Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-20T01:45:14.857Z Has data issue: false hasContentIssue false

Tracking medfly predation by the wolf spider, Pardosa cribata Simon, in citrus orchards using PCR-based gut-content analysis

Published online by Cambridge University Press:  08 June 2009

C. Monzó
Affiliation:
Unidad Asociada de Entomología del Instituto Valenciano de Investigaciones Agrarias y Centro de Investigaciones Biologicas del Consejo Superior de Investigaciones Científicas: Centro de Protección Vegetal y Biotecnología, Instituto Valenciano de Investigaciones Agrarias, Carretera de Moncada a Náquera km 4,5. Apartado 46113 Moncada, Valencia, Spain Unidad Asociada de Entomología del Instituto Valenciano de Investigaciones Agrarias y Centro de Investigaciones Biologicas del Consejo Superior de Investigaciones Científicas: Departamento Biología de Plantas, Centro de Investigaciones Biológicas, C/Ramiro de Maeztu, 9. 28040 Madrid, Spain
B. Sabater-Muñoz*
Affiliation:
Unidad Asociada de Entomología del Instituto Valenciano de Investigaciones Agrarias y Centro de Investigaciones Biologicas del Consejo Superior de Investigaciones Científicas: Centro de Protección Vegetal y Biotecnología, Instituto Valenciano de Investigaciones Agrarias, Carretera de Moncada a Náquera km 4,5. Apartado 46113 Moncada, Valencia, Spain
A. Urbaneja
Affiliation:
Unidad Asociada de Entomología del Instituto Valenciano de Investigaciones Agrarias y Centro de Investigaciones Biologicas del Consejo Superior de Investigaciones Científicas: Centro de Protección Vegetal y Biotecnología, Instituto Valenciano de Investigaciones Agrarias, Carretera de Moncada a Náquera km 4,5. Apartado 46113 Moncada, Valencia, Spain
P. Castañera
Affiliation:
Unidad Asociada de Entomología del Instituto Valenciano de Investigaciones Agrarias y Centro de Investigaciones Biologicas del Consejo Superior de Investigaciones Científicas: Departamento Biología de Plantas, Centro de Investigaciones Biológicas, C/Ramiro de Maeztu, 9. 28040 Madrid, Spain
*
*Author for correspondence Fax: +34 963424001 E-mail: [email protected]

Abstract

The Mediterranean fruit fly, Ceratitis capitata (Wiedemann), which is often controlled chemically, is a major citrus pest in Spain; however, alternative biological control strategies such as those based on the conservation of polyphagous predators should be developed. The wolf spider, Pardosa cribata Simon, is an abundant predator found in citrus orchards in eastern Spain. In this study, we have evaluated polymerase chain reaction (PCR)-based techniques as a means of detecting C. capitata DNA remains in P. cribata specimens. To do so, two pairs of C. capitata species-specific primers were designed and tested. Primer specificity was tested on species closely related to C. capitata and with other pests and natural enemies present in citrus orchards. Medfly DNA was detectable in 100% of P. cribata from 0 to 12 h post ingestion for both primer pairs, decreasing to 37% at 96 h after prey ingestion for one pair of primers. DNA detectability half-lives were of 78.25 h and 78.08 h for each pair of primers but no statistical differences were found between them. Pardosa cribata specimens were field-collected daily after sterile C. capitata pupae had been deployed in the citrus orchard. Afterwards, the wolf spiders were analyzed and DNA remains of C. capitata were detected in 5% of them, with a peak of 15% coinciding with maximum C. capitata emergence. This study is the first to reveal the potential use of DNA markers to track medfly predation by P. cribata in citrus orchards and provides a new tool to estimate the potential role of this spider in biological-control conservation programs.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Agustí, N., Aramburu, J. & Gabarra, R. (1999a) Immunological detection of Helicoverpa armigera (Lepidoptera: Noctuidae) ingested by heteropteran predators: time-related decay and effect of meal size on detection period. Annals of the Entomological Society of America 92, 5662.CrossRefGoogle Scholar
Agustí, N., De Vicente, M.C. & Gabarra, R. (1999b) Development of sequence amplified characterized region (SCAR) markers of Helicoverpa armigera: a new polymerase chain reaction-based technique for predator gut analysis. Molecular Ecology 8, 14671474.CrossRefGoogle ScholarPubMed
Agustí, N., De Vicente, M.C. & Gabarra, R. (2000) Developing SCAR markers to study predation on Trialeurodes vaporariorum. Insect Molecular Biology 9, 263268.CrossRefGoogle ScholarPubMed
Agustí, N., Shayler, S.P., Harwood, J.D., Vaughan, I.P., Sunderland, K.D. & Symondson, W.O.C. (2003a) Collembola as alternative prey sustaining spiders in arable ecosystems: prey detection within predators using molecular markers. Molecular Ecology 12, 34673475.CrossRefGoogle ScholarPubMed
Agustí, N., Unruh, T.R. & Welter, S.C. (2003b) Detecting Cacopsylla pyricola (Hemiptera: Psyllidae) in predator guts using COI mitochondrial markers. Bulletin of Entomological Research 93, 179185.CrossRefGoogle ScholarPubMed
Chen, Y., Giles, K.L., Payton, M.E. & Greenstone, M.H. (2000) Identifying key cereal aphid predators by molecular gut analysis. Molecular Ecology 9, 18871898.CrossRefGoogle ScholarPubMed
Chueca, P., Montón, H., Ripollés, J.L., Castañera, P., Moltó, E. & Urbaneja, A. (2007) Spinosad bait treatments as an alternative to malathion in controlling the Mediterranean fruit fly, Ceratitis capitata, (Diptera: Tephritidae) in the Mediterranean Basin. Journal of Pesticide Science 32, 407411.CrossRefGoogle Scholar
de León, J.H., Fournier, V., Hagler, J.R. & Daane, K.M. (2006) Development of molecular diagnostic markers for sharpshooters Homalodisca coagulata and Homalodisca liturata for use in predator gut content examinations. Entomologia Experimentalis et Applicata 119, 109119.CrossRefGoogle Scholar
Foltan, P., Sheppard, S., 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, 41474158.CrossRefGoogle ScholarPubMed
Fournier, V., Hagler, J., Daane, K., de León, J. & Groves, R. (2008) Identifying the predator complex of Homalodisca vitripennis (Hemiptera: Cicadellidae): a comparative study of the efficacy of an ELISA and PCR gut content assay. Oecologia 157, 629640.CrossRefGoogle ScholarPubMed
Greenstone, M.H. (1999) Spider predation: How and why we study it. Journal of Arachnology 27, 333342.Google Scholar
Greenstone, M.H., Rowley, D.L., Weber, D.C., Payton, M.E. & Hawthorne, D.J. (2007) 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 97, 201209.CrossRefGoogle ScholarPubMed
Hagler, J.R., Naranjo, S.E., Bradleydunlop, D., Enriquez, F.J. & Henneberry, T.J. (1994) A monoclonal-antibody to Pink-Bollworm (Lepidoptera, Gelechiidae) egg antigen – A tool for predator gut analysis. Annals of the Entomological Society of America 87, 8590.CrossRefGoogle Scholar
Hagler, J.R., Naranjo, S.E., Erickson, M.L., Machtley, S.A. & Wright, S.F. (1997) Immunological examinations of species variability in predator gut content assays: Effect of predator:prey protein ratio on immunoassay sensitivity. Biological Control 9, 120128.CrossRefGoogle Scholar
Hagen, K.S., Mills, N.J., Gordh, G. & McMurtry, J.A. (1999) Terrestrial arthropod predators of insects and mite pests. pp. 383504in Bellows, T.S. & Fisher, T.W. (Eds) Handbook of Biological Control: Principles and Applications of Biological Control. San Diego, USA, Academic Press.CrossRefGoogle Scholar
Harper, G.L., King, R.A., Dodd, C.S., Harwood, J.D., Glen, D.M., Bruford, M.W. & Symondson, W.O.C. (2005) Rapid screening of invertebrate predators for multiple prey DNA targets. Molecular Ecology 14, 819827.CrossRefGoogle ScholarPubMed
Harwood, J.D. & Obrycki, J.J. (2005) Quantifying aphid predation rates of generalist predators in the field. European Journal of Entomology 102, 335350.CrossRefGoogle Scholar
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, 20492057.CrossRefGoogle Scholar
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, 20592067.CrossRefGoogle ScholarPubMed
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, 344352.CrossRefGoogle ScholarPubMed
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, 947963.CrossRefGoogle ScholarPubMed
Latorre, A., Moya, A. & Ayala, F.J. (1986) Evolution of mitochondrial DNA in Drosophila subobscura. Proceedings of the National Academy of Sciences, USA 83, 86498653.CrossRefGoogle ScholarPubMed
Legaspi, J.C., Legaspi, B.C., Meagher, R.L. & Ciomperlik, M.A. (1996) Evaluation of Serangium parcesetosum (Coleoptera: Coccinellidae) as a biological control agent of the silverleaf whitefly (Homoptera: Aleyrodidae). Environmental Entomology 25, 14211427.CrossRefGoogle Scholar
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 (Aranaea, Lycosidae). Journal of Applied Entomology 129, 330335.CrossRefGoogle Scholar
Magaña, C., Hernández-Crespo, P., Ortego, F. & Castañera, P. (2007) Resistance to Malathion in Field Populations of Ceratitis capitata. Journal of Economic Entomology 100, 18361843.CrossRefGoogle ScholarPubMed
Magaña, C., Hernández-Crespo, P., Brun-Barale, A., Couso-Ferrer, F., Bride, J.M., Castañera, P., Feyereisen, R. & Ortego, F. (2008) Mechanisms of resistance to malathion in the medfly Ceratitis capitata. Insect Biochemistry and Molecular Biology 38, 756762.CrossRefGoogle ScholarPubMed
Marc, P., Canard, A. & Ysnel, F. (1999) Spiders (Araneae) useful for pest limitation and bioindication. Agriculture, Ecosystems and Environment 74, 229273.CrossRefGoogle Scholar
Monzó, C., Sabater-Muñoz, B., Urbaneja, A. & Castañera, P. (2007) Importancia de los depredadores polífagos presentes en suelo de los cítricos en la depredación de Ceratitis capitata. Phytoma España 194, 1314.Google Scholar
Monzó, C., Mollá, O., Castañera, P. & Urbaneja, A. (2009) Activity density of Pardosa cribata in Spanish citrus orchards and its predatory capacity on Ceratitis capitata and Myzus persicae. BioControl 54, 393402.CrossRefGoogle Scholar
Morris, T.I., Campos, M., Kidd, N.A.C. & Symondson, W.O.C. (1999) What is consuming Prays oleae (Bernard) (Lep.: Yponomeutidae) and when: a serological solution? Crop Protection 18, 1722.CrossRefGoogle Scholar
Nicholas, K.B., Nicholas, H.B. Jr & Deerfield, D.W. II (1997) GeneDoc: Analysis and Visualization of Genetic Variation. EMBNET.news 4, 14.Google Scholar
Rychlik, W. (1992) OLIGO 4.06, Primer Analysis Software. National Biosciences Inc. Publishers, Plymouth, USA.Google Scholar
San Andrés, V., Urbaneja, A., Sabater-Muñoz, B. & Castañera, P. (2007) A novel molecular approach to assess mating success of sterile Ceratitis capitata (Diptera: Tephritidae) males in sterile insect technique programs. Journal of Economic Entomology 100, 14441449.CrossRefGoogle ScholarPubMed
Sheppard, S.K., Henneman, M.L., Memmott, J. & Symondson, W.O.C. (2004) Infiltration by alien predators into invertebrate food webs in Hawaii: a molecular approach. Molecular Ecology 13, 20772088.CrossRefGoogle ScholarPubMed
Sheppard, S.K., Bell, J., Sunderland, K.D., Fenlon, J., Skervin, D. & Symondson, W.O.C. (2005) Detection of secondary predation by PCR analyses of the gut contents of invertebrate generalist predators. Molecular Ecology 14, 44614468.CrossRefGoogle ScholarPubMed
Sunderland, K. (1999) Mechanisms underlying the effects of spiders on pest populations. The Journal of Arachnology 27, 308316.Google Scholar
Sunnucks, P. & Hales, D.F. (1996) Numerous transposed sequences of mitochondrial cytochrome oxidase I–II in aphids of the genus Sitobion (Hemiptera: Aphididae). Molecular Biology and Evolution 13, 510524.CrossRefGoogle ScholarPubMed
Symondson, W.O.C. (2002) Molecular identification of prey in predator diets. Molecular Ecology 11, 627641.CrossRefGoogle ScholarPubMed
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, 741753.CrossRefGoogle Scholar
Symondson, W.O.C., Gasull, T. & Liddell, J.E. (1999) Rapid identification of adult whiteflies in plant consignments using monoclonal antibodies. Annals of Applied Biology 134, 271276.CrossRefGoogle Scholar
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, 137147.CrossRefGoogle Scholar
Symondson, W.O.C., Sunderland, K.D. & Greenstone, M.H. (2002b) Can generalist predators be effective biocontrol agents? Annual Review of Entomology 47, 561594.CrossRefGoogle ScholarPubMed
Traugott, M. (2003) The prey spectrum of larval and adult Cantharis species in arable land: An electrophoretic approach. Pedobiologia 47, 161169.CrossRefGoogle Scholar
Urbaneja, A., Mari, F.G., Tortosa, D., Navarro, C., Vanaclocha, P., Bargues, L. & Castañera, P. (2006) Influence of ground predators on the survival of the mediterranean fruit fly pupae, Ceratitis capitata, in Spanish citrus orchards. Biocontrol 51, 611626.CrossRefGoogle Scholar
Zaidi, R.H., Jaal, Z., Hawkes, N.J., Hemingway, J. & Symondson, W.O.C. (1999) Can multiple-copy sequences of prey DNA be detected amongst the gut contents of invertebrate predators? Molecular Ecology 8, 20812087.CrossRefGoogle ScholarPubMed