Prey-mediated effects of the protease inhibitor aprotinin on the predatory carabid beetle Nebria brevicollis

Journal of Insect Physiology

Volumn 48, Issue 12, 2002, Pages 1093-1101

  Burgess, E P J ^a   Lövei, Gabor L ^b   Malone, L A ^a   Nielsen, I W ^b   Gatehouse, H S ^a   Christeller, J T ^a  

^a THE NEW ZEALAND INSTITUTE FOR PLANT AND FOOD RESEARCH LIMITED   (New Zealand)

^b DANISH INSTITUTE OF AGRICULTURAL SCIENCES   (Denmark)

Author keywords

Ground beetles; Helicoverpa armigera; Nebria brevicollis; Protease inhibitor; Transgenic plant; Tri trophic interactions

Indexed keywords

BEETLE; ENZYME; INHIBITION; PREDATOR-PREY INTERACTION;

CARABIDAE; COLEOPTERA; HELICOVERPA ARMIGERA; NEBRIA BREVICOLLIS;

EID: 0036895018     PISSN: 00221910     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-1910(02)00202-0     Document Type: Article

References (60)

1. Allsopp, P.G., Nutt, K.A., Geijskes, R.J., Smith, G.R., Suasa, A.W., 2000. Transgenic sugarcane with increased resistance to canegrubs. In: Allsopp, P.G. (Ed.), Sugarcane Pest Management in the New Millennium, 4th Sugarcane Entomology Workshop, International Society for Sugar Cane Technology, Khon Kaen, Thailand, 7-10 February., pp. 63-67.
2. Ashouri, A., Overney, S., Michaud, D., Cloutier, C., 1998. Fitness and feeding are affected in the two-spotted stinkbug, Perillus bioculatus, by the cysteine proteinase inhibitor, Oryzacystatin I. Archives of Insect Biochemistry and Physiology 38, 74-83.
3. Bell, H., Fitches, E.C., Down, R., Ford, L., Marris, G., Edwards, J., Gatehouse, J.A., Gatehouse, A.M.R., 2001. The effect of dietary cowpea trypsin inhibitor (CpTI) on the growth and development of the tomato moth Lacanobia oleracea (Lepidoptera: Noctuidae) and on the success of the gregarious ectoparasitoid Eulophus pennicornis (Hymenoptera: Eulophidae). Pest Management Science 57, 57-65.
4. Broadway, R.M., 1997. Dietary regulation of serine proteinases that are resistant to serine proteinase inhibitors. Journal of Insect Physiology 43, 855-874.
5. Broadway, R.M., Duffey, S.S., 1986. Plant proteinase inhibitors: mechanism of action and effect on the growth and digestive physiology of larval Heliothis zea and Spodoptera exiqua. Journal of Insect Physiology 32, 827-833.
6. Broadway, R.M., Duffey, S.S., 1988. The effect of plant protein quality on insect digestive physiology and the toxicity of plant proteinase inhibitors. Journal of Insect Physiology 34, 1111-1117.
7. Burgess, E.P.J., Stevens, P.S., Keen, G.K., Laing, W.A., Christeller, J.T., 1991. Effects of protease inhibitors and dietary protein level on the black field cricket, Teleogryllus commodus. Entomologia Experimentalis et Applicata 61, 123-130.
8. Cheung, A.C., Gooding, R.H., 1970. A study of trypsin in Calosoma calidum (FAB.) and Carabus taedatus FAB. Comparative Biochemistry and Physiology B 37, 331-338.
9. Christeller, J.T., Burgess, E.P.J., Mett, V., Gatehouse, H.S., Markwick, N.P., Murray, C., Malone, L.A., Wright, M., Philip, B.A., Watt, D., Gatehouse, L.N., Lövei, G.L., Shannon, A.L., Phung, M.M., Watson, L., Laing, W.A., 2002. The expression of a mammalian proteinase inhibitor, bovine spleen trypsin inhibitor (SI), in tobacco and effects on Helicoverpa armigera larvae. Transgenic Research 11, 161-173.
10. Conway, G., Toenniessen, G., 1999. Feeding the world in the twenty-first century. Nature 402 (Suppl.), C55-C58.
11. Coppedge, B.R., Jones, J.M., Felton, G.W., Stephen, F.M., 1994. Examination of midgut proteinases of the adult southern pine beetle (Coleoptera: Scolytidae). Journal of Entomological Science 29, 457-465.
12. Couty, A., de la Vina, G., Clark, S.J., Kaiser, L., Pham-Delegue, M.H., Poppy, G.M., 2001. Direct and indirect sublethal effects of Galanthus nivalis agglutinin (GNA) on the development of a potato-aphid parasitoid, Aphelinus abdominalis (Hymenoptera Aphelinidae). Journal of Insect Physiology 47, 553-561.
13. Daily, G.C., 1997. Nature's Services. Island Press, Washington, DC.
14. De Boer, J., Schuler, T., 2000. Risk assessment of GM crops: Do GM apple trees affect predatory mites? Antenna London B76.
15. De Leo, F., Bonade-Bottino, M., Ceci, L.R., Gallerani, R., Jouanin, L., 2001. Effects of a mustard trypsin inhibitor expressed in different plants on three lepidopteran pests. Insect Biochemistry and Molecular Biology 31, 593-602.
16. Delledonne, M., Allegro, G., Belenghi, B., Balestrazzi, A., Picco, F., Levine, A., Zelasco, S., Calligari, P., Confalonieri, M., 2001. Transformation of white poplar (Populus alba L.) with a novel Arabidopsis thaliana cysteine proteinase inhibitor and analysis of insect pest resistance. Molecular Breeding 7, 35-42.
17. Down, R.E., Ford, L., Mosson, H.J., Fitches, E., Gatehouse, J.A., Gatehouse, A.M.R., 1999. Protease activity in the larval stage of the parasitoid wasp, Eulophus pennicornis (Nees) (Hymenoptera: Eulophidae); effects of protease inhibitors. Parasitology 119, 157-166.
18. Dutton, A., Klein, H., Romeis, J., Bigler, F., 2002. Uptake of Bt-toxin by herbivores feeding on transgenic maize and consequences for the predator Chrysoperla carnea. Ecological Entomology 27, 441-447.
19. Gatehouse, J.A., Gatehouse, A.M.R., Brown, D.P., 2000. Control of phytophagous insect pests using serine proteinase inhibitors. In: Michaud, D. (Ed.), Recombinant Protease Inhibitors in Plants. Landes Bioscience, Eurekah. com, Texas, USA, pp. 9-26.
20. Gatehouse, L.N., Shannon, A., Burgess, E.P.J., Christeller, J.T., 1997. Characterization of major midgut proteinase cDNAs from Helicoverpa armigera larvae and changes in gene expression in response to four proteinase inhibitors in the diet. Insect Biochemistry and Molecular Biology 27, 929-944.
21. Gebhard, W., Tchesche, H., Fritz, H., 1986. Biochemistry of aprotinin and aprotinin-like inhibitors. In: Barett, A.J., Salvesen, G. (Eds.), Proteinase Inhibitors. Elsevier, Amsterdam, pp. 375-388.
22. Gooding, R.H., Huang, C.T., 1969. Trypsin and chymotrypsin from the beetle Pterostichus melanarius. Journal of Insect Physiology 15, 325-339.
23. Green, N.M., Work, E., 1953. Pancreatic trypsin inhibitor. 2. Reaction with trypsin. Biochemical Journal 54, 347-352.
24. Hunter-Fujita, F.R., Entwistle, P.F., Evans, H.F., Crook, N.E., 1998. Insect Viruses and Pest Management. Wiley, Chichester.
25. Johnston, K.A., Gatehouse, J.A., Anstee, J.H., 1993. Effects of soybean protease inhibitors on the growth and development of larval Helicoverpa armigera. Journal of Insect Physiology 39, 657-664.
26. Jongsma, M.A., Bolter, C., 1977. The adaptation of insects to plant proteinase inhibitors. Journal of Insect Physiology 43, 885-895.
27. Jørgensen, H.B., Lövei, G.L., 1999. Tri-trophic effect on predator feeding: Consumption by the carabid Harpalus affinis of Heliothis armigera caterpillars fed on proteinase inhibitor-containing diet. Entomologia Experimentalis et Applicata 93, 113-116.
28. Kalbfleisch, J.D., Prentice, R.L., 1980. Statistical Analysis of Failure Time Data. Wiley, New York.
29. Laskowski, M. Jr., Kato, I., 1980. Protein inhibitors of proteinases. Annual Review of Biochemistry 49, 593-626.
30. Lee, S.I., Lee, S.H., Koo, J.C., Chun, J.C., Lim, C.O., Mun, J.H., Song, Y.H., Cho, M.J., 1999. Soybean Kunitz trypsin inhibitor (SKTI) confers resistance to the brown planthopper (Nilaparvata lugens Stal) in transgenic rice. Molecular Breeding 5, 1-9.
31. Lehane, M.J., Blakemore, D., Williams, S., Moffatt, M.R., 1995. Regulation of digestive enzyme levels in insects. Comparative Biochemistry and Physiology B 110, 285-289.
32. Lindroth, C.H., 1985. The Carabidae (Coleoptera) of Fennoscandia and Denmark. Fauna Entomologica Scandinavica, vol. 15, pt 1. Scandinavian Science Press Ltd, Leiden, Copenhagen.
33. Lövei, G.L., 2001. Ecological risks and benefits of transgenic plants. Proceedings of the New Zealand Plant Protection Society 54, 93-100.
34. Lövei, G., Jørgensen, H., McCambridge, M., 2000. Effect of a proteinase inhibitor across trophic levels: Short vs. long-term consequences for a predator. Antenna London 245, 78.
35. Lövei, G.L., Sarospataki, M., 1990. Carabids in agricultural fields in Eastern Europe. In: Stork, N.E. (Ed.), The Role of Ground Beetles in Ecological and Environmental Research. Intercept Ltd, Hanover, UK, pp. 87-93.
36. Lövei, G.L., Sunderland, K.D., 1996. The ecology and behaviour of ground beetles. Annual Review of Entomology 41, 231-256.
37. McManus, M.T., Burgess, E.P.J., 1995. Effects of the soybean (Kunitz) trypsin inhibitor on growth and digestive proteases of larvae of Spodoptera litura. Journal of Insect Physiology 41, 731-738.
38. McManus, M.T., Burgess, E.P.J., Philip, B.A., Watson, L.M., Laing, W.A., Voisey, C.R., White, D.W.R., 1999. Expression of the soybean (Kunitz) trypsin inhibitor in transgenic tobacco: Effects on larval development of Spodoptera litura. Transgenic Research 8, 383-395.
39. Markwick, N.P., Laing, W.A., Christeller, J.T., McHenry, J.Z., Newton, M.R., 1998. Overproduction of digestive enzymes compensates for inhibitory effects of protease and α-amylase inhibitors fed to three species of leafrollers (Lepidoptera: Tortricidae). Journal of Economic Entomology 91, 1265-1276.
40. Mayntz, D., Toft, S., 2001. Nutrient composition of the prey's diet affects growth and survivorship of a generalist predator. Oecologia 127, 207-213.
41. Murugan, K., Kumar, N.S., Jeyabalan, D., Nathan, S.S., Sivaramakrishnan, S., Swamiappan, M., 2000a. Influence of Helicoverpa armigera (Hubner) diet on its parasitoid Campoletis chlorideae Uchida. Insect Science and its Application 20, 23-31.
42. Murugan, K., Jeyabalan, D., Kumar, N.S., Nathan, S.S., Sivaramakrishnan, S., 2000b. Influence of host plant on growth and reproduction of Aphis nerii and feeding and prey utilization of its predator Menochilus sexmaculatus. Indian Journal of Experimental Biology 38, 598-603.
43. Nelemans, M.N.E., 1987. On the life-history of the carabid beetle Nebria brevicollis (F.). Netherlands Journal of Zoology 37, 26-42.
44. Nelemans, M.N.E., den Boer, P.J., Spee, A., 1989. Recruitment and summer diapause in the dynamics of a population of Nebria brevicollis (F.) (Coleoptera, Carabidae). Oikos 56, 157-169.
45. Overney, S., Yelle, S., Cloutier, C., 1998. Occurrence of cysteine digestive proteases in Perillus bioculatus, a natural predator of the Colorado potato beetle. Comparative Biochemistry and Physiology B 120, 191-196.
46. Penney, M.M., 1969. Diapause and reproduction in Nebria brevicollis (F.) (Coleoptera: Carabidae). Journal of Animal Ecology 38, 219-233.
47. Price, P.W., Bouton, C.E., Gross, P., McPheron, B.A., Thompson, J.N., Weis, A.E., 1980. Interactions among three trophic levels: Influence of plants on interactions between insect herbivores and natural enemies. Annual Review of Ecology and Systematics 11, 41-65.
48. Scherney, F., 1959. Unsere Laufkaefer. Ziemsen Verlag, Wittenberg.
49. Schuler, T.H., Denholm, I., Jouanin, L., Clark, S.J., Clark, A.J., Poppy, G.M., 2001. Population-scale laboratory studies of the effect of transgenic plants on nontarget insects. Molecular Ecology 10, 1845-1853.
50. Silva, C.P., Terra, W.R., Lima, R.M., 2001. Differences in midgut serine proteinases from larvae of the bruchid beetles Callosobruchus maculatus and Zabrotes subfasciatus. Archives of Insect Biochemistry and Physiology 47, 18-28.
51. Strand, A., Hurry, V., Henkes, S., Huner, N., Gustafsson, P., Gardeström, P., Stitt, M., 1999. Acclimation of Arabidopsis leaves developing at low temperatures, Increasing cytoplasmic volume accompanies increased activities of enzymes in the Calvin cycle and in the sucrose-biosynthesis pathway. Plant Physiology 119, 1387-1398.
52. Terra, W.R., Cristofoletti, P.T., 1996. Midgut proteases in three divergent species of Coleoptera. Comparative Biochemistry and Physiology B 113, 725-730.
53. Thie, N.M.R., Houseman, J.G., 1990. Cysteine and serine proteolytic activities in larval midgut of yellow mealworm, Tenebrio molitor L. (Coleoptera: Tenebrionidae). Insect Biochemistry 20, 741-744.
54. Thiele, H.-U., 1977. Carabid Beetles in Their Environments. A Study on Habitat Selection by Adaptations in Physiology and Behaviour. Springer, Berlin/Heidelberg/New York.
55. Tilman, D., Fargione, J., Wolff, B., D'Antonio, C., Dobson, A., Howarth, R., Schindler, D., Schlesinger, W.H., Simberloff, D., Swackhamer, D., 2001. Forecasting agriculturally driven global environmental change. Science 292, 281-284.
56. USDA, 2002. Nutrient Database for Standard Reference, Release 15 (August 2002), USDA Agricultural Research Service, Nutrient Data Laboratory. Available from http://www.nal.usda.gov/fnic/cgi-bin/nut - search.pl.
57. Vaje, S., Mossakowski, D., Gabel, D., 1984. Temporal, intra-and inter-specific variation of proteolytic enzymes in carabid beetles. Insect Biochemistry 14, 313-320.
58. Van der Putten, W.H., Vet, L.E.M., Harvey, J.A., Wackers, F.L., 2001. Linking above- and below-ground multitrophic interactions of plants, herbivores, pathogens, and their antagonists. Trends in Ecology and Evolution 16, 547-554.
59. Vet, L.E.M., 1999. From chemical to population ecology: Infochemical use in an evolutionary context. Journal of Chemical Ecology 25, 31-49.
60. Voisey, C.R., Dudas, B., Biggs, R., Burgess, E.P.J., Wigley, P.J., McGregor, P.G., Lough, A.J., Beck, D.L., Forster, R.L.S., White, D.W.R., 2000. Transgenic pest and disease resistant white clover plants. In: Spangenberg, G. (Ed.), Proceedings of the Second International Symposium on Molecular Breeding of Forage Crops, Lorne and Hamilton, Australia. 19-24 November 2000. Molecular Breeding of Forage Crops: Developments in Plant Breeding, vol. 10. Kluwer Academic Publishers, London, pp. 239-250.