Advertisement

Journal of Pest Science

, Volume 90, Issue 2, pp 447–457 | Cite as

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

  • Aude Gilabert
  • Bertrand Gauffre
  • Nicolas Parisey
  • Jean-François Le Gallic
  • Patrick Lhomme
  • Vincent Bretagnolle
  • Charles-Antoine Dedryver
  • Jacques Baudry
  • Manuel Plantegenest
Original Paper

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.

Keywords

Landscape ecology Crop colonization Rhopalosiphum padi Isotopic analyses Barley yellow dwarf virus 

Notes

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.

Compliance with ethical standards

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.

References

  1. 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 CrossRefGoogle Scholar
  2. 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 CrossRefGoogle Scholar
  3. 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 CrossRefGoogle Scholar
  4. 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 CrossRefGoogle Scholar
  5. 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 CrossRefGoogle Scholar
  6. 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 CrossRefGoogle Scholar
  7. Bonnieux F, Rainelli P, Vermersch D (1998) Estimating the supply of environmental benefits by agriculture: a French case study. Environ Resour Econ 11:135–153CrossRefGoogle Scholar
  8. 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 CrossRefPubMedGoogle Scholar
  9. 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 14:922–932CrossRefPubMedGoogle Scholar
  10. 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 CrossRefGoogle Scholar
  11. 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 155–170Google Scholar
  12. 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 CrossRefPubMedGoogle Scholar
  13. Donald PF, Green RE, Heath MF (2001) Agricultural intensification and the collapse of Europe’s farmland bird populations. Proc R Soc B Biol Sci 268:25–29CrossRefGoogle Scholar
  14. 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 CrossRefGoogle Scholar
  15. 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 CrossRefPubMedGoogle Scholar
  16. 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 93:1217–1222CrossRefPubMedGoogle Scholar
  17. 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 106:49–55CrossRefGoogle Scholar
  18. 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 CrossRefGoogle Scholar
  19. Geiger F et al (2010) Persistent negative effects of pesticides on biodiversity and biological control potential on European farmland. Basic Appl Ecol 11:97–105CrossRefGoogle Scholar
  20. 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 CrossRefGoogle Scholar
  21. Hadfield JD (2010) MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R Package. J Stat Softw 33:1–22CrossRefGoogle Scholar
  22. 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 CrossRefPubMedGoogle Scholar
  23. 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 64:667–676CrossRefGoogle Scholar
  24. 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 CrossRefGoogle Scholar
  25. 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 153–186CrossRefGoogle Scholar
  26. Krebs JR, Wilson JD, Bradbury RB, Siriwardena GM (1999) The second silent spring? Nature 400:611–612CrossRefGoogle Scholar
  27. 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 79:345–360CrossRefGoogle Scholar
  28. 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 126:75–90CrossRefGoogle Scholar
  29. 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 90:860–866CrossRefPubMedGoogle Scholar
  30. 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 78:241–249CrossRefGoogle Scholar
  31. 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 CrossRefPubMedGoogle Scholar
  32. 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 CrossRefGoogle Scholar
  33. 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 CrossRefGoogle Scholar
  34. Mole S, Joern A, Oleary MH, Madhavan S (1994) Spatial and temporal variation in carbon isotope discrimination in prairie graminoids. Oecologia 97:316–321CrossRefGoogle Scholar
  35. 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 CrossRefGoogle Scholar
  36. 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 CrossRefPubMedGoogle Scholar
  37. Osborne CP et al (2014) A global database of C4 photosynthesis in grasses. New Phytol 204:441–446. doi: 10.1111/nph.12942 CrossRefPubMedGoogle Scholar
  38. 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 313–320Google Scholar
  39. Parry H (2013) Cereal aphid movement: general principles and simulation modelling. Mov Ecol 1:14CrossRefPubMedPubMedCentralGoogle Scholar
  40. 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 CrossRefGoogle Scholar
  41. Plumb RT (1990) The epidemiology of barley yellow dwarf in Europe. In: Burnett PA (ed) World perspectives on barley yellow dwarf. CIMMYT, Mexico, pp 215–227Google Scholar
  42. 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 24:337–349CrossRefGoogle Scholar
  43. 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 108:218–227CrossRefGoogle Scholar
  44. 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 CrossRefGoogle Scholar
  45. Stoate C, Boatman ND, Borralho RJ, Carvalho CR, de Snoo GR, Eden P (2001) Ecological impacts of arable intensification in Europe. J Environ Manag 63:337–365CrossRefGoogle Scholar
  46. Thies C, Roschewitz I, Tscharntke T (2005) The landscape context of cereal aphid-parasitoid interactions. Proc R Soc B Biol Sci 272:203–210CrossRefGoogle Scholar
  47. 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 45:238–253CrossRefGoogle Scholar
  48. 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 CrossRefGoogle Scholar
  49. 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 CrossRefPubMedGoogle Scholar
  50. 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 9:337–346CrossRefGoogle Scholar
  51. 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 CrossRefGoogle Scholar
  52. 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 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Aude Gilabert
    • 1
    • 5
  • Bertrand Gauffre
    • 2
    • 3
  • Nicolas Parisey
    • 1
  • Jean-François Le Gallic
    • 1
  • Patrick Lhomme
    • 1
    • 6
  • Vincent Bretagnolle
    • 2
  • Charles-Antoine Dedryver
    • 1
  • Jacques Baudry
    • 4
  • Manuel Plantegenest
    • 1
  1. 1.Institut de Génétique Environnement et Protection des Plantes (IGEPP)UMR 1349 INRA, Agrocampus Ouest and Université de Rennes 1Le RheuFrance
  2. 2.Centre d’Etudes Biologiques de Chizé (CEBC)UMR 7372 CNRS and Université de La RochelleBeauvoir-sur-NiortFrance
  3. 3.USC1339 CEBCINRABeauvoir-sur-NiortFrance
  4. 4.UR0980 SAD-PaysageINRARennesFrance
  5. 5.MIVEGEC (UMR CNRS/IRD/UM 5290)CHRU de MontpellierMontpellierFrance
  6. 6.Department of BiologyPennsylvania State UniversityUniversity ParkUSA

Personalised recommendations