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Ocular tentacle malformation in Deroceras reticulatum (Mollusca: Gastropoda: Agriolimacidae)

Abstract

Malformations in animals have long been known. In gastropod, natural and induced malformations are mentioned in different systems and in ocular tentacles, mainly linked to cases of parasitism and exposure to pollutants (molluscicides and chemicals). In this study we present a new malformation not documented in the ocular tentacles of slug Deroceras reticulatum that could be due to the action of pesticides. This malformation in D. reticulatum is the first malformation to be mentioned for South America in nursery gardens.

Key-Words
Anomalies; Nursery gardens; Pesticides; Slugs

INTRODUCTION

Malformations in animals have been cited in several cases, particularly in gastropod molluscs, mainly linked to cases of parasitism and exposure to pollutants (molluscicides and chemicals). These malformations can affect their reproductive system, mantle, foot or ocular tentacles (Simroth, 1905Simroth, H. 1905. Über zwei seltene Missbildungen an Nacktschencken. Zeitschrift für wissenschaftliche Zoologie, 82: 494-522.; Boettger, 1956Boettger, C. 1956. Über einen Fall von pathologischer Gestaltveränderung bei einer Wegschnecke der Art Arion ater (L.). Biologisches Zentralblatt, 75: 257-267.; Wiktorowa, 1962Wiktorowa, J. 1962. An interesting anomaly in Limax cinereoniger Wolf (Limacidae, Pulmonata). Zoologica Poloniae, 12: 101-106.; Jackiewicz et al., 1998Jackiewicz, M.; Koralewska-Batura, E. & Lesicki, A. 1998. Anomalies of soft body parts in Acicula polita (Hartmann, 1840), Deroceras laeve (O.F. Müller, 1774) and Deroceras reticulatum (O.F. Müller, 1774) (Mollusca, Gastropoda. Biological Bulletin of Poznan, 35: 39-42.; Barroso et al., 2000Barroso, C.; Moreira, M. & Gibbs, P. 2000. Comparison of imposex and intersex development in four prosobranch species for TBT Monitoring of a Southern European Estuarine System. (Ria de Aveiro, NW Portugal). Marine Ecology Progress Series, 201: 221-232.; Lahbib et al., 2008Lahbib, Y.; Abidli, S. & El Menif, N.T. 2008. Imposex level and penis malformation in Hexaplex trunculus from the Tunisian coast. American Malacological Bulletin, 24: 79-89.; Sawasdee & Kohler, 2009Sawasdee, B. & Köhler, H. 2009. Embryo toxicity of pesticides and heavy metals to the ramshorn snail, Marisa cornuarietis (Prosobranchia). Chemosphere, 75: 1539-1547.; El Ayari et al., 2018El Ayari, T.; Mleiki, A. & El Menif, N.T. 2018. Ocular tentacle regeneration and associated malformations in Stramonita haemastoma (Gastropoda: Muricidae). Hidrobiologia, 806: 215-226.). The abnormal variations developed in the tentacles of gastropods are remarkable, and occur under both natural and experimental conditions. Among the natural anomalies observed are: a simple tentacle with a central cephalic position (Wächtler, 1929Wächtler, W. 1929. Eine merkwürdige Missbildung der Augenträger und der Radula einer Landlungenschnecke. Zoologischer Anzeiger, 83: 169-177.; Chetail, 1958Chetail, M. 1958. Synophtalmie spontanée chez Arion rufus L. et Agriolimax agrestis L. Bulletin de la Société Zoologique de France, 83: 246.; Jackiewicz, 1969Jackiewicz, M. 1969. Interesujący przypadek anormalnooeci czuka u Physa acuta Drap. (Mollusca, Basommatophora). Fragmenta Faunistica, 15: 199-206.), two tentacles arising from the same base (Techow, 1910Techow, G. 1910. Missbildungen bei der Fühlerregeneration von Süsswasserschnecken. Zoologischer Anzeiger, 35: 321-324.; Hofmann, 1912Hofmann, E. 1912. Beiträge zur Teratologie der Schnecken. Zoologischer Anzeiger, 39: 249-259.), partially fused tentacles located in the center of the head (Römer, 1903Römer, J. 1903. Merkwürdige Fühlerbildung an einer Weinbergschnecke. Natur u Haus, 11: 253.) or bifurcated tentacles (Jackiewicz, 1969Jackiewicz, M. 1969. Interesujący przypadek anormalnooeci czuka u Physa acuta Drap. (Mollusca, Basommatophora). Fragmenta Faunistica, 15: 199-206.; Jackiewicz et al., 1998Jackiewicz, M.; Koralewska-Batura, E. & Lesicki, A. 1998. Anomalies of soft body parts in Acicula polita (Hartmann, 1840), Deroceras laeve (O.F. Müller, 1774) and Deroceras reticulatum (O.F. Müller, 1774) (Mollusca, Gastropoda. Biological Bulletin of Poznan, 35: 39-42.). Other anomalies present in tentacles have been induced experimentally by the amputation of the tentacle (Techow, 1910Techow, G. 1910. Missbildungen bei der Fühlerregeneration von Süsswasserschnecken. Zoologischer Anzeiger, 35: 321-324.; Hofmann 1912Hofmann, E. 1912. Beiträge zur Teratologie der Schnecken. Zoologischer Anzeiger, 39: 249-259.). Among the species where tentacular malformations and their subsequent regeneration had been observed, the following can be mentioned: marine gastropods: Stramonita haemastoma (Linnaeus, 1767), Strombus pugilis Linnaeus, 1758, Conomurex luhuanus (Linnaeus, 1758); freshwater gastropods: Planorbarius corneus (Linnaeus, 1758), Lymnaea stagnalis (Linnaeus, 1758); and terrestrial gastropods: Arion subfuscus (Draparnaud, 1805), Deroceras laeve (Müller, 1774), Helix pomatia Linnaeus, 1758, Cornu aspersum (Müller, 1774), and Cepaea hortensis (Müller, 1774).

Despite of the existence of several anomalies all over the globe, in South America, more precisely in Argentina, references about the presence of malformations in terrestrial molluscs are scarce, associating them to studies on molluscicides (Clemente et al., 2008Clemente, N.L.; López, A.N.; Monterubbianesi, M.G.; Cazzaniga, N.J. & Manetti, P.L. 2008. Biological studies and phenology of the slug Deroceras reticulatum (Müller, 1774) (Pulmonata: Stylommatophora). Invertebrate Reproduction & Development, 52: 23-30.), in which under laboratory conditions the lethality and the impossibility of reproducing are proved as consequences of these agents.

In the framework of identifying pathways of dispersion of invasive slugs in commercial nursery gardens in Buenos Aires province (Argentina), we present the first report of ocular tentacle malformation for Deroceras reticulatum (Müller, 1774).

MATERIAL AND METHODS

Sampling was carried out during the month of November 2016 in four commercial nursery gardens located in the district of San Pedro (33°41’29”S, 59°40’36”W), Buenos Aires province, Argentina. The molluscs were obtained by manual collection, in natural areas, in plantations and “pots”. The molluscs collected were photographed while living in their environment and then relaxed in menthol solution for one day, to be later preserved in alcohol, and deposited in the Malacological Collection at the La Plata Museum of the La Plata National University, Buenos Aires Province, Argentina (MLP-Ma). Determination of the specimens was based on Barker (1999Barker, G.M. 1999. Naturalised terrestrial Stylommatophora (Mollusca: Gastropoda). Lincoln, N. Z. Manaaki Whenua Press. 257p. (Fauna of New Zealand № 38).).

RESULTS AND DISCUSSION

The sampling resulted in 77 molluscs collected, 35 are native slugs of the family Veronicellidae and 42 are exotic slugs of the family Agriolimacidae. Between the exotic slugs, 41 belong to Deroceras laeve and 1 to Deroceras reticulatum (MLP-Ma 14550). The origin of Deroceras reticulatum is believed to be Europe (Wiktor, 1996Wiktor, A. 1996. The slugs of the former Yugoslavia (Gastropoda terrestrial nuda - Arionidae, Milacidae, Limacidae, Limacidae, Agriolimacidae. Annales Zoologici, Varsóvia, 46: 1-110.) and currently has a worldwide distribution and is a pest for some plant species as well as vector of various harmful parasitic organisms for both humans and other animals (Berg, 1997Berg, G.H. 1997. Caracoles y babosas de importancia cuarentenaria agrícola y médica para América Latina y el Caribe. San Salvador (El Salvador), OIRSA. 133p.).

This specimen of D. reticulatum (total length 24 mm, Fig. 1) has a malformation, in which the ocular tentacles are fused along their entire length, giving the appearance of presenting a single ocular tentacle. The fusion takes place only between the body walls, whereas the two ocular nerve cords run separately, within the same tentacular structure, so that ocular sensors are situated side by side (Fig. 1).

Figure 1
Deroceras reticulatum in life. Right side view (A); dorsal view (B); detail of the ocular tentacles (C-D); left side view (E). Scale bar: 2 mm.

The malformation observed in D. reticulatum of San Pedro is not the most common type, since amputations, bifurcations or partial fusions of the tentacles are usually detected as mentioned above (Römer, 1903Römer, J. 1903. Merkwürdige Fühlerbildung an einer Weinbergschnecke. Natur u Haus, 11: 253.; Wächtler, 1929Wächtler, W. 1929. Eine merkwürdige Missbildung der Augenträger und der Radula einer Landlungenschnecke. Zoologischer Anzeiger, 83: 169-177.; Chetail, 1958Chetail, M. 1958. Synophtalmie spontanée chez Arion rufus L. et Agriolimax agrestis L. Bulletin de la Société Zoologique de France, 83: 246.; Jackiewicz, 1969Jackiewicz, M. 1969. Interesujący przypadek anormalnooeci czuka u Physa acuta Drap. (Mollusca, Basommatophora). Fragmenta Faunistica, 15: 199-206.; El Ayari et al., 2018El Ayari, T.; Mleiki, A. & El Menif, N.T. 2018. Ocular tentacle regeneration and associated malformations in Stramonita haemastoma (Gastropoda: Muricidae). Hidrobiologia, 806: 215-226.). Although only one individual with this malformation was registered, it is important to document their registration, which is the first to be mentioned in South America. This specimen was found inside a commercial nursery, this being the first record of malformation in this type of anthropogenic environment. Which could indicate that its malformation was related to pesticides used to keep crops and ornamental plants free of pests. We will continue to sample these sites to evaluate if more specimens with malformations are found.

ACKNOWLEDGMENTS

This study was financially supported by project N727 of the Facultad de Ciencias Naturales y Museo (UNLP). We thank specially to proprietaries of commercial nursery gardens by facilitate access to them.

REFERENCES

  • Barker, G.M. 1999. Naturalised terrestrial Stylommatophora (Mollusca: Gastropoda). Lincoln, N. Z. Manaaki Whenua Press. 257p. (Fauna of New Zealand № 38).
  • Barroso, C.; Moreira, M. & Gibbs, P. 2000. Comparison of imposex and intersex development in four prosobranch species for TBT Monitoring of a Southern European Estuarine System. (Ria de Aveiro, NW Portugal). Marine Ecology Progress Series, 201: 221-232.
  • Berg, G.H. 1997. Caracoles y babosas de importancia cuarentenaria agrícola y médica para América Latina y el Caribe. San Salvador (El Salvador), OIRSA. 133p.
  • Boettger, C. 1956. Über einen Fall von pathologischer Gestaltveränderung bei einer Wegschnecke der Art Arion ater (L.). Biologisches Zentralblatt, 75: 257-267.
  • Chetail, M. 1958. Synophtalmie spontanée chez Arion rufus L. et Agriolimax agrestis L. Bulletin de la Société Zoologique de France, 83: 246.
  • Clemente, N.L.; López, A.N.; Monterubbianesi, M.G.; Cazzaniga, N.J. & Manetti, P.L. 2008. Biological studies and phenology of the slug Deroceras reticulatum (Müller, 1774) (Pulmonata: Stylommatophora). Invertebrate Reproduction & Development, 52: 23-30.
  • El Ayari, T.; Mleiki, A. & El Menif, N.T. 2018. Ocular tentacle regeneration and associated malformations in Stramonita haemastoma (Gastropoda: Muricidae). Hidrobiologia, 806: 215-226.
  • Hofmann, E. 1912. Beiträge zur Teratologie der Schnecken. Zoologischer Anzeiger, 39: 249-259.
  • Jackiewicz, M. 1969. Interesujący przypadek anormalnooeci czuka u Physa acuta Drap. (Mollusca, Basommatophora). Fragmenta Faunistica, 15: 199-206.
  • Jackiewicz, M.; Koralewska-Batura, E. & Lesicki, A. 1998. Anomalies of soft body parts in Acicula polita (Hartmann, 1840), Deroceras laeve (O.F. Müller, 1774) and Deroceras reticulatum (O.F. Müller, 1774) (Mollusca, Gastropoda. Biological Bulletin of Poznan, 35: 39-42.
  • Lahbib, Y.; Abidli, S. & El Menif, N.T. 2008. Imposex level and penis malformation in Hexaplex trunculus from the Tunisian coast. American Malacological Bulletin, 24: 79-89.
  • Römer, J. 1903. Merkwürdige Fühlerbildung an einer Weinbergschnecke. Natur u Haus, 11: 253.
  • Sawasdee, B. & Köhler, H. 2009. Embryo toxicity of pesticides and heavy metals to the ramshorn snail, Marisa cornuarietis (Prosobranchia). Chemosphere, 75: 1539-1547.
  • Simroth, H. 1905. Über zwei seltene Missbildungen an Nacktschencken. Zeitschrift für wissenschaftliche Zoologie, 82: 494-522.
  • Techow, G. 1910. Missbildungen bei der Fühlerregeneration von Süsswasserschnecken. Zoologischer Anzeiger, 35: 321-324.
  • Wächtler, W. 1929. Eine merkwürdige Missbildung der Augenträger und der Radula einer Landlungenschnecke. Zoologischer Anzeiger, 83: 169-177.
  • Wiktor, A. 1996. The slugs of the former Yugoslavia (Gastropoda terrestrial nuda - Arionidae, Milacidae, Limacidae, Limacidae, Agriolimacidae. Annales Zoologici, Varsóvia, 46: 1-110.
  • Wiktorowa, J. 1962. An interesting anomaly in Limax cinereoniger Wolf (Limacidae, Pulmonata). Zoologica Poloniae, 12: 101-106.
  • Edited by: Luiz Ricardo Lopes de Simone
  • Published with the financial support of the Committee of "Programa de Apoio às Publicações Científicas Periódicas da USP" (SIBi-USP)

Publication Dates

  • Publication in this collection
    03 Oct 2019
  • Date of issue
    2019

History

  • Received
    06 Aug 2018
  • Accepted
    02 July 2019
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