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Limax maximus

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Limax maximus
Scientific classification Edit this classification
Domain: Eukaryota
Kingdom: Animalia
Phylum: Mollusca
Class: Gastropoda
Order: Stylommatophora
Family: Limacidae
Genus: Limax
Species:
L. maximus
Binomial name
Limax maximus
Synonyms

[3]

  • Limax cinereus Lister, 1678
  • Limax cinereus O. F. Müller, 1774 (partim)
  • Limacella parma Brard, 1815
  • Limax antiquorum Férussaac, 1819 (partim)
  • Limax maculatus Nunneley, 1837 (non maculatus Kaleniczenko, 1851)
  • Limax cellarius (d'Argenville) Lessona et Polonera, 1882
  • Limax carbonarius albanicus Jaeckel, 1954

Limax maximus (literally, "biggest slug"), known by the common names great grey slug and leopard slug, is a species of slug in the family Limacidae, the keeled slugs.[4] It is among the largest keeled slugs, Limax cinereoniger being the largest.

Limax maximus is the type species of the genus Limax. The adult slug measures 10–20 cm (3.9–7.9 in) in length and is generally a light greyish or grey-brown with darker spots and blotches, although the coloration and exact patterning of the body of this slug species is quite variable.

This species has a very unusual and distinctive mating method, where the pair of slugs use a thick thread of mucus to hang suspended in the air from a tree branch or other structure.

Although native to Europe, this species has been accidentally introduced to many other parts of the world, first discovered outside its native range in Philadelphia, USA in 1867.[5] [clarification needed]

Description

External anatomy

The body length of the adult is 10-20 cm (4-8 in).[6]

The greater part of the body is rounded, but there is a short keel on its tail, with about 48 longitudinal rows of elongate, detached tubercles.[7] The body color is pale-grey, ash-colored, brownish or sometimes yellowish-white. The body is longitudinally streaked or spotted with black. The pattern of spotting is variable. The shield is always black-spotted. The sole of the foot is a uniform ash or yellowish-ash color.[8] The foot-fringe is pale, with a row of minute submarginal blackish tubercles.[7]

Drawing of color variability of Limax maximus

The tentacles are very long and slender.[7] The reproductive pore is near the base of the right upper tentacle.[9]

The shield is oblong, about one third of the total length of the animal. The shield is rounded in front, angular behind, and forming an angle of about 80 degrees when in motion, usually of a similar tint to the body, but boldly marbled or maculate with black, somewhat concentrically and interruptedly ridged around a sub-posterior nucleus.[7]

The pneumostome is just posterior to the midpoint of the mantle, as it is in all Limacidae.

The mucus is colorless and iridescent, and not very adhesive.[7]

Although color varieties have no actual taxonomic significance, a large number of color varieties have been described, prominent among them being the varieties serpentinus, vulgaris, cellarius (typical), johnstoni, maculatus, ferrussaci, obscurus, fasciatus and rufescens, of Alfred Moquin-Tandon, and cornaliee, of Pini.[8][10]

Internal anatomy

Reproductive system of Limax maximus:
HG = hermaphrodite gland = ovotestis
HD = hermaphrodite duct
AG = albumen gland
SO = spermoviduct
OV = oviduct
VD = vas deferens = sperm-duct
RS = receptaculum seminis
P = penis
PRM = penis retractor muscle
G = genital pore

The shell of Limax maximus is reduced and internal, under the shield. The occurrence of this internal shell was known to Pliny the Elder; the shell was used by the ancient physicians for the sake of its carbonate of lime.[11]

The calcitic shell is situated beneath the hinder part of the shield, and is perceptible through the skin. The color of the shell is whitish. The shape of the shell is oblong-oval and thin, slightly convex above, and correspondingly concave beneath, with a membranous margin. The apex or nucleus is at the posterior margin but inclined towards the left side, and forming the apophysis by which the shell is organically attached to the animal.[7] The length of the shell is 13 mm (1⁄2 in) and the width of the shell is 7 mm (1⁄4 in).[7] Shells of different Limacidae species are undiagnostic: in other words, they are not helpful for identification purpose.

Digestive system: The formula of the radula is: 62-73/ × 138–157.[3] The intestine has six convolutions and is without a caecum.[9] Of the six convolutions of the intestine, four are imbedded in the liver, and two hang freely in the body cavity.[9]

The nervous system is composed of the typical ganglia. The pedal ganglia are placed beneath the radula sac and joined by an anterior and a posterior commissure. The abdominal ganglion lies a little to the right of the median line. The visceral ganglia occupy the angle between the lingual sheath and the oesophagus and the buccal ganglia are widely separated but joined by a commissure nearly as thick as the ganglia themselves.[7]

Reproductive system: The hermaphrodite gland (HG) is elongated and large, and is connected with spermoviduct (SO) by means of the hermaphrodite duct (HD) which takes its course through a portion of the albumen gland (AG). The spermoviduct is thick and well convoluted, and separates further down into a vas deferens or sperm-duct (VD) and an oviduct (OV). The former opens into the upper end of a very long penis (P), to which a strong retractor muscle (PRM) is attached. The lower portion of the penis unites with that of the oviduct at the genital orifice, so that there is no vestibule. The receptaculum seminis (RS) opens into the lower end of the penis near the junction of the two ducts.[9]

Internal shell, dorsal view. Scale bar is in mm.

Distribution

Fossil distribution

The internal shells of the different species of Limacidae are not recognizable to the species level. Therefore, the fossil distribution of Limax maximus (and other Limacidae species) is unknown. Unidentified calcitic shells of Limacidae are known from European Tertiary and Quaternary deposits.

Indigenous distribution

This species is now widely distributed around the world, but it is generally considered to be native to Europe and Mediterranean countries of Africa.[3][12]

Western Europe:

Eastern Europe:

Africa:

In a compost heap in New Jersey

Nonindigenous distribution

The non-indigenous distribution of Limax maximus includes many countries worldwide:[12]

Penises of Limax maximus during mating.

1- penises after protrusion from the body. 2 - commencement of the appearance of the frill. 3 - frill partially unrolled. 4 - frill completely expanded, preparatory to twisting together. 5 - penises tightly coiled together, forming the whorled knot. 6 - the succeeding umbrella form. 7 - umbrella form with horizontal margins reversed. 8 - umbrella form with double margins.

Europe:

  • all remaining countries not already listed above.

Africa

North America:

  • Canada (present in 5 of 10 provinces)[15]
  • Mexico
  • United States (present in 46 of 50 states)

South America:

Asia:

Oceania:

Behavior

Limax maximus is nocturnal, feeding at night.[11] It is not very active or prolific.[11] When alarmed, or at rest, this slug merely draws its head within the shield, but does not otherwise contract its body. When irritated, it is said to expand its shield.[11]

The homing instinct is strongly developed in this species, which, after its nocturnal rambles or foraging expeditions, usually returns to the particular crevice or chink in which it has established itself.[7]

Limax maximus is capable of associative learning, specifically classical conditioning, because it is capable of aversion learning and other types of learning.[16][17] It can also detect deficiencies in a nutritionally incomplete diet if the essential amino acid methionine is experimentally removed from its food.[18]

Ecology

Habitat

The slug is almost always found near human habitation — usually in lawns, gardens, cellars or in other damp areas.

This species is not gregarious. It frequents gardens, damp and shady hedgerows and woods, hiding during the day beneath stones, under fallen trees, or other obscure and damp places. It does however exhibit a decided preference for the vicinity of human habitations, and readily takes up its abode in damp cellars or outbuildings.[7]

In Ireland, this predilection for human dwellings is not exhibited, and the species is restricted to woods and other similar places. It may even be met almost within a high-water mark on the seashore.[7]

Feeding habits

Limax maximus is omnivorous. It is a detrivore, cleaning up dead plants and fungi,[7] and a carnivore known to pursue other slugs at a top speed of 15 centimetres (6 in) per minute.[19] It is listed as a major agricultural pest by the Institute of Food and Agricultural Science Florida.[20]

Life cycle

With egg cluster

The eggs of this slug are deposited in a cluster, slightly attached to each other.[11] Eggs are transparent, elastic and slightly yellowish in color.[9] The size of the egg is 6×4.5 mm.[21][22] They hatch in about a month.[7]

The tiny slugs which emerge from the eggs need at least two years to reach sexual maturity.[23]

The lifespan of Limax maximus is 2.5–3 years.[24]

Mating

Mating of Limax maximus filmed

The mating habits of Limax maximus are considered unusual among slugs: the hermaphrodite slugs court, usually for hours, by circling and licking each other. After this, the slugs will climb into a tree or other high area and then, entwined together, lower themselves on a thick string of mucus, evert their white translucent mating organs (penises) from their gonopores (openings on the right side of the head), entwine these organs, and exchange sperm. Both participants will later lay hundreds of eggs.

Parasites

Parasites of Limax maximus include the nematode Agfa flexilis, which lives in its salivary glands,[7][unreliable source?] the nematode Angiostoma limacis, which lives in its rectum,[7][unreliable source?] and Angiostrongylus costaricensis.[25]

Like some other slugs, this species is often infested by the white parasitic slug mite Riccardoella limacum. This mite swarms its body and invades its respiratory cavity.[11]

A meningitis-causing nematode, Angiostrongylus cantonensis, which normally infests the lungs of rats, has a larval stage which can only live in molluscs, including slugs. This nematode was once known to be a problem only in tropical areas, but it has since spread to other regions. Live slugs that are accidentally eaten with improperly cleaned vegetables, such as lettuce, or slugs which have been improperly cooked, can act as vectors for the parasite.[26][27]

  • on a forest floor in France
    on a forest floor in France
  • on a leaf in Germany
    on a leaf in Germany
  • Canberra, Australia
    Canberra, Australia
  • A lighter specimen
    A lighter specimen
  • var. candida
    var. candida
  • Mating
    Mating

References

This article incorporates public domain text from references.[7][8][9][11]

  • Spencer, H.G., Marshall, B.A. & Willan, R.C. (2009). Checklist of New Zealand living Mollusca. pp 196–219 in Gordon, D.P. (ed.) New Zealand inventory of biodiversity. Volume one. Kingdom Animalia: Radiata, Lophotrochozoa, Deuterostomia. Canterbury University Press, Christchurch.

Notes

  1. ^ Rowson, B. (2017). "Limax maximus". IUCN Red List of Threatened Species. 2017: e.T170900A85577040. doi:10.2305/IUCN.UK.2017-3.RLTS.T170900A85577040.en. Retrieved 27 April 2021.
  2. ^ (in Latin) Linnaeus C. 1758. Systema naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Tomus I. Editio decima, reformata. pp. [1-4], 1-824. Holmiae. (Salvius).
  3. ^ a b c (in Polish) Wiktor, A. 1989. Limacoidea et Zonitoidea nuda. Slimaki pomrowioksztaltne (Gastropoda: Stylommatophora). Fauna Poloniae 12, Polska Akademia Nauk, Warszawa, 208 pp., 165-168.
  4. ^ Marshall, B. (2014). Limax maximus Linnaeus, 1758. Accessed through: World Register of Marine Species at http://www.marinespecies.org/aphia.php?p=taxdetails&id=819992 on 2014-11-06
  5. ^ "details". www.tsusinvasives.org. Retrieved 4 November 2022.
  6. ^ (in German) M.P. Kerney, A. D. Cameron, J. H. Jungbluth: Die Landschnecken Nord- und Mitteleuropas. Verlag Paul Parey, Hamburg und Berlin 1983, ISBN 3-490-17918-8, page 183.
  7. ^ a b c d e f g h i j k l m n o p q Taylor, J. W. (7 November) 1902. part 8, pages 1-52. Monograph of the land and freshwater Mollusca of the British Isles. Testacellidae. Limacidae. Arionidae. Taylor Brothers, Leeds. Introduction page XV., pages 34-52.
  8. ^ a b c Tryon G. W. 1885. Manual of Conchology. Second series: Pulmonata Volume 1. Testacellidae, Oleacinidae, Streptaxidae, Helicoidea, Vitrinidae, Limacidae, Arionidae. 364 pp., 60 plates, pages 189-190, plate 46 figure 31-35, 39; plate 49, figure 76.
  9. ^ a b c d e f Scharff R. F. (July) 1891. The slugs of Ireland. The Scientific Transactions of the Royal Dublin Society, volume IV., series II. Dublin, Royal Dublin Society; London, Williams & Norgate. 513-563. Limax maximus on pages page 517-521. plate LVII.
  10. ^ Pini. 1876. Bull. Soc. Mal. Ital. ii., 83. (There is described Limax cornaliae Pini)
  11. ^ a b c d e f g Jeffreys J. G. 1862. British conchology: or, an account of the Mollusca which now inhabit the British Isles and the surrounding seas. Volume I. Land and freshwater shells. page 137-138.
  12. ^ a b Barker, Gary (8 March 2015). "Limax maximus (leopard slug)". CABI Invasive Species Compendium. Centre for Agriculture and Bioscience International. Retrieved 8 October 2016.
  13. ^ Kerney, M. P. & R.A.D. Cameron, 1979, A Field Guide to the Land Snails of Britain and North-west Europe. Collins, Glasgow.
  14. ^ (in Dutch) Limax maximus. Stichting ANEMOON, accessed 10 August 2009
  15. ^ "Unwanted slug with an interesting sex life spotted in Comox Valley". CBC News. Canadian Broadcasting Corporation. 15 September 2015.
  16. ^ Sahley, Christie; Rudy, Jerry W.; Gelperin, Alan (1981). "An analysis of associative learning in a terrestrial mollusc". Journal of Comparative Physiology. 144 (1): 1–8. doi:10.1007/BF00612791. S2CID 33533146.
  17. ^ Sahley CL, Martin KA, Gelperin A (August 1990). "Analysis of associative learning in the terrestrial mollusc Limax maximus. II. Appetitive learning". Journal of Comparative Physiology A. 167 (3): 339–45. doi:10.1007/bf00192569. PMID 2231476. S2CID 1196224.
  18. ^ Delaney K, Gelperin A (September 1986). "Post-ingestive food-aversion learning to amino acid deficient diets by the terrestrial slug Limax maximus". Journal of Comparative Physiology A. 159 (3): 281–95. doi:10.1007/BF00603975. PMID 3772825. S2CID 3117184.
  19. ^ Sandelin, Rob (2007–2011). "Snails and Slugs of the Pacific Lowlands". A Field Guide to the Lowland Northwest. Sky Valley Environments. Archived from the original on 20 July 2011.
  20. ^ Stange, Lionel A.; Deisler, Jane E.; Fasulo, Thomas (June 2009), "Slugs (of Florida) (Gastropoda: Pulmonata) / EENY-087", Featured Creatures, Entomology and Nematology Department, Florida Cooperative Extension Service, Institute of Food and Agricultural Sciences, University of Florida
  21. ^ Heller, J. Life History Strategies. In: Barker, G. M. (ed.): The Biology of Terrestrial Molluscs. CABI Publishing, Oxon, UK. 2001. ISBN 0-85199-318-4. 1-146, cited page: 428.
  22. ^ (in German) Frömming, E. Biologie der Mitteleuropäischen Landgastropoden. Duncker & Humblot, Berlin. 1954.
  23. ^ Fox, Richard (3 July 2006). "Limax maximus: Great Slug, with notes on Arion ater and Ariolimax columbianus". Invertebrate Anatomy OnLine. Lander University.
  24. ^ Limax maximus Archived 2009-08-19 at the Wayback Machine. UF / IFAS Featured Creatures Web site, publication date: June 1999, latest revision: May 2009. accessed 1 August 2009.
  25. ^ Teixeira CG, Thiengo SC, Thome JW, Medeiros AB, Camillo-Coura L, Agostini AA (1993). "On the diversity of mollusc intermediate hosts of Angiostrongylus costaricensis Morera & Cespedes, 1971 in southern Brazil". Memórias do Instituto Oswaldo Cruz. 88 (3): 487–9. doi:10.1590/S0074-02761993000300020. PMID 8107609.
  26. ^ Sanjaya N. Senanayake, Don S. Pryor, John Walker & Pam Konecny 2003. First report of human angiostrongyliasis acquired in Sydney. The Medical Journal of Australia, 179 (8): 430-31.
  27. ^ Salleh, A. (20 October 2003). "Man's brain infected by eating slugs". The Lab: News in Science. Australian Broadcasting Company.

Further reading

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