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Arthropod-Plant Interactions

, Volume 7, Issue 3, pp 249–258 | Cite as

Red oilseed rape? The potential for manipulation of petal colour in control strategies for the pollen beetle (Meligethes aeneus)

  • Samantha M. CookEmail author
  • Matthew P. Skellern
  • Thomas F. Döring
  • John A. Pickett
Original Paper

Abstract

The pollen beetle (Meligethes aeneus) is a major pest of oilseed rape (Brassica napus) at the inflorescence stage and is well known to prefer colours called yellow by human observers over many other colours. While commercial cultivars of oilseed rape have yellow flowers, little is known about the potential to manipulate host plant location and reduce subsequent infestation by this pest through variation in flower colour. We investigated the responses of pollen beetles to flowers of a white-petalled oilseed rape variety that had been dyed different colours in semi-field arena and field experiments. Flowers dyed blue or red were less heavily infested than those dyed yellow or the white flowers, indicating that blue and red flowers were less attractive than yellow and white ones. This response was most likely due to differences in petal colour because olfactometer studies showed that beetle responses to the odours of the coloured treatments did not differ. The comparatively high infestation of untreated white flowers is interpreted as a consequence of their high UV reflectance; the presence of a UV receptor in M. aeneus is suggested, and its role in visually guided insect–plant interactions in this species described. The potential for manipulation of petal colour in control strategies for the pollen beetle is discussed.

Keywords

Brassica napus Colour Flower Host plant Integrated pest management Push–pull Trap crop Visual cues 

Notes

Acknowledgments

We are very grateful to Rosemary Collier and Graham Teakle at The University of Warwick Crop Centre for early discussions on this work, Darren Murray at VSNi for statistical advice, Christine Trittermann for technical assistance, Ingrid Williams for her support throughout this work and Peter Werner at CPB Twyford (now KWS-UL Ltd) for supplying seed of the white-petalled oilseed rape breeders line. We thank Lars Chittka at the Queen Mary University, London, and two anonymous reviewers for providing constructive comments that helped to improve this manuscript. This work was funded by the UK Department for Food and Rural Affairs. Rothamsted Research is a national institute of bioscience strategically funded by the UK Biotechnology and Biological Sciences Research Council (BBSRC).

Supplementary material

11829_2013_9252_MOESM1_ESM.docx (83 kb)
Supplementary material 1 (DOCX 84 kb)

References

  1. Alford DV, Nilsson C, Ulber B (2003) Insect pests of oilseed rape crops. In: Alford DV (ed) Biocontrol of oilseed rape pests. Blackwell Science, Oxford, pp 9–42CrossRefGoogle Scholar
  2. Arnold SEJ, Chittka L (2012) Illumination preference, illumination constancy and colour discrimination by bumblebees in an environment with patchy light. J Exp Biol 215(13):2173–2180. doi: 10.1242/Jeb.065565 PubMedCrossRefGoogle Scholar
  3. Bernays EA, Chapman RF (1994) Host-plant selection by phytophagous insects. Chapman & Hall, LondonGoogle Scholar
  4. Blight MM, Smart LE (1999) Influence of visual cues and isothiocyanate lures on capture of the pollen beetle, Meligethes aeneus in field traps. J Chem Ecol 25(7):1501–1516CrossRefGoogle Scholar
  5. Briscoe AD, Chittka L (2001) The evolution of color vision in insects. Annu Rev Entomol 46:471–510. doi: 10.1146/annurev.ento.46.1.471 PubMedCrossRefGoogle Scholar
  6. Brunel EJ, Mesquida J, Renard M, Tanguy X (1994) Répartition de l’entomofaune pollinisatrice sur des fleurs de colza (Brassica napus L.) et de navette (Brassica campestris L.): incidence du caractère apétale de la navette. Apidologie 25:12–20CrossRefGoogle Scholar
  7. Chandler S, Tanaka Y (2007) Genetic modification in floriculture. Crit Rev Plant Sci 26(4):169–197. doi: 10.1080/07352680701429381 CrossRefGoogle Scholar
  8. Chittka L, Waser NM (1997) Why red flowers are not invisible to bees. Israel J Plant Sci 45(2–3):169–183CrossRefGoogle Scholar
  9. Chittka L, Shmida A, Troje N, Menzel R (1994) Ultraviolet as a component of flower reflections, and the color-perception of hymenoptera. Vision Res 34(11):1489–1508. doi: 10.1016/0042-6989(94)90151-1 PubMedCrossRefGoogle Scholar
  10. Cook SM (2000) Conditioned responses of free-flying honey bees to pollen cues. In: The use of pollen cues in resource location by a pollinator and a pest, Chap 7. Nottingham UniversityGoogle Scholar
  11. Cook SM, Bartlet E, Murray DA, Williams IH (2002) The role of pollen odour in the attraction of pollen beetles to oilseed rape flowers. Entomol Exp Appl 104(1):43–50CrossRefGoogle Scholar
  12. Cook SM, Sandoz JC, Martin AP, Murray DA, Poppy GM, Williams IH (2005) Could learning of pollen odours by honey bees (Apis mellifera) play a role in their foraging behaviour? Physiol Entomol 30(2):164–174. doi: 10.1111/j.1365-3032.2005.00445.x CrossRefGoogle Scholar
  13. Cook SM, Watts NP, Castle LM, Williams IH (2006) Determining the sex of insect pests of oilseed rape for behavioural bioassays. IOBC/wprs Bull 29(7):207–213Google Scholar
  14. Cook SM, Khan ZR, Pickett JA (2007a) The use of push-pull strategies in integrated pest management. Annu Rev Entomol 52:375–400. doi: 10.1146/annurev.ento.52.110405.091407 PubMedCrossRefGoogle Scholar
  15. Cook SM, Rasmussen HB, Birkett MA, Murray DA, Pye BJ, Watts NP, Williams IH (2007b) Behavioural and chemical ecology underlying the success of turnip rape (Brassica rapa) trap crops in protecting oilseed rape (Brassica napus) from the pollen beetle (Meligethes aeneus). Arthropod-Plant Inte 1(1):57–67. doi: 10.1007/s11829-007-9004-5 CrossRefGoogle Scholar
  16. Döring TF, Skellern MP, Watts NP, Cook SM (2012) Colour choice behaviour in the pollen beetle, Meligethes aeneus (Coleoptera: Nitidulidae). Physiol EntomolGoogle Scholar
  17. Dyer AG, Whitney HM, Arnold SEJ, Glover BJ, Chittka L (2007) Mutations perturbing petal cell shape and anthocyanin synthesis influence bumblebee perception of Antirrhinum majus flower colour. Arthropod-Plant Inte 1(1):45–55. doi: 10.1007/s11829-007-9002-7 CrossRefGoogle Scholar
  18. Foster SP, Harris MO (1997) Behaviorial manipulation methods for insect pest-management. Annu Rev Entomol 42:123–146PubMedCrossRefGoogle Scholar
  19. Fritzsche R (1957) Zur Biologie und Ökologie der Rapsschädlinge aus der Gattung Meligethes. Zeitschrift für Angewandte Entomologie 40(2):222–280. doi: 10.1111/j.1439-0418.1957.tb00863.x CrossRefGoogle Scholar
  20. Giamoustaris A, Mithen R (1996) The effect of flower colour and glucosinolates on the interaction between oilseed rape and pollen beetles. Entomol Exp Appl 80(1):206–208CrossRefGoogle Scholar
  21. Golding YC, Sullivan MS, Sutherland JP (1999) Visits to manipulated flowers by Episyrphus balteatus (Diptera: Syrphidae): partitioning the signals of petals and anthers. J Insect Behav 12(1):39–45. doi: 10.1023/A:1020925030522 CrossRefGoogle Scholar
  22. Goos M, Deptuch S, Faligowska K (1976) Introductory studies on collecting insects using coloured traps in field experiments. Polskie Pismo Entomologiczne 46:829–834Google Scholar
  23. Goto T (1987) Structure, stability and colour variation of natural anthocyanins. In: Herz W, Grisebach H, Kirby G, Tamm C (eds) Progress in the chemistry of organic natural products, vol 52. Springer-Verlag, Vienna, pp 113–158Google Scholar
  24. Hansen DM, Van der Niet T, Johnson SD (2012) Floral signposts: testing the significance of visual ‘nectar guides’ for pollinator behaviour and plant fitness. P Roy Soc B-Biol Sci 279(1729):634–639. doi: 10.1098/rspb.2011.1349 CrossRefGoogle Scholar
  25. Hoballah ME, Gubitz T, Stuurman J, Broger L, Barone M, Mandel T, Dell’Olivo A, Arnold M, Kuhlemeier C (2007) Single gene-mediated shift in pollinator attraction in Petunia. Plant Cell 19(3):779–790. doi: 10.1105/tpc.106.048694 PubMedCrossRefGoogle Scholar
  26. Jersáková J, Jürgens A, Šmilauer P, Johnson SD (2012) The evolution of floral mimicry: identifying traits that visually attract pollinators. Funct Ecol 26(6):1381–1389. doi: 10.1111/j.1365-2435.2012.02059.x CrossRefGoogle Scholar
  27. Johnson SD, Andersson S (2002) A simple field method for manipulating ultraviolet reflectance of flowers. Can J Bot 80(12):1325–1328. doi: 10.1139/B02-116 CrossRefGoogle Scholar
  28. Katsumoto Y, Fukuchi-Mizutani M, Fukui Y, Brugliera F, Holton TA, Karan M, Nakamura N, Yonekura-Sakakibara K, Togami J, Pigeaire A, Tao GQ, Nehra NS, Lu CY, Dyson BK, Tsuda S, Ashikari T, Kusumi T, Mason JG, Tanaka Y (2007) Engineering of the rose flavonoid biosynthetic pathway successfully generated blue-hued flowers accumulating delphinidin. Plant Cell Physiol 48(11):1589–1600. doi: 10.1093/Pcp/Pcm131 PubMedCrossRefGoogle Scholar
  29. Kelber A, Vorobyev M, Osorio D (2003) Animal colour vision—behavioural tests and physiological concepts. Biol Rev 78(1):81–118. doi: 10.1017/S1464793102005985 PubMedCrossRefGoogle Scholar
  30. Kevan PG, Baker HG (1983) Insects as flower visitors and pollinators. Annu Rev Entomol 28:407–453CrossRefGoogle Scholar
  31. Kevan PG, Giurfa M, Chittka L (1996) Why are there so many and so few white flowers? Trends Plant Sci 1(8):280–284CrossRefGoogle Scholar
  32. Kevan PG, Chittka L, Dyer AG (2001) Limits to the salience of ultraviolet: lessons from colour vision in bees and birds. J Exp Biol 204(14):2571–2580PubMedGoogle Scholar
  33. Kostal V (1992) Monitoring of activity and abundance of adult pollen beetle (Meligethes-Aeneus F) and cabbage stem weevil (Ceutorhynchus-Pallidactylus Marsh) in winter rape stand. Rost Vyroba 38(3–4):297–306Google Scholar
  34. Kovach J, Rieckenberg R, English-Loeb G, Pritts M (1999) Oviposition patterns of the strawberry bud weevil (Coleoptera: Curculionidae) at two spatial scales and implications for management. J Econ Entomol 92(6):1358–1363Google Scholar
  35. Lancashire PD, Bleiholder H, Vandenboom T, Langeluddeke P, Stauss R, Weber E, Witzenberger A (1991) A uniform decimal code for growth-stages of crops and weeds. Ann Appl Biol 119(3):561–601CrossRefGoogle Scholar
  36. Laska P, Zelenkova I, Bicik V (1986) Color attraction in species of the genera-Delia (Diptera, Anthomyidae), Ceutorhynchus, Meligethes and Phyllotreta (Coleoptera, Curculionidae, Nitidulidae, Chrysomelidae). Acta Entomol Bohemos 83(6):418–424Google Scholar
  37. Leavitt H, Robertson IC (2006) Petal herbivory by chrysomelid beetles (Phyllotreta sp.) is detrimental to pollination and seed production in Lepidium papilliferum (Brassicaceae). Ecol Entomol 31 (6):657–660. doi:  10.1111/j.1365-2311.2006.00820.x
  38. Lebesa LN, Khan ZR, Hassanali A, Pickett JA, Bruce TJA, Skellern M, Kruger K (2011) Responses of the blister beetle Hycleus apicicornis to visual stimuli. Physiol Entomol 36(3):220–229. doi: 10.1111/j.1365-3032.2011.00787.x CrossRefGoogle Scholar
  39. Lu CY, Chandler SF, Mason JG, Brugliera F (2003) Florigene flowers: from laboratory to market. Plant biotechnology, 2002 and beyond. Springer, DordrechtGoogle Scholar
  40. Lubbock J (1882) Ants, bees and wasps: a record of observations on the habits of social Hymenoptera. Kegan Paul, Trench, Trubner & Co, LondonCrossRefGoogle Scholar
  41. Lunau K (1988) Angeborenes und erlerntes verhalten beim blütenbesuch von schwebfliegen—attrappenversuche mit Eristalis pertinax (Scopoli) (Diptera, Syrphidae). Zoologische Jahrbucher Abteilung für Allemeine Zoologie und Physiologie der Tiere 92:487–499Google Scholar
  42. Lunau K (2000) The ecology and evolution of visual pollen signals. Plant Syst Evol 222(1–4):89–111. doi: 10.1007/Bf00984097 CrossRefGoogle Scholar
  43. Lunau K, Wacht S, Chittka L (1996) Colour choices of naive bumble bees and their implications for colour perception. J Comp Physiol A 178(4):477–489CrossRefGoogle Scholar
  44. Mänd M, Williams IH, Viik E, Karise R (2010) Oilseed rape, bees and integrated pest management. In: Williams IH (ed) Biocontrol-based integrated management of oilseed rape pests. Springer-Verlag, LondonGoogle Scholar
  45. Menzel R (1985) Learning in honey bees in an ecological and behavioural context. Forts Zool 31:55–74Google Scholar
  46. Mothershead K, Marquis RJ (2000) Fitness impacts of herbivory through indirect effects on plant-pollinator interactions in Oenothera macrocarpa. Ecology 81(1):30–40Google Scholar
  47. Nabirye J, Nampala P, Kyamanywa S, Ogenga-Latigo MW, Wilson H, Adipala E (2003) Determination of damage-yield loss relationships and economic injury levels of flower thrips on cowpea in eastern Uganda. Crop Prot 22(7):911–915. doi: 10.1016/S0261-2194(03)00086-3 CrossRefGoogle Scholar
  48. Nilsson C (1987) Yield losses in summer rape caused by pollen beetles (Meligethes spp.). Swed J Agric Res 17(3):105–111Google Scholar
  49. Nozzolillo C, Anderson J, Warwick S (1995) Anthocyanoplasts in the Brassicaceae: does their presence serve as a chemotaxonomic marker within the family? Polyphenols Actualities 12:25–26Google Scholar
  50. Owen CR, Bradshaw HD (2011) Induced mutations affecting pollinator choice in Mimulus lewisii (Phrymaceae). Arthropod-Plant Inte 5(3):235–244. doi: 10.1007/s11829-011-9133-8 CrossRefGoogle Scholar
  51. Peter CI, Johnson SD (2008) Mimics and magnets: the importance of color and ecological facilitation in floral deception. Ecology 89(6):1583–1595. doi: 10.1890/07-1098.1 PubMedCrossRefGoogle Scholar
  52. Prokopy RJ, Collier RH, Finch S (1983) Visual detection of host plants by cabbage root Flies. Entomol Exp Appl 34(1):85–89CrossRefGoogle Scholar
  53. Spaethe J, Tautz J, Chittka L (2001) Visual constraints in foraging bumblebees: flower size and color affect search time and flight behaviour. P Natl Acad Sci USA 98(7):3898–3903. doi: 10.1073/pnas.071053098 CrossRefGoogle Scholar
  54. Stavenga DG, Smits RP, Hoenders BJ (1993) Simple exponential functions describing the absorbency bands of visual pigment spectra. Vision Res 33(8):1011–1017PubMedCrossRefGoogle Scholar
  55. Tanaka Y, Tsuda S, Kusumi T (1998) Metabolic engineering to modify flower color. Plant Cell Physiol 39(11):1119–1126CrossRefGoogle Scholar
  56. Tansey JA, Dosdall LM, Keddie BA, Noble SD (2010) Contributions of visual cues to cabbage seedpod weevil, Ceutorhynchus obstrictus (Marsham) (Coleoptera: Curculionidae), resistance in novel host genotypes. Crop Prot 29(5):476–481. doi: 10.1016/j.cropro.2009.11.005 CrossRefGoogle Scholar
  57. Thieme T, Heimbach U, Muller A (2010) Chemical control of insect pests and insecticide resistance in oilseed rape. In: Williams IH (ed) Biocontrol-based integrated management of oilseed rape pests. Springer-Verlag, London, pp 131–335Google Scholar
  58. Waser NM, Price MV (1985) The effect of nectar guides on pollinator preference—experimental studies with a montane herb. Oecologia 67(1):121–126. doi: 10.1007/Bf00378462 CrossRefGoogle Scholar
  59. Wasmann E (1926) Versuche über den Farbensinn des Rapskafers (Meligethes aeneus L.). Zeitschrift für Wissenschaftliche Insektenbiologie 21:147Google Scholar
  60. Williams IH (2004) Advances in insect pest management of oilseed rape in Europe. In: Ishaaya I, Horowitz AR (eds) Novel approaches to insect pest management. Springer-Verlag, Berlin, pp 181–208Google Scholar
  61. Williams IH (2010) The major insect pests of oilseed rape in Europe and their management: an overview. In: Williams IH (ed) Biocontrol-based integrated management of oilseed rape pests. Springer-Verlag, London, pp 1–43CrossRefGoogle Scholar
  62. Williams IH, Cook SM (2010) Crop location by oilseed rape pests and host location by their parasitoids. In: Williams IH (ed) Biocontrol-based integrated management of oilseed rape pests. Springer-Verlag, London, pp 215–244CrossRefGoogle Scholar
  63. Williams IH, Free JB (1978) Feeding and mating-behavior of pollen beetles (Meligethes-Aeneus Fab) and seed weevils (Ceutorhynchus-Assimilis Payk) on oil-seed rape (Brassica-Napus L.). J Agric Sci 91:453–459CrossRefGoogle Scholar
  64. Yoshioka Y, Horisaki A, Kobayashi K, Syafaruddin NiikuraS, Ninomiya S, Ohsawa R (2005) Intraspecific variation in the ultraviolet colour proportion of flowers in Brassica rapa L. Plant Breed 124(6):551–556CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Samantha M. Cook
    • 1
    Email author
  • Matthew P. Skellern
    • 1
  • Thomas F. Döring
    • 2
    • 3
  • John A. Pickett
    • 1
  1. 1.Rothamsted ResearchHarpendenUK
  2. 2.The Organic Research CentreElm Farm, Hamstead MarshallUK
  3. 3.Department of Life SciencesImperial College LondonAscotUK

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