigua – Westerlund & Blanc, 1879: 79 [Iles de Céfalonie et d’Ithaque]

Helix thiesseana – Westerlund & Blanc, 1879: 80 [Ile d’Eubée partie boréale]

Helix Thiesseana – Godet, 1880: 25 [Chalcis (Euboea)]

Helix ambigua – Hesse, 1882: 322 [auf Corfu an der strasse nach Castrades, und auf Zante an der Citadelle]

Helix (Helicogena) ambigua – Boettger, 1883: 317 [Corfu]

Helix (Helicogena) ambigua var. Thiesseae – Boettger, 1883: 329 [Patras; incorrect subsequent spelling of Helix thiesseana Kobelt, 1878 ]

Helix (Helicogena) ambigua var. Thiesseae – Boettger, 1885: 118 [Achaia, Santameri]

Helix [Pomatia] ambigua – Tryon & Pilsbry, 1888: 244, pl. 69, fig. 30 [Corfu, Cephalonia]

H e l i x [Po m a t i a] a m b i g u a Va r. t h i e s s e a n a – Tryon & Pilsbry, 1888: 244, pl. 69, fig. 31 [Achaia; Chalcis, Euboea]

Helix ambigua – Westerlund, 1889: 458 [ Griechenland auf Corfu, Cephalonia, Zante, Ithaka].

Helix ambigua Forma clathrata Westerlund, 1889: 459 [Corfu u. Epirus]

Helix thiesseana – Westerlund, 1889: 459 [ Griechenland bei Chalkis auf Euboea].

Helix (Pomatia) ambigua – Kobelt W, 1891–92: 24, pl. 127, fig. 766 [in Griechenland und Epirus, sowie auf den jonischen Inseln]

Helix (Pomatia) ambigua var. aetolica Kobelt W, 1891 –92: 106, pl. 146, figs. 936–937, non Helix (Macularia) Codringtoni var. Aetolica O. Boettger, 1888 (currently Codringtonia parnassia Roth, 1855 ) [Vrachori in Aetolien; on the plate erroneously labelled as Helix ambigua var. acarnanica ]

Helix ambigua – Schuberth, 1892: 51, pl. 5, fig. 18 [Corfu]

Helix (Pomatia) ambigua – Kobelt W, 1893–97: 778, pl. 215, figs 1–2 [auf der jonischen Inseln, in Epirus und Nordgriechenland]

Helix (Pomatia) ambigua var. aetolica – Kobelt W, 1893–97: 778, pl. 215, figs 2 [Vrachori]

Helix (Pomatia) thiesseana – Kobelt W, 1893–97: 779, pl. 215, figs 3–4 [bei Chalkis auf Euböa]

Helix (Pomatia) thiesseana – Sturany, 1902: 405 [Kalavryta, 800 m Höhe]

Helix (Helicogena) ambigua – Kobelt W, 1902–06: 117, pl. 323, figs 1–4

Helix (Helicogena) ambigua thiesseana – Kobelt W, 1902–06: 118, pl. 215, figs 3–4

Helix (Pomatia) ambigua – Sangiorgi, 1903: 94 [Cefalonia, comune]

Helix (Helicogena) ambigua thiesseana – Hesse, 1920: 183, pl. 654, figs 6–7 [Patras, Cerigo]

Helix (Helicogena) ambigua – Hesse 1915-1920: 251 [ Griechenland, Jon. Inseln, Kreta]

Helicogena cincta subsp. ambigua – Käufel, 1930: 185 [Korfu, Levkas, Kephalonia]

Helix cincta Rasse ambigua – Knipper, 1939: 369

Helix (Helicogena) cincta ambigua – Käufel & Fuchs, 1941: 201 [Zante: Maries, Keri, Skopos]

Helix cincta ambigua – Zilch, 1952: 150

Helix (cincta thiesseana ) – Zilch, 1952: 150

Helix cincta ambigua – Klemm, 1962: 255 [Levkas: Frini, Olivenhain]

Helix (Helix) cincta ambigua – Rähle, 1980: 218 [Kephallinia, Zakynthos]

Helix (Helix) cincta ambigua – Liebegott, 1986: 22 [Skopelos, Kira Panagia, Giura, Piperi]

Helix cincta ambigua – Rähle, 1986: 6 [Ithaki]

Helix (Helix) cincta borealis – Hausdorf, 1993: 45

Helx (Helix) cincta ambigua – Frank, 1997: 141

Helix cincta – Facorellis et al., 1998: 965 [mesolithic: Gioura]

Helix (Helix) cincta – Welter-Schultes, 1998a: 100 [Crete: Anopoli, Alikampos; Gavdos, Gavdopoula]

Helix cincta borealis – Neubert et al., 2000: 113 [ Turkey: between Kaş and Demre]

Helix cincta – Triantis et al., 2008: 475 [island group of Skyros]

Helix cincta – Welter-Schultes, 2012: 611 [partim]

Helix cincta cincta – Psonis et al., 2015: 383 [partim: Crete: Anopoli, Alikampos; Skyros; Peloponnese: Skollis mountain; Kerkyra: Pantokratoras mountain ]

Helix borealis – Neubert, 2014: 98

Helix borealis – Korábek et al., 2015

Helix borealis – Neubert & Korábek, 2015

DISTRIBUTION OF HELIX BOREALIS

Helix borealis has a fragmented distribution. Its main range lies in the Peloponnese, south-western Pindus and the Ionian coast and Islands. On Evvia it is restricted to the north of the island (Neubert, 2014), unless it also lives near Chalkis, as stated in the original description (Kobelt, 1878). It was collected live on Skopelos and Skyros in the northern Sporades. Liebegott (1986) reports it only subfossil from Kyra Panagia, Gioura and Piperi in the northern Sporades; also Facorellis et al. (1998) refers to old shells (older than 7700 BC) from Gioura. On Crete, the species is apparently rare; only two confirmed localities and one probable were reported (Welter-Schultes, 1998a; Psonis et al., 2015). On the islands of Gavdos and Gavdopoula, south of Crete, it is most likely extinct. Shells dated to c. 6000–25 000 BC by radiocarbon analysis demonstrate the autochthonous origin of the species on these islands. However, they also indicate that the species may have been extinct for a long time already (Welter-Schultes, 1998a). In Anatolia, the distribution is broader than indicated by Neubert (2014). The species has been found in the province of Antalya between Kaş, Finike and Kemer (Neubert et al., 2000; own data); the known sites are listed in Table 2.

PHENOTYPIC DIVERSITY OF H. BOREALIS

The variation in conchological characters exhibits some geographic structure, which can be partly identified with the taxa distinguished by Kobelt (1895), partly the varieties have not been formally described. On Corfu and in the vicinity of Igoumenitsa lives a form identifiable with typical H. borealis (Supporting Information, Fig. S1D ). Usually, the three upper bands are separated and well visible on the top of the shell, and the aperture has an ochre, rather than brown, colour. Towards the south (Acarnania and the islands of Lefkada, Kefalonia, Zakynthos) the shell colour is often pale without bands, but with a slightly darker upper half of the shell ( Fig. 1C ; Supporting Information, Fig. S1E ). The colour of the aperture is similar and the coloration is often well developed only on the palatum and upper columella. These two forms were not distinguished from each other by the mitochondrial phylogeny, but together form a distinctive clade sister to the next form ( Fig. 3 ).

Snails similar to the syntypes of H. aetolica live in the northern Peloponnese, Aetolia, Evrytania, and marginally also in western Thessaly ( Fig. 1E ; Supporting Information, Fig. S1F ). They usually have a regularly rounded shell with developed, but often inconspicuous, bands. The upper three usually fuse and their colour does not contrast much with that of the background. The aperture margins are completely dark-coloured. Younger individuals are sometimes covered by brown periostracum, which peels off rapidly, but the periostracum seems to be well developed only at more humid sites. Spiral sculpture varies but is often developed and relatively coarse. To the south of the Peloponnese, the shell surface coloration is often paler, with the background more whitish, and there is a tendency to have better separated and more contrasting bands (Supporting Information, Fig. S1G ). However, the bands may also be reduced ( Fig. 1D ; Supporting Information, Fig. S1H ). This and the previous form are not clearly separable and there are intermediates, but there is also a corresponding phylogenetic south–north divide ( Fig. 4 ).

Populations from Evvia ( Fig. 1B ; Supporting Information, Fig. S1B ) are characterized by pale shells with completely reduced or highly vestigial banding; aperture margins are dark. The upper half of the shell is usually slightly darker than the lower half. The shells often lack spiral sculpture. Columella and aperture margins are relatively slim. This form corresponds fully to H. thiesseana . The analysed individual from Skopelos island (north of Evvia) was also of this type.

The examined shells from Crete (Supporting Information, Fig. S1C ) were small (around 3 cm), had a dark aperture and pale, but developed, banding and vestigial spiral sculpture. The Turkish populations (Supporting Information, Fig. S1A ) are similar to H. thiesseana , and most of the differences may stem from differences in size. The shells are smaller, more compact, and with a smoother surface and finer transverse ribs. Also, unlike H. thiesseana , the Turkish snails often have narrow brown longitudinal bands on the older whorls. Typically, the middle band is the darkest one and is aligned with the suture.

The foot is greyish brown with darker, grey or brown back ( Fig. 1 ). The morphology of the genital organs was described by Hesse (1915–20: 183, pl. 654) from specimens from Patra and Kythira Island. Earlier, Schuberth (1892: 51) mentioned a specimen from Corfu as having a short stem of mucous glands and a curved love dart. Neubert (2014: 101) dissected an individual from south-western Anatolia. We examined three individuals from Evvia, 12 from six localities of the ‘ H. aetolica ’ morphotype, two individuals from Kefalonia and one typical H. borealis from Corfu. The genital system (Supporting Information, Fig. S2 ) does not differ substantially from that of related species (Neubert, 2014) nor are there consistent differences between mitochondrial clades. Short and weakly ramified mucous glands are characteristic. They are usually markedly shorter than the dart sac, but may also be as long as the sac. The love dart is curved towards its tip, with two high and sharp blades in the plane of the curve and two low blunt blades on the sides (the state is unknown for the Cretan-Turkish lineage). The diverticulum branches off in the proximal third to half of the combined pedunculus and bursa stem length. It is usually thick, but its length varies greatly from short (Supporting Information, Fig. S2E , individuals from a locality near Kalavryta, Peloponnese) to almost reaching the length of the bursa stem; sometimes, it is aligned with the bursa stem. The interior of the penis (Supporting Information, Fig. S3 ) also does not provide characters to differentiate between the H. borealis clades. The atrial stimulator is a knob of varying size.

ECOLOGY OF HELIX BOREALIS

The habitats where we found H. borealis varied greatly. On Evvia, the snails were attached to high limestone cliffs. Near Sparti, living specimens were also found on bare exposed limestone rocks. In the ruins of ancient Messene, we found it in the grass between the remains of the buildings. In the western Peloponnese, it is often found on Plio-Pleistocene sand and gravel deposits; on this substrate, we found shells on margins of pine forests. On the western coast, we found it in numbers on sand dunes covered with shrubs, a few hundred meters from the shore. Individuals of the ‘ H. aetolica ’ form with closely related haplotypes were found in a grazed phrygana at low elevation (Supporting Information, Fig. S4A ), fir growths near Karpenisi at c. 1200 m a.s.l. (Supporting Information, Fig. S4B ), and even at a small junk heap under Platanus L. trees in a village. In the north, the species is not limited to limestone. The phenology of the species likely strongly differs between regions. In the south, it is already largely inactive, at least by mid-April, in contrast to the northern part of the range in the mountains in Aetolia. Welter-Schultes (1998a) reports that on Crete the species allegedly emerges after the first October or November rains, only to disappear a few days later.

Although there seems to be substantial plasticity, individual lineages may be more restricted in their tolerances. In fact, broadly tolerant is the ‘ H. aetolica ’ form from Peloponnese, Aetolia-Acarnania, Phocis and Evrytania, which appears common in parts of its range. Some other lineages, such as ‘ H. thiesseana ’ and the Cretan lineage, have restricted distributions and probably narrower (realized) niches. At several sites from Lefkada to the Albanian frontier, we have found only old-looking empty shells in April 2016, but it is impossible to say whether this reflects the season or a recent decline. It is also well possible that most of the mortality occurs when the snails are buried in the soil.

Figures

Figure 1. Live individuals of the Mediterranean clade Helix species: H. cincta (A), H. borealis (B–E) and H. melanostoma (F). A, Cyprus, Kato Drys; B, Greece, Evvia, between Vassilika and Ellinika; C, Greece, Peloponnese, by Rogi near Kalavryta; D, Greece, Kefalonia: Asos; E, Greece, Peloponnese, near Sparti; F, north-western Tunisia, Kef Governorate, near Sers.

Figure 2. Distribution of sampling sites and assignment of locally sampled individuals to major mitochondrial clades of the Mediterranean clade of Helix. Different symbols and colours correspond to different groups as in Figure 4. Areas used for biogeographic reconstructions are shown and labelled with letters corresponding to those in Figure 5. A, northern Adriatic basin; B, northern Africa; C, Apennine Peninsula and Corsica; D, Greece, western Aegean and Crete; E, eastern Aegean and western Anatolia; F, northern Levant.

Figure 3. Phylogeny of the major mitochondrial clades of the Mediterranean clade of Helix inferred from a concatenated alignment of partial mitochondrial COI and 16S gene sequences. A, neighbour-net network; B, maximum likelihood tree. Branch labels in B indicate SH-aLRT support values, standard bootstrap proportions from 1000 pseudoreplicates, and posterior probabilities from a Bayesian analysis, respectively.

Figure 4. Detailed unrooted phylogeny of the Mediterranean clade inferred from a concatenated alignment of partial mitochondrial COI and 16S gene sequences. The tree is a 50% majority rule consensus of the posterior of a Bayesian analysis with MrBayes. Branch labels indicate SH-aLRT support values, standard bootstrap proportions from 1000 pseudoreplicates, and posterior probabilities from a Bayesian analysis, respectively.Only posterior probabilities are shown for some branches near the tips due to space constraints. Tips are labelled by isolate codes (our data) or GenBank accession numbers of 16S sequences (data from other authors) and two-letter ISO country codes; where needed for interpretation of the results, geographic origin of the sample is given, usually by the closest significant town. Red arrowheads point to samples presumed here to be taken outside of the native range of the respective species. Clade symbols and colours correspond to Figure 2. Abbreviations: anct, anctostoma; thiess, thiesseana; undesc, undescribed; valent, valentini.