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.
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Hadfield JD (2010) MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R Package. J Stat Softw 33:1–22
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
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
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
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
Krebs JR, Wilson JD, Bradbury RB, Siriwardena GM (1999) The second silent spring? Nature 400:611–612
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
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
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
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
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
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
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
Mole S, Joern A, Oleary MH, Madhavan S (1994) Spatial and temporal variation in carbon isotope discrimination in prairie graminoids. Oecologia 97:316–321
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
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
Osborne CP et al (2014) A global database of C4 photosynthesis in grasses. New Phytol 204:441–446. doi:10.1111/nph.12942
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
Parry H (2013) Cereal aphid movement: general principles and simulation modelling. Mov Ecol 1:14
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
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
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
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
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
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
Thies C, Roschewitz I, Tscharntke T (2005) The landscape context of cereal aphid-parasitoid interactions. Proc R Soc B Biol Sci 272:203–210
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
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
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
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
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
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
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
Corresponding author
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
About this article
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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10340-016-0790-3