Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-11T13:43:51.907Z Has data issue: false hasContentIssue false
  • English
  • Français

Early-season predation on aphids by winter-active spiders in apple orchards revealed by diagnostic PCR

Published online by Cambridge University Press:  02 November 2012

C. Boreau de Roincé ,
C. Lavigne ,
J.-F. Mandrin ,
C. Rollard  and
W.O.C. Symondson
C. Boreau de Roincé
Affiliation:
Centre Technique Interprofessionnel des Fruits et Légumes, Centre de Balandran, BP 32, 30127 Bellegarde, France INRA, UR 1115, Plantes et Systèmes de culture Horticoles, F-84000, Avignon, France Cardiff School of Biosciences, Cardiff University, Sir Martin Evans Building, Museum Avenue, Cardiff CF10 3AX, UK
C. Lavigne
Affiliation:
INRA, UR 1115, Plantes et Systèmes de culture Horticoles, F-84000, Avignon, France
J.-F. Mandrin
Affiliation:
Centre Technique Interprofessionnel des Fruits et Légumes, Centre de Balandran, BP 32, 30127 Bellegarde, France
C. Rollard
Affiliation:
Muséum national d'Histoire naturelle, Département Systématique & Evolution, USM OSEB, 61 rue Buffon, CP 53, 75005 Paris, France
W.O.C. Symondson*
Affiliation:
Cardiff School of Biosciences, Cardiff University, Sir Martin Evans Building, Museum Avenue, Cardiff CF10 3AX, UK
*
*Author for correspondence Fax: +44 (0)29 208 74116 E-mail: Symondson@cardiff.ac.uk
Get access Rights & Permissions [Opens in a new window]

Abstract

Aphids are major pests in apple orchards, debilitating the crop and spreading disease. We investigated whether early-season predation by canopy spiders may be effectively controlling aphid numbers in three organic orchards. For this purpose, we monitored the aphid population dynamics from the winter eggs to colony stages and compared this to spider abundances and rates of predation on aphids detected by diagnostic polymerase chain reaction. For the latter, we applied existing general aphid primers. We found that spiders ate colony fundatrices and that aphid numbers were negatively related to spider abundance. Spiders were the main active predators within the orchards when the first colony fundatrices were present, indicating their importance in the early control of aphid populations.

Keywords

Aphis pomiconservation biological controldiagnostic PCRDysaphis plantagineageneralist predatorgut content analysis
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 103 , Issue 2 , April 2013 , pp. 148 - 154
Copyright
Copyright © Cambridge University Press 2012

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., Shayler, S.P., Harwood, J.D., Vaughan, I.P., Sunderland, K.D. & Symondson, W.O.C. (2003) Collembola as alternative prey sustaining spiders in arable ecosystems: prey detection within predators using molecular markers. Molecular Ecology 12, 3467–3475.Google Scholar
Birkhofer, K., Gavish-Regev, E., Endlweber, K., Lubin, Y.D., von Berg, K., Wise, D.H. & Scheu, S. (2008) Cursorial spiders retard initial aphid population growth at low densities in winter wheat. Bulletin of Entomological Research 98, 249–255.CrossRefGoogle ScholarPubMed
Blommers, L.H.M., Helsen, H.H.M. & Vaal, F. (2004) Life history data of the rosy apple aphid Dysaphis plantaginea (Pass.) (Homopt., Aphididae) on plantain and as migrant to apple. Journal of Pest Science 77, 155–163.Google Scholar
Bonnemaison, L. (1959) Le puceron cendré du pommier (Dysaphis plantaginea Pass.) Morphologie et biologie – Méthodes de lutte. Annales INRA, Série C Epiphyties III, 257–322.Google Scholar
Brown, M.W. (2004) Role of aphid predator guild in controlling spirea aphid populations on apple in West Virginia, USA. Biological Control 29, 189–198.Google Scholar
Brown, M.W. (2011) Importance of early arrival of adult Harmonia axyridis for control of Aphis spiraecola on apple. Biocontrol 56, 65–69.Google Scholar
Carroll, D.P. & Hoyt, S.C. (1984) Natural enemies and their effect on apple aphid, Aphis pomi Degeer (Homoptera, Aphididae), colonies on young apple trees in central Washington. Environmental Entomology 13, 469–481.Google Scholar
Chang, G.C. & Kareiva, P. (1999) The case for indigenous generalists in biological control. pp. 103–115in Hawkins, B. & Cornell, H. (Eds) Theoretical Approaches to Biological Control. Cambridge, UK, Cambridge University Press.CrossRefGoogle Scholar
Chen, Y., Giles, K.L., Payton, M.E. & Greenstone, M.H. (2000) Identifying key cereal aphid predators by molecular gut analysis. Molecular Ecology 9, 1887–1898.Google Scholar
Chiverton, P.A. (1986) Predator density manipulation and its effects on populations of Rhopalosiphum padi (Hom, Aphididae) in spring barley. Annals of Applied Biology 109, 49–60.Google Scholar
Deberardinis, E., Baronio, P. & Baumgartner, J. (1994) The effect of aphid (Dysaphis plantaginea Pass, Hom, Aphididae) feeding on apple fruit growth. Ecological Modelling 72, 115–127.Google Scholar
Dib, H., Simon, S., Sauphanor, B. & Capowiez, Y. (2010) The role of natural enemies on the population dynamics of the rosy apple aphid, Dysaphis plantaginea Passerini (Hemiptera: Aphididae) in organic apple orchards in south-eastern France. Biological Control 55, 97–109.Google Scholar
Finke, D.L. & Snyder, W.E. (2010) Conserving the benefits of predator biodiversity. Biological Conservation 143, 2260–2269.Google Scholar
Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google Scholar
Fréchette, B., Cormier, D., Chouinard, G., Vanoosthuyse, F. & Lucas, E. (2008) Apple aphid, Aphis spp. (Hemiptera: Aphididae), and predator populations in an apple orchard at the non-bearing stage: The impact of ground cover and cultivar. European Journal of Entomology 105, 521–529.Google Scholar
Graf, B., Baumgärtner, J. & Delucchi, V. (1985) Life table statistics of three apple aphids, Dysaphis plantaginea, Rhopalosiphum insertum, and Aphis pomi (Homoptera, Aphididae), at constant temperatures. Zeitschrift für Angewandte Entomologie 99, 285–294.CrossRefGoogle Scholar
Greenstone, M.H. (1999) Spider predation: How and why we study it. Journal of Arachnology 27, 333–342.Google Scholar
Hart, A.J., Bale, J.S. & Fenlon, J.S. (1997) Developmental threshold, day-degree requirements and voltinism of the aphid predator Episyrphus balteatus (Diptera: Syrphidae). Annals of Applied Biology 130, 427–437.Google Scholar
Harwood, J.D. & Obrycki, J.J. (2005) Quantifying aphid predation rates of generalist predators in the field. European Journal of Entomology 102, 335–350.Google Scholar
Helsen, M., Vaal, F. & Blommers, L. (1998) Phenology of the common earwig Forficula auricularia L. (Dermaptera: Forficulidae) in an apple orchard. International Journal of Pest Management 44, 75–79.Google Scholar
Hodge, M.A. (1999) The implications of intraguild predation for the role of spiders in biological control. Journal of Arachnology 27, 351–362.Google Scholar
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.Google Scholar
Korenko, S. & Pekar, S. (2010) Is there intraguild predation between winter-active spiders (Araneae) on apple tree bark? Biological Control 54, 206–212.CrossRefGoogle Scholar
Korenko, S., Pekar, S. & Honek, A. (2010) Predation activity of two winter-active spiders (Araneae: Anyphaenidae, Philodromidae). Journal of Thermal Biology 35, 112–116.Google Scholar
Kuusk, A.K., Cassel-Lundhagen, A., Kvarnheden, A. & Ekbom, B. (2008) Tracking aphid predation by lycosid spiders in spring-sown cereals using PCR-based gut-content analysis. Basic and Applied Ecology 9, 718–725.Google Scholar
Marc, P. & Canard, A. (1997) Maintaining spider biodiversity in agroecosystems as a tool in pest control. Agriculture Ecosystems & Environment 62, 229–235.Google Scholar
Marc, P., Canard, A. & Ysnel, F. (1999) Spiders (Araneae) useful for pest limitation and bioindication. Agriculture Ecosystems & Environment 74, 229–273.Google Scholar
Miliczky, E.R., Horton, D.R. & Calkins, C.O. (2008) Observations on phenology and overwintering of spiders associated with apple and pear orchards in south-central Washington. Journal of Arachnology 36, 565–573.CrossRefGoogle Scholar
Minarro, M., Hemptinne, J.L. & Dapena, E. (2005) Colonization of apple orchards by predators of Dysaphis plantaginea: sequential arrival, response to prey abundance and consequences for biological control. Biocontrol 50, 403–414.CrossRefGoogle Scholar
Mizell, R.F. & Schiffhauer, D.E. (1987) Trunk traps and overwintering predators in pecan orchards: survey of species and emergence times. Florida Entomologist 70, 238–244.Google Scholar
Morse, J.G. & Croft, B.A. (1987) Biological control of Aphis pomi Hom, Aphididae of Aphidoletes aphidimyza Dip, Cecidomyiidae: a predator-prey model. Entomophaga 32, 339–356.Google Scholar
Mueller, T.F., Blommers, L.H.M. & Mols, P.J.M. (1988) Earwig (Forficula auricularia) predation on the woolly apple aphid, Eriosoma lanigerum. Entomologia Experimentalis et Applicata 47, 145–152.Google Scholar
Murdoch, W.W., Chesson, J. & Chesson, P.L. (1985) Biological control in theory and practice. American Naturalist 125, 344–366.Google Scholar
Obrycki, J.J. & Tauber, M.J. (1981) Phenology of three coccinellid species thermal requirements for development. Annals of the Entomological Society of America 74, 31–36.Google Scholar
Pekar, S. & Kocourek, F. (2004) Spiders (Araneae) in the biological and integrated pest management of apple in the Czech Republic. Journal of Applied Entomology 128, 561–566.CrossRefGoogle Scholar
Qubbaj, T., Reineke, A. & Zebitz, C.P.W. (2005) Molecular interactions between rosy apple aphids, Dysaphis plantaginea, and resistant and susceptible cultivars of its primary host Malus domestica. Entomologia Experimentalis et Applicata 115, 145–152.Google Scholar
R Development Core Team (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available online at http://www.R-project.org (accessed 20 September 2012).Google Scholar
Riechert, S.E. & Lockley, T. (1984) Spiders as biological control agents. Annual Review of Entomology 29, 299–320.Google Scholar
Simon, S., Bouvier, J.C., Debras, J.F. & Sauphanor, B. (2009) Biodiversity and pest management in orchard systems. A review. Agronomy for Sustainable Development 30, 139–152.Google Scholar
Symondson, W.O.C. (2002) Molecular identification of prey in predator diets. Molecular Ecology 11, 627–641.Google Scholar
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.Google Scholar
Wise, D.H. (2006) Cannibalism, food limitation, intraspecific competition and the regulation of spider populations. Annual Review of Entomology 51, 441–465.Google Scholar
Wyss, E., Niggli, U. & Nentwig, W. (1995) The impacts of spiders on aphid populations in a strip-managed apple orchard. Journal of Applied Entomology-Zeitschrift Fur Angewandte Entomologie 119, 473–478.Google Scholar
Wyss, E., Villiger, M., Hemptinne, J.L. & Muller-Scharer, H. (1999) Effects of augmentative releases of eggs and larvae of the ladybird beetle, Adalia bipunctata, on the abundance of the rosy apple aphid, Dysaphis plantaginea, in organic apple orchards. Entomologia Experimentalis et Applicata 90, 167–173.Google Scholar