Tracking predator density dependence and subterranean predation by carabid larvae on slugs using monoclonal antibodies

Ecological Entomology

Volumn 34, Issue 5, 2009, Pages 569-579

  Thomas, R S ^a   Harwood, J D ^a,b   Glen, D M ^a,c,d   Symondson, W O C ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF KENTUCKY   (United States)

^c Styloma Research and Consulting   (United Kingdom)

^d UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Arion intermedius; Density dependence; Deroceras reticulatum; Intra specific competition; Molecular diagnostics; Molluscs; Pterostichus melanarius; Soil predators

Indexed keywords

ANTIBODY; BEETLE; BIOCONTROL AGENT; BIOLOGICAL CONTROL; CROP PEST; DENSITY DEPENDENCE; DIET; FOOD PREFERENCE; GASTROPOD; GROWTH RATE; INTRASPECIFIC COMPETITION; POPULATION REGULATION; PREDATION; PREDATOR-PREY INTERACTION; SUBTERRANEAN ENVIRONMENT;

ARION INTERMEDIUS; CARABIDAE; COLEOPTERA; DEROCERAS RETICULATUM; GASTROPODA; MOLLUSCA; PTEROSTICHUS MELANARIUS; TRITICUM AESTIVUM;

EID: 70349148164     PISSN: 03076946     EISSN: 13652311     Source Type: Journal    
DOI: 10.1111/j.1365-2311.2009.01104.x     Document Type: Article

References (64)

1. Barker, G.M 2002) Molluscs as Crop Pests. CABI Publishing, Wallingford, U.K.
2. Barton-Browne, L 1995) Ontogenic changes in feeding behavior. Regulatory Mechanisms in Insect Feeding (ed. by R. F. Chapman and G. deBoer pp. 307 342. Chapman and Hall, New York.
3. Bett, J.A 1960) The breeding seasons of slugs in gardens. Proceedings of the Zoological Society of London, 135, 559 568.
4. Bohan, D.A., Bohan, A.C., Glen, D.M., Symondson, W.O.C., Wiltshire, C.W. Hughes, L 2000a) Spatial dynamics of predation by carabid beetles on slugs. Journal of Animal Ecology, 69, 367 369.
5. Bohan, D.A., Glen, D.M., Wiltshire, C.W. Hughes, L 2000b) Parametric intensity and the spatial arrangement of the terrestrial mollusc herbivores Deroceras reticulatum and Arion intermedius. Journal of Animal Ecology, 69, 1031 1046.
6. Buckland, S.M. Grime, J.P 2000) The effects of trophic structure, soil fertility on the assembly of plant communities. Oikos, 91, 336 352.
7. Currie, C.R., Spence, J.R. Niemela, J 1996) Competition, cannibalism and intraguild predation among ground beetles (Coleoptera: Carabidae): a laboratory study. Coleopterists Bulletin, 50, 135 148.
8. Desender, K., van den Broek, D. Maelfait, J.P 1985) Population biology and reproduction in Pterostichus melanarius Ill. (Coleoptera, Carabidae) from a heavily grazed pasture ecosystem. Mededelingen Faculteit Landbouwwetenschappen, Rijksuniversiteit, Gent, 50, 567 575.
9. Foltan, P., Sheppard, S.K., Konvicka, M. Symondson, W.O.C 2005) The significance of facultative scavenging in generalist predator nutrition: detecting decayed prey in the guts of predators using PCR. Molecular Ecology, 14, 4147 4158.
10. Glen, D.M., Milsom, N.F. Wiltshire, C.W 1989) Effects of seed-bed conditions on slug numbers and damage to winter-wheat in a clay soil. Annals of Applied Biology, 115, 177 190.
11. Glen, D.M. Wiltshire, C.W 1986) Estimating slug populations from bait-trap catches. Proceedings of the 1986 British Crop Protection Conference - Pests and Diseases 3, pp. 1151 1158, Thornton Heath, U.K.
12. Glen, D.M., Wiltshire, C.W. Milsom, N.F 1984) Slugs and straw disposal in winter wheat. Proceedings of the 1984 British Crop Protection Conference - Pests and Diseases 1, pp. 139 144, Thornton Heath, U.K.
13. Glen, D.M., Wiltshire, C.W., Walker, A.J., Wilson, M.J. Shewry, P.R 1996) Slug problems and control strategies in relation to crop rotations. Aspects of Applied Biology, 47, 153 160.
14. Godan, D 1983) Pest Slugs and Snails, Biology and Control. Springer-Verlag, Berlin, Germany.
15. Greene, A 1975) Biology of the five species of Cychrini (Coleoptera: Carabidae) in the steppe region of southeastern Washington. Melanderia, 19, 1 43.
16. Harper, G.L., King, R.A., Dodd, C.S., Harwood, J.D., Glen, D.M., Bruford M.W. et al 2005) Rapid screening of invertebrate predators for multiple prey DNA targets. Molecular Ecology, 14, 819 827.
17. Holland, J.M 2002) The Agroecology of Carabid Beetles. Intercept, Andover, U.K.
18. Holt, R.D. Lawton, J.H 1994) The ecological consequences of shared natural enemies. Annual Review of Ecology and Systematics, 25, 495 520.
19. Hunter, P.J. Symonds, B.V 1971) The leap-frogging slug. Nature, 229, 349.
20. Hurka, K 1975) Laboratory studies on the life cycle of Pterostichus melanarius (Illig.) (Coleoptera: Carabidae). Vestnik Ceskoslovenska Spolecnosti Zoologicka, 39, 265 274.
21. Juen, A. Traugott, M 2007) Revealing species-specific trophic links in soil food webs: molecular identification of scarab predators. Molecular Ecology, 16, 1545 1557.
22. King, R.A., Read, D.S., Traugott, M. Symondson, W.O.C 2008) Molecular analysis of predation: a review of best practice for DNA-based approaches. Molecular Ecology, 17, 947 963.
23. Liddell, J.E. Cryer, A 1991) A Practical Guide to Monoclonal Antibodies. John Wiley and Sons, Chichester, U.K.
24. Luff, M.L 1974) Adult and larval feeding habits of Pterostichus madidus (F.) (Coleoptera: Carabidae). Journal of Natural History, 8, 403 409.
25. Manga, N 1972) Population metabolism of Nebria brevicollis (F.). Oecologia, 10, 223 242.
26. McKemey, A.R 2000) Integrating behavioural aspects of carabid-slug interactions with immunological data on predator ecology. PhD thesis, Cardiff University, Cardiff, U.K.
27. McKemey, A.R., Glen, D.M., Wiltshire, C.W. Symondson, W.O.C 2006) Molecular quantification of slug density in the soil using monoclonal antibodies. Soil Biology & Biochemistry, 38, 2903 2909.
28. McKemey, A., Symondson, W.O.C. Glen, D.M 2003) Predation and prey size choice by the carabid beetle Pterostichus melanarius (Coleoptera: Carabidae): the dangers of extrapolating from laboratory to field. Bulletin of Entomological Research, 93, 227 234.
29. Murdoch, W.W., Cheeson, J. Cheeson, P.L 1985) Biological control in theory and practice. American Naturalist, 125, 344 366.
30. Niemala, J., Spence, J.R. Carcamo, H 1997) Establishment and interactions of carabid populations: an experiment with native and introduced species. Ecography, 20, 643 652.
31. Paill, W 2000) Slugs as prey for larvae and imagines of Carabus violaceus (Coleoptera: Carabidae). Natural History and Applied Ecology of Carabid Beetles, Proceedings of the IX European Carabidologists Meeting (ed. by P. Brandmayr, G. Lövei, T. Z. Brandmayr, A. Casale and A. Vigna Taglainti pp. 304. Pensoft, Sofia, Bulgaria.
32. Paill, W 2004) Slug feeding in the carabid beetle Pterostichus melanarius: seasonality and dependence on prey size. Journal of Molluscan Studies, 70, 203 205.
33. Pakarinen, E 1994a) Autotomy in arionid and limacid slugs. Journal of Molluscan Studies, 60, 19 23.
34. Pakarinen, E 1994b) The importance of mucus as a defense against carabid beetles by the slugs Arion fasciatus and Deroceras reticulatum. Journal of Molluscan Studies, 60, 149 155.
35. Pollet, M. Desender, K 1985) Adult and larval feeding ecology in Pterostichus melanarius Ill. (Coleoptera, Carabidae). Mededelingen Faculteit Landbouwwetenschappen, Rijksuniversiteit, Gent, 50, 581 594.
36. Port, C.M. Port, G.R 1986) The biology and behaviour of slugs in relation to crop damage and control. Agricultural Zoology Reviews, 1, 255 299.
37. Read, D.S., Sheppard, S.K., Bruford, M.W., Glen, D.M. Symondson, W.O.C 2006) Molecular detection of predation by soil microarthropods on nematodes. Molecular Ecology, 15, 1963 1972.
38. Rollo, C.D 1982) The regulation of activity in populations of the terrestrial slug Limax maximus (Gastropoda, Limacidae). Researches on Population Ecology, 24, 1 32.
39. Rollo, C.D. Wellington, W.G 1979) Intra- and inter-specific agonistic behaviour among terrestrial slugs (Pulmonata: Stylommatophora). Canadian Journal of Zoology, 57, 846 855.
40. Scheifler, R., Gomot-de Vaufleury, A., Toussaint, M.L. Badot, P.M 2002) Transfer and effects of cadmium in an experimental food chain involving the snail Helix aspersa and the predatory carabid beetle Chrysocarabus splendens. Chemosphere, 48, 571 579.
41. Smith, J.W., Wiedenmann, R.N. Gilstrap, F.E 1997) Challenges and opportunities for biological control in ephemeral crop habitats: an overview. Biological Control, 10, 2 3.
42. South, A 1964) Estimation of slug populations. Annals of Applied Biology, 53, 251 258.
43. South, A 1989) A comparison of the life-cycles of the slugs Deroceras reticulatum (Muller) and Arion intermedius Normand on permanent pasture. Journal of Molluscan Studies, 55, 9 22.
44. South, A 1992) Terrestrial Slugs. Biology, Ecology and Control. Chapman and Hall, London, U.K.
45. Spence, J.R. Sutcliffe, J.F 1982) Structure and function of feeding in larvae of Nebria (Coleoptera, Carabidae). Canadian Journal of Zoology-Revue Canadienne de Zoologie, 60, 2382 2394.
46. Sunderland, K.D., Axelsen, J.A., Dromph, K., Freier, B., Hemptinne, J.L., Holst, N.H. et al 1997) Pest control by a community of natural enemies. Arthropod Natural Enemies in Arable Land. III. The Individual, the Population and the Community (ed. by W. Powell Acta Jutlandica, 72, 271 326. Aarhus University Press, Aarhus, Denmark.
47. Sunderland, K.D., Powell, W. Symondson, W.O.C 2005) Populations and communities. Insects as Natural Enemies: A Practical Perspective (ed. by M. A. Jervis pp. 299 434. Springer, Berlin, Germany.
48. Symondson, W.O.C 1993) Chemical confinement of slugs: an alternative to electric fences. Journal of Molluscan Studies, 59, 259 261.
49. Symondson, W.O.C 2002) Molecular identification of prey in predator diets. Molecular Ecology, 11, 627 641.
50. Symondson, W.O.C 2004) Coleoptera (Carabidae, Drilidae, Lampyridae and Staphylinidae) as predators of terrestrial gastropods. Natural Enemies of Terrestrial Molluscs (ed. by G. M. Barker pp. 37 84. CAB International, Oxford, U.K.
51. Symondson, W.O.C., Cesarini, S., Dodd, P.W., Harper, G.L., Bruford, M.W., Glen, D.M. et al 2006) Biodiversity vs. biocontrol: positive and negative effects of alternative prey on control of slugs by carabid beetles. Bulletin of Entomological Research, 96, 637 645.
52. Symondson, W.O.C., Erickson, M.L. Liddell, J.E 1997) Species-specific detection of predation by Coleoptera on the milacid slug Tandonia budapestensis (Mollusca: Pulmonata). Biocontrol Science & Technology, 7, 457 465.
53. Symondson, W.O.C., Erickson, M.L. Liddell, J.E 1999) Development of a monoclonal antibody for the detection and quantification of predation on slugs within the Arion hortensis agg. (Mollusca: Pulmonata). Biological Control, 16, 274 282.
54. Symondson, W.O.C., Glen, D.M., Ives, A.R., Langdon, C.J. Wiltshire, C.W 2002a) Dynamics of the relationship between a generalist predator and slugs over five years. Ecology, 83, 137 147.
55. Symondson, W.O.C., Glen, D.M., Wiltshire, C.W., Langdon, C.J. Liddell, J.E 1996) Effects of cultivation techniques and methods of straw disposal on predation by Pterostichus melanarius (Coleoptera: Carabidae) upon slugs (Gastropoda, Pulmonata) in an arable field. Journal of Applied Ecology, 33, 741 753.
56. Symondson, W.O.C. Liddell, J.E 1993) A monoclonal antibody for the detection of arionid slug remains in carabid predators. Biological Control, 3, 207 214.
57. Symondson, W.O.C. Liddell, J.E 1995) Decay-rates for slug antigens within the carabid predator Pterostichus melanarius monitored with a monoclonal-antibody. Entomologia Experimentalis et Applicata, 75, 245 250.
58. Symondson, W.O.C. Liddell, J.E 1996) A species-specific monoclonal antibody system for detecting the remains of Field Slugs, Deroceras reticulatum (Müller) (Mollusca: Pulmonata), in carabid beetles (Coleoptera: Carabidae). Biocontrol Science & Technology, 6, 91 99.
59. Symondson, W.O.C., Mendis, V.W. Liddell, J.E 1995) Monoclonal antibodies for the identification of slugs and their eggs. EPPO Bulletin, 25, 377 382.
60. Symondson, W.O.C., Sunderland, K.D. Greenstone, M.H 2002b) Can generalist predators be effective biocontrol agents? Annual Review of Entomology, 47, 561 594.
61. Thiele, H.U 1977) Carabid Beetles in Their Environment; A Study in Habitat Selection by Adaptation in Physiology and Behaviour. Springer-Verlag, Berlin, Germany.
62. Thomas, C.F.G., Parkinson, L. Marshall, E.J.P 1998) Isolating the components of activity-density for the carabid beetle Pterostichus melanarius in farmland. Oecologia, 116, 103 112.
63. Thomas, R.S 2002) An immunological and behavioural study of the role of carabid beetle larvae as slug control agents in cereal crops. PhD thesis, Cardiff University, Cardiff, U.K.
64. Thomas, R.S., Glen, D.M. Symondson, W.O.C 2007) Prey detection through olfaction by the soil dwelling larvae of the carabid predator Pterostichus melanarius. Soil Biology and Biochemistry, 40, 207 216.