Feeding mode and prey detectability half-lives in molecular gut-content analysis: An example with two predators of the Colorado potato beetle

Bulletin of Entomological Research

Volumn 97, Issue 2, 2007, Pages 201-209

  Greenstone, M H ^a   Rowley, D L ^a   Weber, D C ^a   Payton, M E ^b   Hawthorne, D J ^c  

^a AGRICULTURAL RESEARCH SERVICE   (United States)

^b OKLAHOMA STATE UNIVERSITY   (United States)

^c University of Maryland   (United States)

Author keywords

Chrysomelidae; Coccinellidae; Coleomegilla; DNA half life; Gut analysis; Leptinotarsa; PCR; Podisus

Indexed keywords

DNA;

BEETLE; BIOASSAY; DIGESTION; DNA; FEEDING BEHAVIOR; HALF LIFE; POLYMERASE CHAIN REACTION; POPULATION DECLINE; PREDATOR; PREY AVAILABILITY;

ANIMAL; ARTICLE; BEETLE; COMPARATIVE STUDY; DIGESTION; DIGESTIVE FUNCTION; FEEDING BEHAVIOR; HETEROPTERA; INSECT CONTROL; METABOLISM; PHYSIOLOGY; PREDATION; STOMACH JUICE; TIME;

ANIMALS; BEETLES; DIGESTION; DIGESTIVE PHYSIOLOGY; DNA; FEEDING BEHAVIOR; GASTROINTESTINAL CONTENTS; HETEROPTERA; INSECT CONTROL; PREDATORY BEHAVIOR; TIME FACTORS;

ANIMALIA; CHRYSOMELIDAE; COCCINELLIDAE; COLEOMEGILLA; COLEOMEGILLA MACULATA; LEPTINOTARSA; LEPTINOTARSA DECEMLINEATA; PODISUS; PODISUS MACULIVENTRIS;

EID: 34248181909     PISSN: 00074853     EISSN: 14752670     Source Type: Journal    
DOI: 10.1017/S000748530700497X     Document Type: Article

References (69)

1. Admassu, B., Juen, A. & Traugott, M. (2006) Earthworm primers for DNA-based gut content analysis and their cross-reactivity in a multi-species system. Soil Biology and chemistry 38, 1308-1315.
2. Aldrich, J.R. & Cantelo, W.W. (1999) Suppression of Colorado potato beetle infestation by pheromone-mediated augmentation of the predatory spined soldier bug, Podisus maculiventris (Say) (Heteroptera: Pentatomidae). Agricultural and Forest Entomology 1, 209-217.
3. Anderson, J.F. (1970) Metabolic rates of spiders. Comparative Biochemistry and Physiology 33, 51-72.
4. BARC (2003) Beltsville Area Research Center, Station no. 2 North Farm - History and Information (http://www.ba.ars.usda.gov/weather/ba-weather-2. html).
5. Benton, A.H. & Crump, J. (1981) Observations on the spring and summer behavior of the 12-spotted ladybird beetle, Coleomegilla maculata (DeGeer) (Coleoptera: Coccinellidae). Journal of the New York Entomological Society 89, 102-105.
6. Butt, J.H. (1951) Feeding habits and mechanism of the Mexican bean beetle. Memoirs of the Cornell University Agricultural Experiment Station 306, 1-32.
7. Byrne, A., Grafius, E., Bishop, B. & Pett, W. (2004) Susceptibility of Colorado potato beetle populations to imidacloprid and thiamethoxam. Arthropod Management Tests 29, L12.
8. Calder, C.R., Harwood, J.D. & Symondson, W.O.C. (2005) Detection of scavenged material in the guts of predators using monoclonal antibodies: a significant source of error? Bulletin of Entomological Research 95, 57-62.
9. Chang, G.C. & Kareiva, P. (1999) The case for indigenous generalists in biological control. pp. 103-115 in Hawkins, B.A. & Cornell, H.V. (Eds) Theoretical approaches to biological control. Cambridge, Cambridge University Press.
10. Chen, Y.K., Giles, K.L., Payton, M.E. & Greenstone, M.H. (2000) Identifying key cereal aphid predators by molecular gut analysis. Molecular Ecology 9, 1887-1898.
11. Cohen, A.C. (1990) Feeding adaptations of some predaceous Hemiptera. Annals of the Entomological Society of America 83, 1215-1223.
12. Cohen, A.C. (1998) Solid-to-liquid feeding: the inside(s) story of extra-oral digestion in predaceous Arthropoda. American Entomologist 14, 103-117.
13. Coll, M. & Guershon, M. (2002) Omnivory in terrestrial arthropods: mixing plant and prey diets. Annual Review of Entomology 47, 267-297.
14. De León, J.H., Fournier, V., Hagler, J.R. & Daane, K.M. (2006) Development of diagnostic markers for sharpshooters Homalodisca coagulata and Homalodisca liturata for use in predator gut content examinations. Entomologia Experimentalis et Applicata 119, 109-119.
15. Dempster, J.P. (1960) Quantitative study of the predators on the eggs and larvae of the broom beetle, Phytodecta olivacea Forster, using the precipitin test. Journal of Animal Ecology 29, 149-154.
16. Ehrlich, H.A. (1989) PCR technology: principles and applications for DNA amplification. New York, Stockton Press.
17. Ferro, D.N. (1994) Biological control of the Colorado potato beetle. pp. 357-375 in Zehnder, G.W., Powelson, M.L., Jansson, R.K. & Raman, K.V.A. (Eds) Advances in potato pest biology and management. St Paul, Minnesota, American Phytopathological Society Press.
18. Fichter, B.L. & Stephen, W.P. (1981) Time-related decay in prey antigens ingested by the predator Podisus maculiventris (Hemiptera, Pentatomidae) as detected by ELISA. Oecologia 51, 404-407.
19. 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.
20. Fournier, V., Hagler, J.R., Daane, K.M., de Leon, J.H., Groves, R.L., Costa, H.S. & Henneberry, T.J. (2006) Development and application of a glassy-winged and smoke-tree sharpshooter egg-specific predator gut-content ELISA. Biological Control 37, 108-111.
21. Greenstone, M.H. (1979) Spider feeding behaviour optimises dietary essential amino acid composition. Nature 181, 501-503.
22. Greenstone, M.H. (1996) Serological analysis of arthropod predation: past, present and future. pp. 265-300 in Symondson, W.O.C. & Liddell, J.E. (Eds) The ecology of agricultural pests - biochemical approaches. London, Chapman and Hall.
23. Greenstone, M.H. (1999) Spider predation: why and how we study it. Journal of Arachnology 27, 333-342.
24. Greenstone, M.H. & Bennett, A.F. (1980) Foraging strategy and metabolic rate in spiders. Ecology 61, 1255-1259.
25. Greenstone, M.H. & Hunt, J.H. (1993) Determination of prey antigen half-life in Polistes metricus using a monoclonal antibody-based immunodot assay. Entomologia Experimentalis et Applicata 68, 1-7.
26. Greenstone, M.H. & Morgan, C.E. (1989) Predation on Heliothis zea (Lepidoptera: Noctuidae): an instar specific ELISA assay for stomach analysis. Annals of the Entomological Society of America 82, 45-49.
27. Greenstone, M.H., Rowley, D.L., Heimbach, U., Lundgren, J.G., Pfannenstiel, R.S. & Rehner, S.A. (2005) Barcoding generalist predators by polymerase chain reaction: carabids and spiders. Molecular Ecology 14, 3247-3266.
28. Groden, E., Drummond, F.A., Casagrande, R.A. & Haynes, D.L. (1990) Coleomegilla maculata (Coleoptera: Coccinellidae): its predation upon the Colorado potato beetle (Coleoptera: Chrysomelidae) and its incidence in potatoes and surrounding crops. Journal of Economic Entomology 83, 1306-1315.
29. Gurr, G.M. & Wratten, S.D. (Eds) (2000) Biological control: measures of success. Dordrecht, Kluwer.
30. Hagler, J.R. & Naranjo, S.E. (1997) Measuring the sensitivity of an indirect predator gut content ELISA: detectability of prey remains in relation to predator species, temperature, time, and meal size. Biological Control 9, 112-119.
31. Harwood, J.D., Phillips, S.W., Sunderland, K.D. & Symondson, W.O.C. (2001) Secondary predation: quantification of food chain errors in an aphid-spider-carabid system using monoclonal antibodies. Molecular Ecology 10, 2049-2057.
32. Harwood, J.D., Sunderland, K.D. & Symondson, W.O.C. (2004) Prey selection by linyphiid spiders: molecular tracking of the effects of alternative prey on rates of aphid consumption in the field. Molecular Ecology 13, 3549-3560.
33. Hazzard, R.V., Ferro, D.N., van Driesche, R.G. & Tuttle, A.F. (1991) Mortality of eggs of the Colorado potato beetle (Coleoptera: Chrysomelidae) from predation by Coleomegilla maculata (Coleoptera: Coccinellidae). Environmental Entomology 20, 841-848.
34. Heimpel, G.E. & Hough-Goldstein, J.A. (1992) A survey of arthropod predators of Leptinotarsa decemlineata (Say) in Delaware potato fields. Journal of Agricultural Entomology 9, 137-142.
35. Hilbeck, A., Eckel, C. & Kennedy, G.G. (1997) Predation on Colorado potato beetle eggs by generalist predators in research and commercial potato plantings. Biological Control 8, 191-196.
36. Holopainen, J.K. & Helenius, J. (1992) Gut contents of ground beetles (Col., Carabidae), and activity of these and other epigeal predators during an outbreak of Rhopalosiphum padi (Hom., Aphididae). Acta Agriculturae Scandinavica 42, 57-61.
37. Hoogendoorn, M. & Heimpel, G.E. (2001) PCR-based gut content analysis of insect predators: using ribosomal ITS-1 fragments from prey to estimate predation frequency. Molecular Ecology 10, 2059-2067.
38. Hough-Goldstein, J. & McPherson, D. (1996) Comparison of Perillus bioculatus and Podisus maculiventris (Hemiptera: Pentatomidae) as potential control agents of the Colorado potato beetle (Coleoptera: Chrysomelidae). Journal of Economic Entomology 89, 1116-1123.
39. Juen, A. & Traugott, M. (2005) Detecting predation and scavenging by DNA gut-content analysis: a case study using a soil insect predator-prey system. Oecologia 142, 344-352.
40. Juen, A. & Traugott, M. Revealing species-specific trophic links in soil food webs: molecular identification of scarab predators. Molecular Ecology in press.
41. Lister, A., Usher, M.B. & Block, W. (1987) Description and quantification of field attack rates by predatory mites: an example using an electrophoresis method with a species of Antarctic mite. Oecologia 72, 185-191.
42. Ma, J., Li, D., Keller, M., Schmidt, O. & Feng, X. (2005) A DNA marker to identify predation of Plutella xylostella (Lep., Plutellidae) by Nabis kinbergii (Hem., Nabidae) and Lycosa sp. (Araneae, Lycosidae). Journal of Applied Entomology 129, 330-335.
43. Mack, T. & Smilowitz, Z. (1980) The development of a green peach aphid natural enemy sampling procedure. Environmental Entomology 9, 440-445.
44. Mota-Sanchez, D., Hollingworth, E., Grafius, E. & Moyer, D. (2006) Resistance and cross-resistance to neonicotinoid insecticides and spinosad in the Colorado potato beetle (Coleoptera: Chrysomelidae) . Pest Management Science 62, 30-37.
45. Nakamura, M. & Nakamura, K. (1977) Population dynamics of the chestnut gall wasp, Dryocosmus kuriphilus Yamatsu (Hymenoptera: Cynipidae). V. Estimation of the effect of predation by spiders on the mortality of imaginal wasps based on the precipitin test. Oecologia 27, 97-116.
46. Payton, M.E., Greenstone, M.H. & Schenker, N. (2004) Overlapping confidence intervals or standard error intervals: what do they mean in terms of statistical significance? Journal of Insect Science 3, 1-6 (http://www.insectworld.org/3.34).
47. Read, D.M., 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 16, 1963-1972.
48. Riley, E., Clark, G.S.M. & Seeno, T.N. (2003) Catalog of the leaf beetles of America north of Mexico (Coleoptera: Megalopodidae, Orsodacnidae and Chrysomelidae, excluding Bruchinae). Coleopterists Society, Special Publication no. 1.
49. SAS Institute, Inc. (1999) SAS/STAT user's manual, version 8. 4th edn. SAS Institute.
50. Sheppard, S.K. & Harwood, J.D. (2005) Advances in molecular ecology: tracking trophic links through predator-prey food webs. Functional Ecology 19, 751-762.
51. Sheppard, S.K., Bell, J.R., Sunderland, K.D., Fenlon J., Skirvin, D. & Symondson, W.O.C. (2005) Detection of secondary predation by PCR analyses of the gut contents of invertebrate generalist predators. Molecular Ecology 14, 4461-4468.
52. Simon, C., Frati, F., Beckenbach, A., Crespi, B., Liu, H. & Flook, P. (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America 87, 651-701.
53. Sopp, P.I. & Sunderland, K.D. (1989) Some factors affecting the detection period of aphid remains in predators using ELISA. Entomologia Experimentalis et Applicata 51, 11-20.
54. Sopp, P.I., Sunderland, K.D., Fenlon, J.S. & Wratten, S.D. (1992) An improved quantitative method for estimating invertebrate predation in the field using an enzyme-linked immunosorbent assay (ELISA). Journal of Applied Ecology 79, 295-302.
55. Sunderland, K.D. (1975) The diet of some predatory arthropods in cereal crops. Journal of Applied Ecology 12, 507-515.
56. Sunderland, K.D. (1988) Quantitative methods for detecting invertebrate predation in the field. Annals of Applied Biology 112, 201-224.
57. Sunderland, K.D. (1999) Mechanisms underlying the effects of spiders on pest populations. Journal of Arachnology 27, 308-316.
58. Sunderland, K.D., Crook, N.E., Stacey, D.L. & Fuller, B.J. (1987) A study of feeding by polyphagous predators on cereal aphids using ELISA and gut dissection. Journal of Applied Ecology 24, 907-933.
59. Symondson, W.O.C. (2002) Molecular identification of prey in predator diets. Molecular Ecology 11, 627-641.
60. Symondson, W.O.C. & Liddell, J. (1995) Decay rates for slug antigens within the carabid predator Pterostichus melanarius monitored with a monoclonal antibody. Entomologia Experimentalis et Applicata 75, 245-250.
61. Symondson, W.O.C., Erickson, M.L. & Liddell, J. (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.
62. Symondson, W.O.C., Sunderland, K.D. & Greenstone, M.H. (2002) Can generalist predators be effective biocontrol agents? Annual Review of Entomology 47, 561-594.
63. Tipping, P.W., Holko, C., Abdul-Baki, A.A. & Aldrich, J.R. (1999) Evaluating Edovum puttleri Grissell and Podisus maculiventris (Say) for augmentative biological control of Colorado potato beetle in tomatoes. Biological Control 16, 35-42.
64. Triltsch, H. (1999) Food remains in the guts of Coccinella septempunctata (Coleoptera: Coccinellidae) adults and larvae. European Journal of Entomology 96, 355-364.
65. Wallace, S.K. (2004) Molecular gut analysis of carabids (Coleoptera: Carabidae) using aphid primers. Masters thesis, Montana State University, Bozeman, Montana, USA.
66. Weber, D.C. (2003) Colorado beetle: pest on the move. Pesticide Outlook 14, 256-259.
67. Weber, D.C., Rowley, D.L., Greenstone, M.H. & Athanas, M.M. (2006) Prey preference and host suitability of the predatory and parasitoid carabid beetle, Lebia grandis, for several species of Leptinotarsa beetles. 14 pp. Journal of Insect Science 6, 09 (http://www.insectworld.org/6.09).
68. Zaidi, R.H., Jaal, Z., Hawkes, N.J., Hemingway, J. & Symondson, W.O.C. (1999) Can the detection of prey DNA amongst the gut contents of invertebrate predators provide a new technique for quantifying predation in the field? Molecular Ecology 8, 2081-2088.
69. Zhao, J., Grafius, E. & Bishop, B. (2000) Inheritance and synergism of resistance to imidacloprid in the Colorado potato beetle (Coleoptera: Chrysomelidae). Journal of Economic Entomology 93, 1508-1514.