Helix (gastropod)

Helix is a genus of large, air-breathing land snails native to the western Palaearctic and characterized by a globular shell. It is the type genus of the family Helicidae and one of the animal genera described by Carl Linnaeus at the dawn of the zoological nomenclature. Members of the genus first appeared in the fossil record during the Miocene.

Well-known species include Helix pomatia (Roman snail, Burgundy snail, or edible snail) and Helix lucorum (Turkish snail). Cornu aspersum (garden snail), though externally similar and long classified as a member of Helix (as "Helix aspersa"), is not closely related to Helix and belongs to a different tribe of Helicinae.

Taxonomy

In Linnaeus' 10th edition of Systema Naturae, which marks the beginning of the zoological nomenclature, the generic name Helix had been used for a variety of terrestrial (e.g. Zonites algirus), freshwater (e.g. Lymnaea stagnalis), and marine (e.g. Fossarus ambiguus) gastropods. Later authors restricted the name's use to stylommatophoran species with flattened to globular shells, including zonitids and other groups. In the course of the 1800s, several thousand species of Europe and abroad have been described in Helix. By the early 1900s, the genus was split into many separate genera, leaving only species closely related to its type species Helix pomatia in the genus. However, due to the previously broad concept of the genus, Helix is part of the original combination (basionym) of many gastropod names and there still are many nominal taxa described in Helix whose generic placement remains unresolved (taxa inquirenda), although they clearly do not refer to any species of Helix in its present sense.

Since the 2000s, Helix has been subject to extensive molecular phylogenetic studies and taxonomic revisions. These led to the exclusion of several species, most notably the garden snail, and inclusion of others (H. ceratina, H. nicaeensis). Maltzanella, for long considered a subgenus of Helix, was also formally removed from the genus, but is the sister group of Helix.

Two subgenera are currently recognized: H. thessalica and H. lutescens).

Characters on the genital system have been used to define the genus and its subgenera. Unlike Cornu, the penis of Helix contains two papillae with a central opening. There appears to be a tendency for a shortening of the diverticulum of bursa copulatrix and of the eppiphallus, but there is an overlap with related genera in these characters. Mucous glands adjoining the dart sac are usually richly branched.

Distribution

Helix is a western Palaearctic genus. The species diversity is concentrated to the Balkans and Anatolia, with the greatest phylogenetic diversity in Greece. The natural western distribution limits run through mainland France (Helix pomatia), Corsica (H. ceratina), and Algeria (H. melanostoma). In the north, the natural distribution of H. pomatia reaches central Germany and the southern margins of the North European plain. The southernmost species live in North Africa (H. melanostoma, H. pronuba) and the southern Levant (H. engaddensis). The eastern limits are reached in western Iran and Iraqi Kurdistan (H. salomonica) and in the Caucasus (H. lucorum); H. thessalica reaches through Ukraine at least to the western Russian frontier. but it is unclear which species was studied due to a discrepancy between the stated species and sample origin. The haploid number of chromosomes is 27 (studied species were H. lucorum, H. buchii, H. pomatia, H. gussoneana and H. straminea). In H. pomatia, all chromosomes have median or sub-median centromeres. Small supernumerary chromosomes were reported from H. pomatia from England.

Genital system

thumb|Scheme of the genital system in Helix and related Helicidae. D - love-dart, S - stylophore or dart sac, MG - mucous glands, P - penis, EP - epiphallus, FL - flagellum, BTD - bursa tract diverticulum, BT - bursa tract, BC - bursa copulatrix, SRO - spermatophore-receiving organ, SP - spermathecae, sperm storage organ, FP - fertilization pouch, AG - albumen gland, G - genital opening, HD - hermaphroditic duct, OT - ovotestis, PRM - penis retractor muscle, SO - spermoviduct, V - vaginal duct, VD - vas deferens

The structure of the genital system corresponds in most aspects to that of other Helicidae. Its anatomy and function have been studied in detail in H. pomatia.

As all stylommatophorans, Helix snails are hermaphrodites. Sperms and egg cells are produced in a common gonad, the ovotestis (hermaphroditic gland), which is embedded in the hepatopancreas (digestive gland) near the apex of the shell. Gametes are transported through a hermaphroditic duct (ovotestis duct) to the fertilization pouch–spermatheca complex (carrefour) embedded at the base of the albumen gland. and the bursa copulatrix (gametolytic gland) with its stalk and usually a diverticulum of the stalk. The vagina serves the transport of the foreign spermatophore and of eggs. The bursa is attached by a thin stalk to the vagina (marking the boundary between vagina and the free oviduct). The stalk in most cases bears a diverticulum, a blind tube that receives the front part of the spermatophore if present. The diverticulum has been proposed to be a remnant of a seminal duct that originally transported foreign sperm into the fertilization pouch. Sperm leave the tail of the spermatophore and migrate into the oviduct and then to the fertilization pouch; the vast majority of the sperm does not escape in this way and is digested in the bursa. The male and female parts open into a common atrium and a genital pore positioned ventrally behind the right optic tentacle.

A rare teratological individual with paired male genitalia (penis, epiphallus, flagellum) has been reported from Germany.

Reproduction

thumb|Helix pomatia in the initial phase of the mating sequence.

The aspects of reproduction have been studied primarily in H. pomatia, with limited information from other species.

Mating behaviour has been described several times for H. pomatia. In the initial phase, the two snails raise their feet and press the soles against each other and touch each other's tentacles and mouthparts. This takes 15–30 min. Some time later, the dart shooting takes place, although many matings progress without a love dart being employed. The mucous glands produce a whitish secretion just before the shooting, that contains hormones promoting the compound that improves preservation of foreign sperm in the receiving individual. Then, again after a pause, comes the copulation, usually preceded by several unsuccessful attempts in which the reciprocal insertion of penes is not achieved and the genital organs are partially retracted back into the body. Finally, both individuals simultaneously insert the penes into each other's female opening. Within ca. 4–7 min the spermatophore is formed and transferred, after which the snail disengage and retract the everted genital organs. However, the complete reception of the spermatophore takes another 2–3 hours, during which the snails remain partially retracted and inactive.

It has been reported that only one spermatophore is usually transferred during copulation in H. pomatia, so one animal functions as a male and one as a female in each mating. According to that report it is mostly the older snail who lay eggs, while younger function as males. However, because activity is dependent on climatic conditions, the timing of mating and egg laying differs in some other species.

In H. pomatia, the snails copulate usually with multiple mates. As in other pulmonates, the eggs are rich in galactogen produced by the albumen gland. The eggshell is partially mineralized, with crystals of calcium cabonate in a flexible membrane. Clutch size is given in the literature within the range 3–93. Hatching follows roughly 25–26 (range 18–31 while the range reported for H. albescens (smaller body size than H. pomatia, with larger eggs) is only 7–22 eggs per clutch.

Life history

In H. pomatia, sexual maturity is reached after 2–4 (–6) overwinterings, i.e. at the age of 2–4 (–6) years, but this differs between localities as well as between snails from the same clutch. Adult snails cease to grow and form a thickened lip around the aperture. However, the snails sometimes mate already shortly before the lip is formed. The life span of H. pomatia may reach 30 years in the wild.

The length of the life cycle is dependent on environmental conditions. The time from hatching to first egg laying can be shortened in H. pomatia to just 12–13 months under optimal conditions in the captivity, mainly by skipping hibernation. Observations showed preference for some specific plant species

The activity of H. pomatia takes place mostly during the night, especially in juveniles. A homing behaviour has been observed in H. pomatia. The snails disperse during the season, but tend to return to their hibernation grounds towards its end. During the season, they may have an area where they reside and from where they make excursions to known feeding areas and, if needed, attempts to locate new ones. The snails are able to find their way back from distances of tens of meters. The epiphragm is followed inside the shell by a few additional membranes made of dried mucus. When the animal emerges from the dormancy, it discards the calcareous epiphragm using the posterior part of the foot. Helix lucorum may have up to three calcareous epiphragms, but they are much thinner than in H. pomatia. The hibernation and aestivation takes place in the soil, where the snails bury themselves with the foot. Mammals prey on Helix, too. The known predators include hedgehog, mole, shrew, rodents (Rattus, Apodemus) and the wild boar. Helix snails are also attacked by various beetles and flies. The beetle predators belong to the families Carabidae and Lampyridae. The predation by birds, small mammals, and beetles mostly affects juveniles.

A well known facultative parasite of land snails, including Helix, is the nematode Phasmarhabiditis hermaphrodita. Infection by a parasite, probably an unidentified trematode, may cause parasitic castration when the snails do not possess a gonad. Consequently, the shell growth, which would cease with the onset of sexual maturity, may continue, leading to unusually large shells lacking peristome and possessing about a half of a whorl more than usual. The parasitic mite Riccardoella limacum is found on Helix species.

The kinetoplastid Cryptobia helicis lives in the bursa copulatrix of Helix pomatia.

Bacterial diseases of gastropods including Helix are known, but this field is not well researched.

Influence on other species and the environment

Some bee species build their nests inside empty Helix shells (e.g. Rhodanthidium semptemdentatum).

Human use

thumb|A poster advertising a buy up of Helix pomatia for food processing (Czechia, 2008).

Some species, above all H. pomatia and H. lucorum, are collected for human consumption. The culinary use dates back several millennia and has been evidenced for several species across the genus' range.

Mesolithic shell midden dated to 9370 ± 80 and 8110 ± 90 uncalibrated C-14 years bp and providing evidence of collecting was documented for H. pomatella in Abruzzo, Italy. Helix salomonica was consumed in the Zagros in large amount during the Pre-Pottery Neolithic, with evidence of consumption from ~12,000 BC. In North Africa, shell middens from the Caspian culture containing large amounts of H. melanostoma were found.

Ancient Romans collected snails for food and even held them in enclosures, as described by Marcus Terentius Varro (in De Re Rustica, and repeated by Pliny the Elder). It is believed that the Roman snail H. pomatia was introduced to England by the Romans.

Conservation

Most of the species included in the IUCN Red List are classified as Least Concern. One of the species, H. ceratina, is critically endangered and the present known distribution is limited to a very small area near the Ajaccio airport.

List of extant species

{|class="wikitable sortable"

!Scientific name

!IUCN Red List status

!class="unsortable" width=300pt|Distribution

!class="unsortable"|Picture

|Helix albescens Rossmässler, 1839

|180px

|Helix anctostoma Martens, 1874

|Turkey (Nur Dagi and surroundings), Syria (northwestern)

|Helix ankae Korábek & Hausdorf, 2023

|Turkey (northwestern Anatolia)

|Helix antiochiensis Kobelt, 1896

|Syria

|180px

|Helix asemnis Bourguignat, 1860

|180px

|Helix borealis Mousson, 1859

|Greece

|180px

|Helix buchii (Dubois de Montpéreux, 1840)

|Turkey (northeastern), Georgia, Armenia (northern)

|180px

|Helix calabrica Westerlund, 1876

|Helix ceratina Shuttleworth, 1843

|180px

|Helix cincta O. F. Müller, 1774

|180px

|Helix dormitoris Kobelt, 1898

|180px

|Helix engaddensis Bourguignat, 1852

|Israel, West Bank, Jordan, Lebanon

|180px

|Helix fathallae Nägele, 1901

|Helix figulina Rossmässler, 1839

|180px

|Helix godetiana Kobelt, 1878

|180px

|Helix gussoneana L. Pfeiffer, 1848

|Helix kazouiniana Pallary, 1939

|Helix ligata O. F. Müller, 1774

|180px

|Helix lucorum Linnaeus, 1758

|180px

|Helix lutescens Rossmässler, 1837

|180px

|Helix melanostoma Draparnaud, 1801

|180px

|Helix mileti Kobelt, 1906

|180px

| Helix nicaeensis A. Férussac, 1821

|Turkey

|90px

|Helix nucula Mousson, 1854

|180px

|Helix pachya Bourguignat, 1860

|180px

|Helix pathetica Mousson, 1854

|Helix pelagonesica (Rolle, 1898)

|Helix philibinensis Rossmässler, 1839

|Greece, North Macedonia, Bulgaria (southwestern), Albania (by Lake Prespa)

|180x180px

|Helix pomacella Mousson, 1854

|180px

|Helix pomatella Kobelt, 1876

|Helix pomatia Linnaeus, 1758

|180px

|Helix pronuba Westerlund, 1879

|Egypt, Libya, Tunisia (southern), Greece (Crete and other islands, introduced)

|180px

|Helix salomonica Nägele, 1899

|Turkey (southeastern), Iran (western), Iraq (Kurdistan)

|Helix schlaeflii Mousson, 1859

|Albania (central and southern), Greece, North Macedonia (Galičica)

Helix pseudoligata Sinzov, 1897 (Ukraine. Miocene: Sarmatian)
Helix barbeyana De Stefani in De Stefani et al., 1891
Helix krejcii Wenz in Krejci-Graf & Wenz, 1926
Helix mrazeci Sevastos, 1922
Helix sublutescens Wenz in Krejci & Wenz, 1926
Helix maeotica Steklov, 1966 (Russia: Chechnya: river Gums. Miocene: Maeotian=?Tortonian)
Helix varnensis Toula, 1892 (Bulgaria: Varna. Miocene: Sarmatian)
Helix lucorum supralevantina Wenz, 1942 (Romania. Pliocene)

Some extant species are known from Quaternary deposits. The most studied species in this respect is H. pomatia, where the fossils have been used to document the earliest postglacial occurrences in Central Europe. The earliest record in Czechia was dated directly by radiocarbon to 10,120-9,690 BP (but is likely a few hundred years younger); fossils presumably older than 9,402–9,027 BP or 9,403–9,003 BP were found in Baden-Württemberg, Germany. Such records document the speed at which Helix species may extends their ranges by natural means of dispersal.

The quaternary land snail fossil record in more southern parts of Europe is scarce, but some records of Helix exist. Helix figulina dated ~16,000 BP was recorded from the Greek island Antikythera. Helix borealis shells dated to 8,000–27,000 BP were reported from another island, Gavdos.

Other records come from archaeological contexts.

Phylogeny

The phylogenetic relationships between Helix and related genera as well as the internal relationships within the genus have been so far studied only using partial sequences of mitochondrial genes and of the nuclear rRNA gene cluster.