Skip to main content
Log in

Influence of the surrounding landscape on the colonization rate of cereal aphids and phytovirus transmission in autumn

  • Original Paper
  • Published:
Journal of Pest Science Aims and scope Submit manuscript

Abstract

Ecological control has often focused on factors enhancing control of pests by their natural enemies, while factors reducing the colonization rate of crops by pests have been comparatively neglected. We present an approach to assess landscape influence on the intensity of wheat colonization by a major crop pest, the aphid Rhopalosiphum padi. We used trays containing wheat seedlings to monitor field colonization by R. padi and barley yellow dwarf viruses’ transmission in two areas in France in autumn. We assessed the influence of landscape components likely affecting aphid colonization, i.e. maize and grasslands as source of migrants on the number of aphids landing per tray, as well as the host plant of origin and the viruliferous potential of migrants. During the survey, maize was the main source of migrants. Virus transmission was detected in a few cases (4 % positive assays). Colonization was increased by the presence of maize, but reduced by the presence of grasslands at the landscape scale considered here (i.e. at a radius of 1000 m). Our study contributes to a better understanding of disease dynamics in agricultural landscapes. By identifying features of the landscape that surrounds fields and affects these dynamics, growers can develop more efficient crop protection strategies relying on habitat manipulation and rational use of pesticides.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Barro PJD, Wallwork H (1992) The role of annual grasses in the phenology of Rhopalosiphum padi in the low rainfall belt of South Australia. Ann Appl Biol 121:455–467. doi:10.1111/j.1744-7348.1992.tb03456.x

    Article  Google Scholar 

  • Bianchi FJJA, Booij CJH, Tscharntke T (2006) Sustainable pest regulation in agricultural landscapes: a review on landscape composition, biodiversity and natural pest control. Proc R Soc B Biol Sci 273:1715–1727. doi:10.1098/rspb.2006.3530

    Article  CAS  Google Scholar 

  • Birch ANE, Begg GS, Squire GR (2011) How agro-ecological research helps to address food security issues under new IPM and pesticide reduction policies for global crop production systems. J Exp Bot 62:3251–3261. doi:10.1093/jxb/err064

    Article  CAS  Google Scholar 

  • Birkhofer K, Arvidsson F, Ehlers D, Mader VL, Bengtsson J, Smith HG (2016) Organic farming affects the biological control of hemipteran pests and yields in spring barley independent of landscape complexity. Landsc Ecol 31:567–579. doi:10.1007/s10980-015-0263-8

    Article  Google Scholar 

  • Boecklen WJ, Yarnes CT, Cook BA, James AC (2011) On the use of stable isotopes in trophic ecology. Annu Rev Ecol Evol Syst 42:411–440. doi:10.1146/annurev-ecolsys-102209-144726

    Article  Google Scholar 

  • Bommarco R, Wetterlind S, Sigvald R (2007) Cereal aphid populations in non-crop habitats show strong density dependence. J Appl Ecol 44:1013–1022. doi:10.1046/j.0021-8901.2007.01332.x

    Article  Google Scholar 

  • Bonnieux F, Rainelli P, Vermersch D (1998) Estimating the supply of environmental benefits by agriculture: a French case study. Environ Resour Econ 11:135–153

    Article  Google Scholar 

  • Carrière Y et al (2014) Assessing transmission of crop diseases by insect vectors in a landscape context. J Econ Entomol 107:1–10. doi:10.1603/ec13362

    Article  PubMed  Google Scholar 

  • Chaplin-Kramer R, O’Rourke ME, Blitzer EJ, Kremen C (2011) A meta-analysis of crop pest and natural enemy response to landscape complexity. Ecol Lett 14:922–932

    Article  PubMed  Google Scholar 

  • Collin J, St-Pierre CA, Comeau A, Couture L (1997) Effects of barley yellow dwarf viruses and snow molds on yield stability of winter cereals. Can J Plant Pathol 19:406–413. doi:10.1080/07060669709501068

    Article  Google Scholar 

  • Dedryver CA, Harrington R (2004) Epidemiology and forecasting of small grain viruses of the Luteoviridae family. In: Lapierre H, Signoret P (eds) Viruses and virus diseases of Poaceae (Gramineae). INRA edn. Institut National de la Recherche Agronomique (INRA), Versailles, pp 155–170

    Google Scholar 

  • Delmotte F, Leterme N, Gauthier JP, Rispe C, Simon JC (2002) Genetic architecture of sexual and asexual populations of the aphid Rhopalosiphum padi based on allozyme and microsatellite markers. Mol Ecol 11:711–723. doi:10.1046/j.1365-294X.2002.01478.x

    Article  CAS  PubMed  Google Scholar 

  • Donald PF, Green RE, Heath MF (2001) Agricultural intensification and the collapse of Europe’s farmland bird populations. Proc R Soc B Biol Sci 268:25–29

    Article  Google Scholar 

  • Dormann CF et al (2013) Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36:27–46. doi:10.1111/j.1600-0587.2012.07348.x

    Article  Google Scholar 

  • Edwards EJ, Osborne CP, Strömberg CAE, Smith SA, Consortium CG (2010) The origins of C4 grasslands: integrating evolutionary and ecosystem science. Science 328:587–591. doi:10.1126/science.1177216

    Article  CAS  PubMed  Google Scholar 

  • Fabre F, Dedryver CA, Leterrier JL, Plantegenest M (2003) Aphid abundance on cereals in autumn predicts yield losses caused by barley yellow dwarf virus. Phytopathology 93:1217–1222

    Article  CAS  PubMed  Google Scholar 

  • Fabre F, Plantegenest M, Mieuzet L, Dedryver CA, Leterrier JL, Jacquot E (2005) Effects of climate and land use on the occurrence of viruliferous aphids and the epidemiology of barley yellow dwarf disease. Agric Ecosyst Environ 106:49–55

    Article  Google Scholar 

  • Favret C, Voegtlin DJ (2001) Migratory aphid (Hemiptera: Aphididae) habitat selection in agricultural and adjacent natural habitats. Environ Entomol 30:371–379. doi:10.1603/0046-225x-30.2.371

    Article  Google Scholar 

  • Geiger F et al (2010) Persistent negative effects of pesticides on biodiversity and biological control potential on European farmland. Basic Appl Ecol 11:97–105

    Article  CAS  Google Scholar 

  • Gilabert A, Simon J-C, Dedryver C-A, Plantegenest M (2014) Do ecological niches differ between sexual and asexual lineages of an aphid species? Evol Ecol 28:1095–1104. doi:10.1007/s10682-014-9730-y

    Article  Google Scholar 

  • Hadfield JD (2010) MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R Package. J Stat Softw 33:1–22

    Article  Google Scholar 

  • Hadfield JD, Nakagawa S (2010) General quantitative genetic methods for comparative biology: phylogenies, taxonomies and multi-trait models for continuous and categorical characters. J Evol Biol 23:494–508. doi:10.1111/j.1420-9101.2009.01915.x

    Article  CAS  PubMed  Google Scholar 

  • Hammond J, Lister RM, Foster JE (1983) Purification, identity and some properties of an isolate of barley yellow dwarf virus from Indiana. J Gen Virol 64:667–676

    Article  Google Scholar 

  • Hulle M, Coquio S, Laperche V (1994) Patterns in flight phenology of a migrant cereal aphid species. J Appl Ecol 31:49–58. doi:10.2307/2404598

    Article  Google Scholar 

  • Irwin ME, Kampmeier GE, Weisser WW (2007) Aphid movement: process and consequences. In: van Emden HF, Harrington R (eds) Aphids as crop pests. CABI, Wallingford, pp 153–186

    Chapter  Google Scholar 

  • Krebs JR, Wilson JD, Bradbury RB, Siriwardena GM (1999) The second silent spring? Nature 400:611–612

    Article  CAS  Google Scholar 

  • Leather SR, Walters KFA, Dixon AFG (1989) Factors determining the pest status of the bird cherry-oat aphid, Rhopalosiphum padi (L) (Hemiptera, Aphididae), in Europe—a study and review. Bull Entomol Res 79:345–360

    Article  Google Scholar 

  • Leclercq-Le Quillec F, Tanguy S, Dedryver C-A (1995) Aerial flow of barley yellow dwarf viruses and of their vectors in western France. Ann Appl Biol 126:75–90

    Article  Google Scholar 

  • Leclercq-Le Quillec F, Plantegenest M, Riault G, Dedryver C-A (2000) Analyzing and modeling temporal disease progress of barley yellow dwarf virus serotypes in barley fields. Phytopathology 90:860–866

    Article  CAS  PubMed  Google Scholar 

  • Loxdale HD, Brookes CP (1988) Electrophoretic study of enzymes from cereal aphid populations. V: spatial and temporal genetic similarity of holocyclic populations of the bird-cherry oat aphid, Rhopalosiphum padi (L.) (Hemiptera: Aphididae), in Britain. Bull Entomol Res 78:241–249

    Article  CAS  Google Scholar 

  • Martin AE, Fahrig L (2012) Measuring and selecting scales of effect for landscape predictors in species–habitat models. Ecol Appl 22:2277–2292. doi:10.1890/11-2224.1

    Article  PubMed  Google Scholar 

  • Maudsley MJ, Mackenzie A, Thacker JI, Dixon AFG (1996) Density dependence in cereal aphid populations. Ann Appl Biol 128:453–463. doi:10.1111/j.1744-7348.1996.tb07106.x

    Article  Google Scholar 

  • Menalled FD, Costamagna AC, Marino PC, Landis DA (2003) Temporal variation in the response of parasitoids to agricultural landscape structure. Agric Ecosyst Environ 96:29–35. doi:10.1016/S0167-8809(03)00018-5

    Article  Google Scholar 

  • Mole S, Joern A, Oleary MH, Madhavan S (1994) Spatial and temporal variation in carbon isotope discrimination in prairie graminoids. Oecologia 97:316–321

    Article  Google Scholar 

  • Nottingham SF, Hardie JIM, Tatchell GM (1991) Flight behaviour of the bird cherry aphid, Rhopalosiphum padi. Physiol Entomol 16:223–229. doi:10.1111/j.1365-3032.1991.tb00559.x

    Article  Google Scholar 

  • O’Rourke ME, Rienzo-Stack K, Alison GP (2011) A multi-scale, landscape approach to predicting insect populations in agroecosystems. Ecol Appl 21:1782–1791. doi:10.2307/23023117

    Article  PubMed  Google Scholar 

  • Osborne CP et al (2014) A global database of C4 photosynthesis in grasses. New Phytol 204:441–446. doi:10.1111/nph.12942

    Article  CAS  PubMed  Google Scholar 

  • Paliwal YC, Andrews CJ (1990) Barley yellow dwarf virus-host plant interactions affecting winter stress tolerance in cereals. In: Burnett PA (ed) World perspectives on barley yellow dwarf. CIMMYT*DCAS, International Maize and Wheat Improvement Center, Mexico, pp 313–320

    Google Scholar 

  • Parry H (2013) Cereal aphid movement: general principles and simulation modelling. Mov Ecol 1:14

    Article  PubMed  PubMed Central  Google Scholar 

  • Plećaš M et al (2014) Landscape composition and configuration influence cereal aphid–parasitoid–hyperparasitoid interactions and biological control differentially across years. Agric Ecosyst Environ 183:1–10. doi:10.1016/j.agee.2013.10.016

    Article  Google Scholar 

  • Plumb RT (1990) The epidemiology of barley yellow dwarf in Europe. In: Burnett PA (ed) World perspectives on barley yellow dwarf. CIMMYT, Mexico, pp 215–227

    Google Scholar 

  • Ricci B, Franck P, Toubon J-F, Bouvier J-C, Sauphanor B, Lavigne C (2009) The influence of landscape on insect pest dynamics: a case study in southeastern France. Landsc Ecol 24:337–349

    Article  Google Scholar 

  • Roschewitz I, Hucker M, Tscharntke T, Thies C (2005) The influence of landscape context and farming practices on parasitism of cereal aphids. Agric Ecosyst Environ 108:218–227

    Article  Google Scholar 

  • Still CJ, Berry JA, Collatz GJ, DeFries RS (2003) Global distribution of C3 and C4 vegetation: carbon cycle implications. Global Biogeochem Cycle 17:6-1–6-14. doi:10.1029/2001gb001807

    Article  Google Scholar 

  • Stoate C, Boatman ND, Borralho RJ, Carvalho CR, de Snoo GR, Eden P (2001) Ecological impacts of arable intensification in Europe. J Environ Manag 63:337–365

    Article  CAS  Google Scholar 

  • Thies C, Roschewitz I, Tscharntke T (2005) The landscape context of cereal aphid-parasitoid interactions. Proc R Soc B Biol Sci 272:203–210

    Article  Google Scholar 

  • Tscharntke T et al (2008) Reprint of “Conservation biological control and enemy diversity on a landscape scale” [Biol. Control 43 (2007) 294–309]. Biol Control 45:238–253

    Article  Google Scholar 

  • Veres A, Petit S, Conord C, Lavigne C (2013) Does landscape composition affect pest abundance and their control by natural enemies? A review. Agric Ecosyst Environ 166:110–117. doi:10.1016/j.agee.2011.05.027

    Article  Google Scholar 

  • Vialatte A, Simon J-C, Dedryver C-A, Fabre F, Plantegenest M (2006) Tracing individual movements of aphids reveals preferential routes of population transfers in agroecosystems. Ecol Appl 16:839–844. doi:10.2307/40061703

    Article  PubMed  Google Scholar 

  • Vialatte A, Plantegenest M, Simon J-C, Dedryver C-A (2007) Farm-scale assessment of movement patterns and colonization dynamics of the grain aphid in arable crops and hedgerows. Agric For Entomol 9:337–346

    Article  Google Scholar 

  • Wissinger SA (1997) Cyclic colonization in predictably ephemeral habitats: a template for biological control in annual crop systems. Biol Control 10:4–15. doi:10.1006/bcon.1997.0543

    Article  Google Scholar 

  • Zhao Z-H, Hui C, Hardev S, Ouyang F, Dong Z, Ge F (2014) Responses of cereal aphids and their parasitic wasps to landscape complexity. J Econ Entomol 107:630–637. doi:10.1603/ec13054

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank A. Whibley, J. Wintersinger and J. Foucaud for helpful comments on the manuscript. We thank the farmers from ARM and PVS who allowed us to work in their fields. We also acknowledge V. Turpaud Fizzala and I. Badenhausser for their assistance in PVS, L. Mieuzet for help during ELISA tests and J. Bonhomme for helpful advice on the study design. We thank C. Scrimgeour, L. Hunter, H. Kemp and W. Meier-Augenstein for performing isotopic analyses at the Mylnefield Research Services, Scotland, UK. “ANR Landscaphid” (ANR-09-STRA-05) and “ANR Biodivagrim” are also acknowledged. Landscape mapping in both ARM and PVS is supported by the Zone Atelier program and the Institut National de l’Ecologie et de l’Environnement. This research was supported by Bayer CropScience France and a C.I.F.R.E. grant from the Association Nationale de la Recherche Technique.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Manuel Plantegenest.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national and/or institutional guidelines for the care and use of animals were followed.

Additional information

Communicated by M. Jonsson.

Jacques Baudry and Manuel Plantegenest have contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gilabert, A., Gauffre, B., Parisey, N. et al. Influence of the surrounding landscape on the colonization rate of cereal aphids and phytovirus transmission in autumn. J Pest Sci 90, 447–457 (2017). https://doi.org/10.1007/s10340-016-0790-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10340-016-0790-3

Keywords

Navigation