Terrestrial slug problems: Classical biological control and beyond

CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources

Volumn 7, Issue , 2012, Pages

  Howlett, Sally A ^a  

^a Organic Research Centre at Wakelyns Agroforestry   (United Kingdom)

Author keywords

Biological control; Diptera; Microbe; Mollusca; Nematoda; Pest control

Indexed keywords

DIPTERA; GASTROPODA; MOLLUSCA; NEMATODA; SCIOMYZIDAE;

EID: 84868628792     PISSN: None     EISSN: 17498848     Source Type: Journal    
DOI: 10.1079/PAVSNNR20127051     Document Type: Review

References (102)

1. Barker GM. Gastropods on land: phylogeny, diversity and adaptive morphology. In: Barker GM, editor. The Biology of Terrestrial Molluscs. CABI Publishing, Wallingford, Oxford, UK: 2001. p. 1-145.
2. Theenhaus A, Scheu S. The influence of slug (Arion rufus) mucus and cast material addition on microbial biomass, respiration, and nutrient cycling in beech leaf litter. Biology and Fertility of Soils 1996;23(1):80-5.
3. Barker GM. Gastropods as pests in New Zealand pastoral agriculture, with emphasis on Agriolimacidae, Arionidae and Milacidae. In: Barker GM, editor. Molluscs as Crop Pests. CABI Publishing, Wallingford, Oxford, UK; 2002. p. 361-423.
4. Watts A. Rain brings slug invasion. Farmers Weekly 2012 17th July 2012:64-6.
5. Godan D. Pest Slugs and Snails. Biology and Control. 1st ed. Springer-Verlag, Berlin, Heidelberg, New York; 1983.
6. Barker GM. Naturalised Terrestrial Stylommatophora: (Mollusca:Gastropoda) . Manaaki Press, Lincoln, New Zealand; 1999.
7. Wilson MJ. A novel nematode for management of slugs. In: Vincent C, Goettel MS, Lazarovitsi G, editors. Biological Control: A Global Perspective. CAB International, Oxford, UK; 2007. p. 152-9.
8. Port CM, Port GR. The biology and behaviour of slugs in relation to crop damage and control. Agricultural Zoology Reviews 1986;1:253-99.
9. Glen D. Integrated control of slug damage. Pesticide Outlook 2002;13:137-41. (Pubitemid 35028806)
10. Gould HJ. Observations on the susceptibility of maincrop potato varieties to slug damage. Plant Pathology 1965;14:109-11.
11. Winfield AL, Wardlow LR, Smith BF. Further observations on the susceptibility of maincrop potato cultivars to slug damage. Plant Pathology 1967;16:136-8.
12. Ferguson CM, Lewis GC, Hanks CB, Parsons DMJ, Asteraki EJ. Incidence and severity of damage by slugs and snails to leaves of twelve white clover cultivars. Annals of Applied Biology 1989;10:138-9.
13. Glen DM, Jones H, Fieldsend JK. Damage to oilseed rape seedlings by the field slug Deroceras reticulatum in relation to glucosinolate concentration. Annals of Applied Biology 1990;117(1):197-207.
14. Glen DM, Wilson MJ, Hughes L, Cargeeg P, Hajjjar A. Exploring and exploiting the potential of the rhabditid nematode Phasmarhabditis hermaphrodita as a biocontrol agent for slugs. In: Henderson IF, editor. Slug and Snail Pests in Agriculture. British Crop Protection Council: Canterbury, UK; 1996. p. 271-80.
15. Rose JH. Observations on the larval stages of Muellerius capillaris within the intermediate hosts Agriolimax agrestis and A. reticulatus. Journal of Helminthology 1957;31:1-16.
16. Stephenson JW. Slug parasites and predators: Rothamsted Experimental Station Report; 1964.
17. Brooks A, Crook M. The use of molluscicides in UK agriculture and their effects on non-target organisms. The Malacological Society of London Mini-Review. 2003.
18. Strickland AH. Pest control and productivity in British agriculture. Journal of the Royal Society of Arts 1965;113:62-81.
19. Hunter PJ. An estimate of the extent of slug damage to wheat and potatoes in England and Wales. NAAS Quarterly Review 1969;85:31-6.
20. Sly JMA. Pesticide Usage Survey. Arable farm crops and grass: Ministry of Agriculture, Fisheries and Food; 1986.
21. Garthwaite DG, Thomas MR. The usage of molluscicides in agriculture and horticulture in Great Britain over the last 30 years. In: Henderson IF, editor. Slug and Snail Pests in Agriculture. British Crop Protection Council, Canterbury, UK; 1996. p. 39-46.
22. Redbond M. Slugs and snails: The Royal Society of Chemistry; 2003 Oct 2003.
23. Meredith RH. Slug pellets - risks and benefits in perspective. In: Dussart GBJ, editor. British Crop Protection Conference; 2003; Canterbury, UK; 2003. p. 235-42.
24. Rabitsch W. DAISIE European Invasive Alien Species Gateway, 2006. Arion vulgaris. Available from: www.europealiens.org/speciesFactsheet.do?speciesId= 52937 2006. [Accessed 20 August 2012]
25. Nash MA, Thomson LJ, Hoffmann AA. Slug control in Australian canola: monitoring, molluscicidal baits and economic thresholds. Pest Management Science 2007;63:851-9. (Pubitemid 47344748)
26. Mellanby K. Slugs at low temperatures. Nature 1961;189:944.
27. Schüder I. Integrated control of slug and snail pests in hardy nursery stock [PhD thesis]. Newcastle upon Tyne, Tyne and Wear, UK; 2004.
28. Blank RH, Bell DS. Seasonal patterns of pasture seed loss to black crickets (Teleogryllus commodus) and other invertebrates. New Zealand Journal of Agricultural Research 1982;25:123-30.
29. South A. Terrestrial Slugs. Biology, ecology and control. Chapman and Hall, London, UK; 1992.
30. Anon. Slugs and Snails: Ministry of Agriculture, Fisheries and Food; 1979.
31. Duthoit CMG. Slugs and food preferences. Plant Pathology 1964;13(2):73-8.
32. Barker GM. Notes on the introduced terrestrial pulmonata (Gastropoda: Mollusca) of New Zealand. Journal of Molluscan Studies 1982;48:174-81.
33. Runham NW, Hunter PJ. Terrestrial Slugs. 1st ed. Hutchinson and Co. Ltd., London, UK; 1970.
34. Glen DM, Moens R. Agriolimacidae, Arionidae and Milacidae as pests in West European cereals. In: Barker GM, editor. Molluscs as Crop Pests. CABI Publishing, Wallingford, UK; 2002. p. 468.
35. Garthwaite DG, Barker I, Parrish G, Smith L, Chippindale C, Pietravalle S. Pesticide usage survey report: Food and Environment Research Agency; 2011. Report No.: 235-7.
36. Purvis G. The hazard posed by methiocarb slug pellets to carabid beetles: understanding population effects in the field. In: Slug and Snail Pests in Agriculture. British Crop Protection Council, Canterbury, UK; 1996. p. 189-96.
37. Studdert VP. Epidemiological features of snail and slug bait poisoning in dogs and cats. Australian Veterinary Journal 1985;62:269-71.
38. Longbottom GM, Gordon ASM. Metaldehyde poisoning in a dairy herd. Veterinary Record 1979;104:454-5. (Pubitemid 9186325)
39. Martin TJ, Forrest JD. Development of Draza in Great Britain. Pflanzenshutz-Nachrichten Bayer 1969;22:205-43.
40. Barnett EA, Fletcher MR, Hunter K, Sharp EA. Pesticide Poisoning of Animals 2000: Investigations of suspected incidents in the United Kingdom: Department of the Environment, Food and Rural Affairs; 2002.
41. Shore RF, Feber RE, Firbank LG, Fishwick SK, Macdonald DW, Norum U. The impacts of molluscicide pellets on spring and autumn populations of wood mice Apodemus sylvaticus. Agriculture, Ecosystems and Environment 1997;64(3):211-7. (Pubitemid 27461800)
42. Position Statement: Environment Agency position on metaldehyde. In: UK Environment Agency; 2011. p. 4.
43. Langan AM, Shaw EM. Responses of the earthworm Lumbricus terrestris (L.) to iron phosphate and metaldehyde slug pellet formulations. Applied Soil Ecology 2006;34:184-9. (Pubitemid 44344468)
44. Barker GM, editor. Natural Enemies of Terrestrial Molluscs. CABI Publishing, Oxford; 2004.
45. Barker GM. Overview of the biology of marsh flies (Diptera: Sciomyzidae), with special reference to predators and parasitoids of terrestrial gastropods. In: Barker GM, editor. Natural enemies of Terrestrial Molluscs. Oxford: CABI Publishing; 2004. p. 227-79.
46. Lisansky S. Microbial Biopesticides. In: Evans HF, editor. Microbial Insecticides: Novelty or Necessity? University of Warwick, British Crop Protection Council, Coventry; 1997. p. 3-10.
47. Straus EE, Knight JD. Microbial insecticides: can farmers be persuaded to use them? In: Evans HF, editor. Microbial Insecticides: Novelty or Necessity? University of Warwick, British Crop Protection Council, Coventry; 1997. p. 141-50.
48. Tatchell GM. Microbial insecticides and IPM: current and future opportunities for the use of biopesticides. In: Evans HF, editor. Microbial Insecticides: Novelty or Necessity? University of Warwick, British Crop Protection Council, Coventry; 1997. p. 191-200.
49. Wilson MJ, Glen DM, George SK. The rhabditid nematode Phasmarhabditis hermaphrodita as a potential biological control agent for slugs. Biocontrol Science and Technology 1993;3(4):503-11.
50. Rae R, Verdun C, Grewal PS, Robertson JF, Wilson MJ. Biological control of terrestrial molluscs using Phasmarhabditis hermaphrodita - progress and prospects. Pest Management Science 2007;63:1153-64. (Pubitemid 350144818)
51. Schneider A. Über, eine Nematodenlarvae und gewisse Verscheidenheiten in den Geschlechtsorganen der Nematoden. Zeitschrift fur Wissenschaft Zoologie 1859;10:176-8.
52. Wilson MJ, Glen DM, George SK, Butler RC. Mass cultivation and storage of the rhabditid nematode Phasmarhabditis hermaphrodita, a biocontrol agent for slugs. Biocontrol Science and Technology 1993;3(4):513-21. (Pubitemid 2030398)
53. Tan L, Grewal PS. Characterisation of the first molluscicidal lipopolysaccharide from Moraxella osloensis. Applied and Environmental Microbiology 2003;69(6):3646-9. (Pubitemid 36693377)
54. Tan L, Grewel PS. Pathogenicity of Moraxella osloensis, a bacterium associated with the nematode Phasmarhabditis hermaphrodita to the slug Deroceras reticulatum. Applied and Environmental Microbiology 2001;67(11):5010-6. (Pubitemid 33701263)
55. Tan L, Grewel PS. Endotoxin activity of Moraxella osloensis against the Grey garden slug, Deroceras reticulatum. Applied and Environmental Microbiology 2002;68(8):3943-7. (Pubitemid 34836707)
56. Wilson MJ, Glen DM, Pearce JD, Rodgers PB. Monoxenic culture of the slug parasite Phasmarhabditis hermaphrodita (Nematoda, Rhabditidae) with different bacteria in liquid and solid-phase. Fundamental and Applied Nematology 1995;18(2):159-66.
57. Bailey SER, Cairns A, Latham R, Abdel Kasi M, Manning P. Onset of immobilisation in the slug Deroceras reticulatum Müller parasitsed by the nematode, Phasmarhabditis hermaphrodita Schneider. In: Slugs and Snails: Agricultural, Veterinary and Environmental Perspectives; 2003: British Crop Protection Council (BCPC) Symposium Proceedings 2003. p. 215-20.
58. Glen DM, Wilson MJ, Pearce JD, Rodgers PB. Discovery and investigation of a novel nematode parasite for biological control of slugs. In: Pests and Diseases; 1994: British Crop Protection Council (BCPC) Symposium Proceedings; 1994. p. 617-24.
59. Wilson MJ, Grewel PS. Biology, production and formulation of slug-parasitic nematodes. In: Grewel PS, Ehlers RU, Shapiro-Ilan DI, editors. Nematodes as Biocontrol Agents. CABI Publishing, Oxford; 2005. p. 431-45.
60. De Nardo EAB, Sindermann AB, Grewal SK, Grewal PS. Non-susceptibility of earthworm, Eisenia fetida to the rhabditid nematode, Phasmarhabditis hermaphrodita, a biocontrol agent of slugs. Biocontrol, Science and Technology 2004;14(1):93-8. (Pubitemid 38178614)
61. Rae R, Robertson JF, Wilson MJ. Susceptibility of indigenous UK earthworms and an invasive pest flatworm to the slug parastic nematode Phasmarhabditis hermaphrodita. Biocontrol, Science and Technology 2005;15(6):623-6. (Pubitemid 41009332)
62. Morand S, Wilson MJ, Glen DM. Nematodes (nematoda) parasitic in terrestrial gastropods. In: Barker GM, editor. Natural Enemies of Terrestrial Molluscs. CABI Publishing, Oxford; 2004. p. 525-57.
63. Jaworska M. Laboratory infection of slugs (Gastropoda: Pulmonata) with entomopathogenic nematodes (Rhabditida: Nematoda). Journal of Invertebrate Pathology 1993;61(2):223-4.
64. Wilson MJ, Glen DM, Hughes LA, Pearce JD, Rodgers PB. Laboratory tests of the potential of entomopathogenic nematodes for the control of field slugs (Deroceras reticulatum). Journal of Invertebrate Pathology 1994;64:182-7. (Pubitemid 124013995)
65. Ester A, Rozen Kv, Molendijk LPG. Field experiments using the rhabditid nematode Phasmarhabditis hermpahrodita or salt as control measures against slugs in green asparagus. Crop Protection 2003;22:689-69.
66. Ester A, Rozen Kv, Molendijk LPG, M.E.T.V. The rhabditid nematode Phasmarhabditis hermaphrodita Schneider as a potential biocontrol agent to control field slugs Deroceras reticulatum (Müller) in Brussels sprouts. In: Slugs and Snails: Agricultural, Veterinary and Environmental Perspectives; 2003; Canterbury: British Crop Protection Council (BCPC) Symposium Proceedings 2003. p. 313-8.
67. Speiser B, Andermatt M. Field trials with Phasmarhabditis hermaphrodita in Switzerland. In: Henderson IF, editor. Slug and Snail Pests in Agriculture. British Crop Protection Council, Canterbury, UK; 1996. p. 419-24.
68. Wilson MJ, Glen DM, George SK, Pearce JD, Wiltshire CW. Biological control of slugs in winter wheat using the rhabditid nematode Phasmarhabditis hermaphrodita. Annals of Applied Biology 1994;125(2):377-90. (Pubitemid 26449528)
69. Rae RG, Robertson JF, Wilson MJ. Susceptibility and immune response of Deroceras reticulatum, Milax gagates and Limax pseudoflavus exposed to the slug parasitic nematode Phasmarhabditis hermaphrodita. Journal of Invertebrate Pathology 2008;97:61-9. (Pubitemid 350235482)
70. Wilson MJ, Burch G, Tourna M, Aalders LT, Barker GM. The potential of a New Zealand strain of Phasmarhabditis hermaphrodita for biological control of slugs. New Zealand Plant Protection 2012;65:161-5.
71. Berg CO. Sciomyzid larvae that feed on snails. Journal of Parasitology 1953;39(6):630-6.
72. Reidenbach JM, Vala JC, Ghamizi M. The slug-killing Sciomyzidae (Diptera): potential agents in the biological control of crop pest molluscs. In: Henderson IF, editor. Slugs and Snails in World Agriculture. British Crop Protection Council, Guildford, UK; 1989. p. 273-80.
73. Murphy WJ, Knutson LV, Chapman EG, McDonnell RJ, Williams CD, Foote BA, et al. Key aspects of the biology of snail-killing Sciomyzidae flies. Annual Review of Entomology 2012;57:425-47.
74. Trelka DG. The behaviour and predatory larvae of Tetancera plebeia (Diptera: Sciomyzidae) and toxicological and neurological aspects of a toxic salivary secretion used to immobilise slugs [PhD thesis]. Cornell University, Ithaca, New York; 1973.
75. Richards EH, DeMarzo D, Port GR, Dani MP, Walters KA. Effects of the nematode Phasmarhabditis hermaphrodita and of venom from the endoparasitic wasp Pimpla hypochondriaca on survival and food consumption of the pest slug Deroceras reticulatum; implications for novel biocontrol strategies. Pest Management Science 2008;64:711-9.
76. Appleton CC, Miller RM, Maharaj R. Control of schistosomiasis host snails in South Africa - the case for biocontrol by predator augmentation using sciomyzid flies. Journal of Medical and Applied Malacology 1993;5:107-16.
77. Davies CJ. Recent introductions for biological control in Hawaii. In: Proc. Hawaiian Entomological Society; 1972. p. 187-90.
78. Tigari S. Theoretical and experimental evidences of biological control of aquatic snails by snail-killing flies in relation to schistosomiasis (Diptera, Sciomyzidae) (Sepedon sphegea). In: First Mediterranean Conf. on Parasitology; Izmir, Turkey; 1977. p. 103-4.
79. Knutson LV, Orth RE. The Sepedon sphegea complex in the Palearctic and Oriental regions: identity, variation and distribution (Diptera: Sciomyzidae). Annals of the Entomological Society of America 1984;77:687-701.
80. Knutson LV, Stephenson JW, Berg CO. Biology of a slugkilling fly, Tetanocera elata (Diptera: Sciomyzidae). Proc. Malacological Society of London 1965;36:213-20.
81. Trelka DG, Foote BA. Biology of the slug-killing Tetanocera (Diptera:Sciomyzidae). Annals of the Entomological Society of America 1970;63:877-95.
82. Vala JC, Knutson LV. Stades immatures et biologie de Limnia unguicorus (Scopoli), Diptère Sciomyzidae pré dateur de mollusques. Annales de la Socié té Entomologique de France 1990;26:443-50.
83. Ayre K, Port GR. Carabid beetles recorded feeding on slugs in arable fields using ELISA. In: Henderson IF, editor. Slug and Snail Pests in Agriculture. British Crop Protection Council, Canterbury, UK; 1996. p. 411-8.
84. Cornic JF. Studies on the feeding habits of three species of carabid beetles and their variations in an apple orchard. Annales de la Societé Entomologique de France 1973;9(1):69-87.
85. Mair J, Port GR. Predation by the carabid beetles Pterostichus madidus and Nebria brevicollis is affected by size and condition of the prey slug Deroceras reticulatum. Agricultural and Forest Entomology 2001;3:99-106. (Pubitemid 32526301)
86. Powell A. Tradeoffs between predation and scavenging in generalist predators [PhD thesis]. Cardiff University, Cardiff; 2011.
87. Symondson WOC. Biological control of slugs by carabids. In: Henderson IF, editor. Slugs and Snails in World Agriculture. British Crop Protection Council, Guildford, UK; 1989. p. 295-300.
88. Port GR, Glen DM, Symondson WOC. Success in Biological Control of Terrestrial Molluscs. In: Gurr G, Wratten SD, editors. Biological Control: Measures of Success: Kluwer Academic Publishers; Dordrecht 2000. p. 133-59.
89. Lacey L, Frutos R, Kaya H, Vail P. Insect pathogens as biological control agents: do they have a future? Biological Control 2001;21:230-48. (Pubitemid 32632730)
90. Howlett SA, Sarathchadra U, Burch G, Young SD, Bell NL, Jackson TA. Prospects for microbial slug control. In: Zydenbos SM, Jackson TA, editors. Microbial Products: Exploiting Microbial Diversity for Sustainable Plant Production. The New Zealand Plant Protection Society, Dunedin, New Zealand; 2010. p. 33-7.
91. Dean WW, Mead AR, Northey WT. Aeromonas liquefaciens in the giant African snail, Achatina fulica. Journal of Invertebrate Pathology 1970;16:346-51.
92. de Gravelle LG. An investigation of a blistering condition in the slug, Veronicella ameghini [MSc]. Louisiana State University, New Orleans; 1971.
93. Dundee DS. Observations on the Veronicellid slugs of the Southern United States. Nautilus 1977;91(3):108-14.
94. Raut SK, Mandal RN. Disease in the pestiferous slug Laevicaulis alte (Gastropoda: Veronicillidae). Malacological Review 1986;19:106.
95. Runham NW. Snail farming in the United Kingdom. In: Henderson IF, editor. Slugs and Snails in World Agriculture British Crop Protection Council, Guildford, UK; 1989. p. 49-55.
96. Kienlen J, Gertz C, Briard P, Hommay G, Chaufaux J. Recherche de la toxicité de diverses souches de Bacillus thuringiensis Berliner vis-à-vis de trois espèces de limaces. Agronomie 1996;16:347-53.
97. Tervet IW, Esslemont JM. A fungus parasite of the eggs of the gray field slug. Journal of the Quekett Microscopical Club 1938;1:1-3.
98. Arias RO, Crowell HH. A contribution to the biology of the grey garden slug. Bulletin of the Southern California Academy of Sciences 1963;62:83-97.
99. South A. A comparison of the life cycles of the slugs Deroceras reticulatum (Müller) and Arion intermedius Normand on permanent pasture. Journal of Molluscan Studies 1989;55:9-22.
100. Nicholas J. The biology of reproduction in two British pulmonate slugs [PhD thesis]: University of Wales; 1984.
101. Howlett SA, Burch G, Sarathchadra U, Bell NL. A bioassay technique to assess the molluscicidal effects of microbes. New Zealand Plant Protection 2009;62:7-11.
102. Wilson MJ, Burch G. An improved bioassay for screening bacteria for biocontrol activity against slugs that avoids volatile-induced slug mortality. Biocontrol, Science and Technology 2012;22:1235-37.