Hostname: page-component-586b7cd67f-dsjbd Total loading time: 0 Render date: 2024-11-26T07:56:26.276Z Has data issue: false hasContentIssue false
  • English
  • Français

The effect of Chrysoperla carnea (Neuroptera: Chrysopidae) and Adalia bipunctata (Coleoptera: Coccinellidae) on the spread of cucumber mosaic virus (CMV) by Aphis gossypii (Hemiptera: Aphididae)

Published online by Cambridge University Press:  11 September 2014

A. Garzón ,
F. Budia ,
P. Medina ,
I. Morales ,
A. Fereres  and
E. Viñuela
A. Garzón
Affiliation:
Unidad de Protección de Cultivos, E. T. S. I. Agrónomos, UPM, Avenida Complutense, s/n, 28040 Madrid, Spain
F. Budia
Affiliation:
Unidad de Protección de Cultivos, E. T. S. I. Agrónomos, UPM, Avenida Complutense, s/n, 28040 Madrid, Spain Associated Unit IVAS CSIC-UPM, Instituto de Ciencias Agrarias, CSIC, Serrano 115 Dpdo, 28006 Madrid, Spain
P. Medina
Affiliation:
Unidad de Protección de Cultivos, E. T. S. I. Agrónomos, UPM, Avenida Complutense, s/n, 28040 Madrid, Spain Associated Unit IVAS CSIC-UPM, Instituto de Ciencias Agrarias, CSIC, Serrano 115 Dpdo, 28006 Madrid, Spain
I. Morales
Affiliation:
Unidad de Protección de Cultivos, E. T. S. I. Agrónomos, UPM, Avenida Complutense, s/n, 28040 Madrid, Spain Associated Unit IVAS CSIC-UPM, Instituto de Ciencias Agrarias, CSIC, Serrano 115 Dpdo, 28006 Madrid, Spain
A. Fereres
Affiliation:
Instituto de Ciencias Agrarias, CSIC, Serrano 115 Dpdo, 28006 Madrid, Spain Associated Unit IVAS CSIC-UPM, Instituto de Ciencias Agrarias, CSIC, Serrano 115 Dpdo, 28006 Madrid, Spain
E. Viñuela*
Affiliation:
Unidad de Protección de Cultivos, E. T. S. I. Agrónomos, UPM, Avenida Complutense, s/n, 28040 Madrid, Spain Associated Unit IVAS CSIC-UPM, Instituto de Ciencias Agrarias, CSIC, Serrano 115 Dpdo, 28006 Madrid, Spain
*
*Author for correspondence E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The effects of two aphidophagous predators, the larvae of Chrysoperla carnea and adults of Adalia bipunctata, on the spread of cucumber mosaic virus (CMV) transmitted in a non-persistent manner by the cotton aphid Aphis gossypii were studied under semi-field conditions. Natural enemies and aphids were released inside insect-proof cages (1 m ×1 m ×1 m) with a central CMV-infected cucumber plant surrounded by 48 healthy cucumber seedlings, and the spatiotemporal dynamics of the virus and vector were evaluated in the short and long term (1 and 5 days) in the presence and absence of the natural enemy. The spatial analysis by distance indices methodology together with other indices measuring the dispersal around a single focus was used to assess the spatial pattern and the degree of association between the virus and its vector. Both natural enemies significantly reduced the number of aphids in the CMV-source plant after 5 days but not after 1 day. The CMV transmission rate was generally low, especially after 1 day, due to the limited movement of aphids from the central CMV-source plant, which increased slightly after 5 days. Infected plants were mainly located around the central virus-infected source plant, and the percentage of aphid occupation and CMV-infected plants did not differ significantly in absence and presence of natural enemies. The distribution patterns of A. gossypii and CMV were only coincident close to the central plant. The complexity of multitrophic interactions and the role of aphid predators in the spread of CMV are discussed.

Keywords

CMVAphis gossypiiChrysoperla carneaAdalia bipunctataSADIEmultitrophic interactions
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 105 , Issue 1 , February 2015 , pp. 13 - 22
Copyright
Copyright © Cambridge University Press 2014 

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

Abbott, W.S. (1925) A method of computing the effectiveness of an insecticide. Journal of Economic Entomology 18, 265–267.CrossRefGoogle Scholar
Abney, M.R., Ruberson, J.R., Herzog, G.A., Kring, T.J., Steinkraus, D.C. & Roberts, P.M. (2008) Rise and fall of cotton aphid (Hemiptera: Aphididae) populations in southeastern cotton production systems. Journal of Economic Entomology 101, 23–35.CrossRefGoogle ScholarPubMed
Adams, A.J. & Hall, F.R. (1990) Initial behavioural responses of Aphis gossypii to defined deposits of bifenthrin on chrysanthemum. Crop Protection 9(1), 39–43.Google Scholar
Bailey, S.M., Irwin, M.E., Kampmeier, G.E., Eastman, C.E. & Hewings, A.D. (1995) Physical and biological perturbations: their effect on the movement of apterous Rhopalosiphum padi (Homoptera: Aphididae) and localized spread of Barley yellow dwarf virus. Environmental Entomology 24, 24–33.Google Scholar
Belliure, B., Amorós-Jiménez, R., Fereres, A. & Marcos-García, M.A. (2011) Antipredator behaviour of Myzus persicae affects transmission efficiency of Broad bean wilt virus 1. Virus Research 159, 206–214.Google Scholar
Bonte, M., Samih, M.A. & De Clercq, P. (2010) Development and reproduction of Adalia bipunctata on factitious and artificial foods. Biocontrol 55(4), 485–491.Google Scholar
Candolfi, M.P., Barret, K.L., Campbell, P.J., Forster, R., Grandy, N., Huet, H.C., Lewis, G., Oomen, P.A., Schmuck, R. & Vogt, H. (2001). Guidance document on regulatory testing and risk assessment procedures for plant protection products with non-target arthropods. p. 46 in Proceedings of the ESCORT 2 Workshop, 21–23 March 2000, Wageningen, The Netherlands, SETAC Europe.Google Scholar
Clark, M.F. & Adams, A.N. (1977) Characteristics of the microplate method of enzyme-linked immunosorbent assay for the detection of plant viruses. Journal of General Virology 34, 475–483.Google Scholar
Collar, J.L., Avilla, C., Duque, M. & Fereres, A. (1995) Assessment of potato virus Y (PVY) spread in bell peppers treated with different insecticides. p. 3 in Abstracts, 6th International Plant Virus Epidemiology Symposium: Epidemiological Aspects of Plant Virus Control, 23–28 April 1995, Jerusalem, Israel.Google Scholar
Dáder, B., Moreno, A., Viñuela, E. & Fereres, A. (2012) Spatio-temporal dynamics of viruses are differentially affected by parasitoids depending on the mode of transmission. Viruses 4, 3069–3089.Google Scholar
Díaz, B.M., Legarrea, S., Marcos-García, M.A. & Fereres, A. (2010) The spatio-temporal relationships among aphids, the entomophthoran fungus, Pandora neoaphidis, and aphidophagous hoverflies in outdoor lettuce. Biological Control 53, 304–311.Google Scholar
Díaz, J.A., Mallor, C., Soria, C., Camero, R., Garzo, E., Fereres, A., Álvarez, J.M., Gómez-Guillamón, A.L., Luis-Arteaga, M. & Moriones, E. (2003) Potential sources of resistance for melon to nonpersistently aphid-borne viruses. Plant Disease 87, 960–964.Google Scholar
Duelli, P. (2001) Lacewings in field crops. pp. 158–171 in McEwen, P., New, T.R. & Whittington, A.E. (Eds) Lacewings in the Crop Environment. Cambridge, UK, Cambrigde University Press.Google Scholar
Ellingsen, I.J. (1969) Fecundity, aphid consumption and survival of the aphid predator Adalia bipunctata L. (Col., Coccinellidae). Norwegian Journal of Entomology 16(2), 91–95.Google Scholar
Fereres, A. & Moreno, A. (2009) Behavioural aspects influencing plant virus transmission by homopteran insects. Virus Research 141, 158–168.Google Scholar
Gurney, B. & Hussey, N.W. (1970) Evaluation of some coccinellid species for the biological control of aphids in protected cropping. Annals of Applied Biology 65, 451–458.CrossRefGoogle Scholar
Hodge, S. & Powell, G. (2008) Complex interactions between a plant pathogen and insect parasitoid via the shared vector–host: consequences for host plant infection. Oecologia 157, 387–397.CrossRefGoogle ScholarPubMed
Hodge, S., Hardie, J. & Powell, G. (2011) Parasitoids aid dispersal of a nonpersistently plant virus by disturbing the aphid vector. Agricultural and Forest Entomology 13, 83–88.Google Scholar
Hooks, C.R.R. & Fereres, A. (2006) Protecting crops from non-persistently aphid-transmitted viruses: a review on the use of barrier plants as a management tool. Virus Research 120, 1–16.Google Scholar
Jeger, M.J., Holt, J., van den Bosch, F. & Madden, L.V. (2004) Epidemiology of insect-transmitted plant viruses: modeling disease dynamics and control interventions. Physiological Entomology 29, 291–304.Google Scholar
Jeger, M.J., Chen, Z., Cunningham, E., Martin, G. & Powell, G. (2012) Population biology and epidemiology of plant virus epidemics: from tripartite to tritrophic interactions. European Journal of Plant Pathology 133, 3–23.Google Scholar
Jiu, M., Zhou, X., Tong, L., Xu, J., Yang, X., Wan, F. & Liu, S. (2007) Vector–virus mutualism accelerates population increase of an invasive whitefly. Plos ONE 2, e182.Google Scholar
Kennedy, J.S. (1951) Benefits to aphids from feeding on galled and virus-infected leaves. Nature 168, 825–826.Google Scholar
Kennedy, J.S., Day, M.F. & Eastop, V.F. (1962) A Conspectus of Aphids as Vectors of Plant Viruses. London, UK, The Eastern Press Ltd.Google Scholar
Korie, S., Clark, S.J., Perry, J.N., Mugglestone, M.A., Barlett, P.W., Marshall, E.J.P. & Mann, J.A. (1998) Analyzing maps of dispersal around a single focus. Environmental and Ecological Statistics 5, 317–344.CrossRefGoogle Scholar
Labonne, G., Quiot, J.B. & Monestiez, P. (1982) Contribution of different aphid species to the spread of cucumber mosaic virus (CMV) in a muskmelon plot. Agronomie 2, 797–804.Google Scholar
Legarrea, S., Velázquez, E., Aguado, P., Fereres, A., Morales, I., Rodríguez, D., Del Estal, P. & Viñuela, E. (2014) Effects of a UV-absorbing greenhouse net on the performance and host finding ability of Aphidius ervi in a lettuce crop. BioControl 59(3), 265–278.Google Scholar
Liu, T.X. & Chen, T.Y. (2001) Effects of three aphid species (Homoptera: Aphididae) on development, survival and predation of Chrysoperla carnea (Neuroptera: Chrysopidae). Applied Entomology and Zoology 36(3), 361–366.Google Scholar
Loebenstein, G. & Raccah, B. (1980) Control of non-persistently transmitted aphid-borne viruses. Phytoparasitica 8(3), 221–235.CrossRefGoogle Scholar
Lommen, S.T.E., Middendorp, C.W., Luijten, C.A., van Schelt, J., Brakefield, P.M. & de Jong, P.W. (2008) Natural flightless morphs of the ladybird beetle Adalia bipunctata improve biological control of aphids on single plants. Biological Control 47, 340–346.Google Scholar
Losey, J.E. & Denno, R.F. (1998) The escape response of pea aphids to foliar-foraging predators: factors affecting dropping behaviour. Ecological Entomology 23, 53–61.Google Scholar
Maris, P.C., Joosten, N.N., Goldbach, R.W. & Peters, D. (2004) Tomato spotted wilt virus infection improves host suitability for its vector Frankliniella occidentalis . Phytopathology 94, 706–711.Google Scholar
McKenzie, C.L., Shatters, R.G. Jr., Doostdar, H., Lee, S.D., Inbar, M. & Mayer, R.T. (2002) Effect of geminivirus infection and Bemisia infestation on accumulation of pathogenesis-related proteins in tomato. Archives of Insect Biochemistry and Physiology 49, 203–214.Google Scholar
Medina, P., Budia, F., Tirry, L., Smagghe, G., & Viñuela, E. (2001) Compatibility of spinosad, tebufenozide and azadirachtin with eggs and pupae of the predator Chrysoperla carnea (Stephens) under laboratory conditions. Biocontrol Science and Technology 11(5), 597–610.Google Scholar
Medina, P., Budia, F., Del Estal, P. & Viñuela, E. (2003). Effects of three modern insecticides: pyriproxifen, spinosad and tebufenozide on survival and reproduction of Chrysoperla carnea adults. Annals of Applied Biology 142, 55–61.Google Scholar
Moreno, A., Tjallingii, F., Fernández-Mata, G. & Fereres, A. (2012) Differences in the mechanism of inoculation between a semi-persistent and a non-persistent aphid-transmitted plant virus. Journal of General Virology 93, 662–667.Google Scholar
Nelson, E.H. & Rosenheim, J.A. (2006) Encounters between aphids and their predators: the relative frequencies of disturbance and consumption. Entomologia Experimentalis et Applicata 118, 211–219.Google Scholar
Ng, J.C.K. & Falk, B.W. (2006) Virus-vector interactions mediating nonpersistent and semipersistent transmission of plant viruses. Annual Review of Phytopathology 44, 183–212.CrossRefGoogle ScholarPubMed
Ng, J.C.K. & Perry, K.L. (2004) Transmission of plant viruses by aphid vectors. Molecular Plant Pathology 5, 505–511.Google Scholar
Omkar, & Pervez, A. (2005). Ecology of two-spotted ladybird, Adalia bipunctata: a review. Journal of Applied Entomology 129(9–10), 465–474.Google Scholar
Palukaitis, P. & García-Arenal, F. (2003) Cucumoviruses. Advances in Virus Research 62, 241–323.Google Scholar
Perry, J.N. (1995) Spatial analysis by distance indices. Journal of Animal Ecology 64, 303–314.CrossRefGoogle Scholar
Perry, J.N. (1998) Measures of spatial pattern for counts. Ecology 79, 1008–1017.Google Scholar
Perry, J.N. & Nixon, P. (2002) A new method to measure spatial association for ecological data. Ecoscience 9, 133–141.Google Scholar
Perry, J.N., Winder, L., Holland, J.M. & Alston, R.D. (1999) Red-blue plots for detecting clusters in count data. Ecological Letters 2, 106–113.Google Scholar
Pirone, T.P. & Perry, K.L. (2002) Aphids-nonpersistent transmission. Advances in Botanical Research 36, 1–19.Google Scholar
Raccah, B. (1986) Nonpersistent viruses: epidemiology and control. pp. 387–429 in Maramorosch, K. (Ed.) Advances in Virus Research, vol. 31. New York, USA, Academic Press.Google Scholar
Robledo Camacho, A., van der Blom, J., Sánchez Martínez, J.A. & Torres Jiménez, S. (2009) Control Biológico En Invernaderos Hortícolas. Almería, Spain, Coexphal.Google Scholar
Roitberg, B.D. & Myers, J.H. (1978) Effect of adult Coccinellidae on the spread of a plant virus by an aphid. Journal of Applied Ecology 15, 775–779.Google Scholar
Scholthof, K.B.G., Adkins, S., Czosnek, H., Palukaitis, P., Jacquot, E., Hohn, T., Hohn, B., Saunders, K., Candresse, T., Ahlquist, P., Hemenway, C. & Foster, G.D. (2011) Top 10 plant viruses in molecular plant pathology. Molecular Plant Pathology 12, 938–954.Google Scholar
Smyrnioudis, I.N., Harrington, R., Clark, S.J. & Katis, N. (2001) The effect of natural enemies on the spread of barley yellow dwarf virus (BYDV) by Rhopalosiphum padi (Hemiptera: Aphididae). Bulletin of Entomological Research 91, 301–306.Google Scholar
Statistical Graphics Corp. (1994–2000) Statgraphics Plus 5.1. Enterprise edition. Rockville, MD, USA.Google Scholar
Tamaki, G., Halfhill, J.E. & Hathaway, D.D. (1970) Dispersal and reduction of Acyrthosiphon pisum (Harris) by Aphidius smithii . Annals of the Entomological Society of America 63, 973–980.Google Scholar
Thackray, D.J., Jones, R.A.C., Bwye, A.M. & Coutts, B.A. (2000) Further studies on the effects of insecticides on aphid vector numbers and spread of cucumber mosaic virus in narrow-leafed lupins (Lupinus angustifolius). Crop Protection 19, 121–139.CrossRefGoogle Scholar
Van Steenis, M.J. (1992) Biological control of the cotton aphid Aphis gossypii Glover (Hom., Aphididae): pre-introduction evaluation of natural enemies. Journal of Applied Entomology 114, 362–380.Google Scholar
Viñuela, E., Händel, U. & Vogt, H. (1996) Evaluación en campo de los efectos secundarios de dos plaguicidas de origen botánico, una piretrina natural y un extracto de neem, sobre Chrysoperla carnea . Boletín Sanidad Vegetal Plagas 22(1), 97–106.Google Scholar
Vogt, H., Bigler, F., Brown, K., Candolfi, M.P., Kemmeter, F., Kühner, C., Moll, M., Travis, A., Ufer, A., Viñuela, E., Waldburger, M. & Waltersdorfer, A. (2000) Laboratory method to test effects of plant protection products on larvae of Chrysoperla carnea (Neuroptera: Chrysopidae). pp. 107–119 in Candolfi, M.P., Blümel, S., Forster, R., Bakker, F.M., Grimm, C., Hassan, S.A., Heimbach, U., Mead-Briggs, M.A., Reber, B., Schmuck, R. & Vogt, H. (Eds) Guidelines to Evaluate Side-Effects of Plant Protection Products to Non-Target Arthropods. Reinheim, Germany, IOBC/WPRS Publication.Google Scholar
Yano, E. (2006) Ecological considerations for biological control of aphids in protected culture. Population Ecology 48, 333–339.Google Scholar