Arthropod-Plant Interactions

, Volume 13, Issue 1, pp 127–137 | Cite as

Identification of flower functional traits affecting abundance of generalist predators in perennial multiple species wildflower strips

  • Séverin HattEmail author
  • Roel Uytenbroeck
  • Thomas Lopes
  • Pierre Mouchon
  • Naoya Osawa
  • Julien Piqueray
  • Arnaud Monty
  • Frédéric Francis
Original Paper


In agricultural fields, wildflower strips can be sown to enhance conservation biological control of insect pests. However, issues remain regarding the composition of flower mixtures to effectively attract and support large communities of natural enemies. Trait-based approaches are promising for this purpose. In the present study, conducted in an agricultural field of Belgium in 2014 and 2015, 15 flower mixtures were considered to explore the relation between the abundance of trapped generalist predators (i.e. lacewings [Neuroptera: Chrysopidae], ladybeetles [Coleoptera: Coccinellidae] and hoverflies [Diptera: Syrphidae]) and the community-weighted means of seven flower traits. Through a redundancy analysis, it was found that the presence/absence of flower ultra-violet pattern and the morphology of the corolla (that determines the accessibility of floral resources) were the traits that significantly affected the abundance of the generalist predators in the flower mixtures. The ladybeetles Harmonia axyridis and Propylea quatuordecimpunctata as well as the lacewings Chrysoperla carnea were more abundant in mixtures with a high cover of flowers showing an ultra-violet pattern, while the opposite was observed for the ladybeetle Coccinella septempunctata. As for hoverflies, Episyrphus balteatus and Eupeodes corollae were more abundant in mixtures with a high cover of flowers with open nectar. These results bring new knowledge regarding how a range of natural enemy species reacts to flower cues in diversified plant communities and should help in elaborating flower mixtures that enhance conservation biological control.


Conservation biological control Coccinellidae Syrphidae Chrysopidae Community-weighted mean Ultra-violet pattern Corolla morphology 



The authors are grateful for the technical support provided by the AgricultureIsLife experimental farm of Gembloux Agro-Bio Tech (University of Liège), Frank Van De Meutter (The Research Institute for Nature and Forest – INBO, Belgium) for verifying the identifications of some hoverfly species, and the TRY initiative on plant traits ( for providing the data on flower traits. This research was funded by the Cellule d’Appui à la Recherche et à l’Enseignement (CARE) AgricultureIsLife–University of Liège (with doctoral scholarships), Wallonia-Brussels International (with the WBI.World post-doctoral scholarship) and the University of Liège-European Commission (with the ‘Be(lgium) International Post-Doc’ Marie-Curie COFUND grant).

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Supplementary material

11829_2018_9652_MOESM1_ESM.docx (18 kb)
Supplementary material 1 (DOCX 18 KB)
11829_2018_9652_MOESM2_ESM.docx (21 kb)
Supplementary material 2 (DOCX 20 KB)
11829_2018_9652_MOESM3_ESM.docx (25 kb)
Supplementary material 3 (DOCX 25 KB)
11829_2018_9652_MOESM4_ESM.docx (23 kb)
Supplementary material 4 (DOCX 24 KB)


  1. Adedipe F, Park Y-L (2010) Visual and olfactory preference of Harmonia axyridis (Coleoptera: Coccinellidae) adults to various companion plants. J Asia Pac Entomol 13:316–323. CrossRefGoogle Scholar
  2. Agee HR, Mitchell ER, Flanders RV (1990) Spectral sensitivity of the compound eye of Coccinella septempunctata (Coleoptera: Coccinellidae). Ann Entomol Soc Am 83:817–819. CrossRefGoogle Scholar
  3. Amy C, Noël G, Hatt S et al (2018) Flower strips in wheat intercropping system: effect on pollinator abundance and diversity in Belgium. Insects 9:114. CrossRefPubMedCentralGoogle Scholar
  4. Balzan MV, Bocci G, Moonen A-C (2014) Augmenting flower trait diversity in wildflower strips to optimise the conservation of arthropod functional groups for multiple agroecosystem services. J Insect Conserv 18:713–728. CrossRefGoogle Scholar
  5. Balzan MV, Bocci G, Moonen A-C (2016) Utilisation of plant functional diversity in wildflower strips for the delivery of multiple agroecosystem services. Entomol Exp Appl 158:319. CrossRefGoogle Scholar
  6. Barbosa PA (1998) Conservation biological control. Academic Press, San DiegoCrossRefGoogle Scholar
  7. Berkvens N, Bonte J, Berkvens D et al (2008) Pollen as an alternative food for Harmonia axyridis. Biocontrol 53:201–210. CrossRefGoogle Scholar
  8. Borcard D, Gillet F, Legendre P (2011) Numerical ecology with R. Springer, New YorkCrossRefGoogle Scholar
  9. Briscoe AD, Chittka L (2001) The evolution of colour vision in insects. Annu Rev Entomol 46:471–510. CrossRefGoogle Scholar
  10. Chen XX, Yan HY, Wei W et al (2009) Effect of spectral sensitivity and intensity response on the phototaxis of Propylea japonica (Thunberg). Acta Ecol Sin 29:2349–2355Google Scholar
  11. Crowder DW, Northfield TD, Strand MR, Snyder WE (2010) Organic agriculture promotes evenness and natural pest control. Nature 466:109–113. CrossRefGoogle Scholar
  12. Dassou AG, Tixier P (2016) Response of pest control by generalist predators to local-scale plant diversity: a meta-analysis. Ecol Evol 6:1143–1153. CrossRefPubMedCentralGoogle Scholar
  13. Díaz S, Cabido M (2001) Vive la différence: plant functional diversity matters to ecosystem processes. Trends Ecol Evol 16:646–655. CrossRefGoogle Scholar
  14. Fiedler AK, Landis DA (2007) Plant characteristics associated with natural enemy abundance at Michigan native plants. Environ Entomol 36:878–886. CrossRefGoogle Scholar
  15. Gardarin A, Plantegenest M, Bischoff A, Valantin-Morison M (2018) Understanding plant–arthropod interactions in multitrophic communities to improve conservation biological control: useful traits and metrics. J Pest Sci 91:943–955CrossRefGoogle Scholar
  16. Garnier E, Navas M-L (2012) A trait-based approach to comparative functional plant ecology: concepts, methods and applications for agroecology. A review. Agron Sustain Dev 32:365–399. CrossRefGoogle Scholar
  17. Grettenberger IM, Tooker JF (2017) Variety mixtures of wheat influence aphid populations and attract an aphid predator. Arthr Plant Interact 11:133–146. CrossRefGoogle Scholar
  18. Hatt S, Lopes T, Boeraeve F et al (2017a) Pest regulation and support of natural enemies in agriculture: experimental evidence of within field wildflower strips. Ecol Eng 98:240–245. CrossRefGoogle Scholar
  19. Hatt S, Uyttenbroeck R, Lopes T et al (2017b) Effect of flower traits and hosts on the abundance of parasitoids in perennial multiple species wildflower strips sown within oilseed rape (Brassica napus) crops. Arthr Plant Interact. Google Scholar
  20. Hatt S, Uyttenbroeck R, Lopes T et al (2017c) Do flower mixtures with high functional diversity enhance aphid predators in wildflower strips? Eur J Entomol 114:66–76. CrossRefGoogle Scholar
  21. Hatt S, Boeraeve F, Artru S et al (2018) Spatial diversification of agroecosystems to enhance biological control and other regulating services: an agroecological perspective. Sci Total Environ 621:600–611. CrossRefGoogle Scholar
  22. Hautier L, San Martin G, Callier P et al (2011) Alkaloids provide evidence of intraguild predation on native coccinellids by Harmonia axyridis in the field. Biol Invasions 13:1805–1814. CrossRefGoogle Scholar
  23. Holland JM, Bianchi FJJA, Entling MH et al (2016) Structure, function and management of semi-natural habitats for conservation biological control: a review of European studies. Pest Manag Sci 72:1638–1651. CrossRefGoogle Scholar
  24. Institut Royal Météorologique (2014) Spring 2014. Accessed 27 Sep 2018
  25. Institut Royal Météorologique (2015) Spring 2015. Accessed 27 Sep 2018
  26. Jones CE, Buchmann SL (1974) Ultraviolet floral patterns as functional orientation cues in Hymenopterous pollination systems. Anim Behav 22:481–485. CrossRefGoogle Scholar
  27. Jonsson M, Kaartinen R, Straub CS (2017) Relationships between natural enemy diversity and biological control. Curr Opin Insect Sci 20:1–6. CrossRefGoogle Scholar
  28. Kattge J, Díaz S, Lavorel S et al (2011) TRY—a global database of plant traits. Glob Chang Biol 17:2905–2935. CrossRefPubMedCentralGoogle Scholar
  29. Kevan P, Giurfa M, Chittka L (1996) Why are there so many and so few white flowers? Trends Plant Sci 1:280–284. CrossRefGoogle Scholar
  30. Koczor S, Szentkiralyi F, Fekete Z, Toth M (2017) Smells good, feels good: oviposition of Chrysoperla carnea-complex lacewings can be concentrated locally in the field with a combination of appropriate olfactory and tactile stimuli. J Pest Sci 90:311–317. CrossRefGoogle Scholar
  31. Kolz S, Kühn I, Durka W (2002) BIOLFLOR - Eine Datenbank zu biologisch-ökologischen Merkmalen der Gefäßpflanzen in Deutschland. Bundesamt für Naturschutz, BonnGoogle Scholar
  32. Koski MH, Ashman T-L (2014) Dissecting pollinator responses to a ubiquitous ultraviolet floral pattern in the wild. Funct Ecol 28:868–877. CrossRefGoogle Scholar
  33. Kral K, Stelzl M (1998) Daily visual sensitivity pattern in the green lacewing Chrysoperla carnea (Neuroptera: Chrysopidae). Eur J Entomol 95:327–333Google Scholar
  34. Laliberté E, Legendre P, Shipley B (2014) FD: measuring functional diversity from multiple traits, and other tools for functional ecology. R package version 1.0-12.
  35. Lambinon J, Delvosalle L, Duvigneaud J (2004) Nouvelle flore de Belgique, du Grand-Duché de Luxembourg, du Nord de la France et des régions voisines, 5th edn. Jardin Botanique National de Belgique, MeiseGoogle Scholar
  36. Lambinon J, De Langhe J-E, Delvosalle L, Duvigneaud J (2008) Flora van België, het Groothertogdom Luxemburg, Noord-Frankrijk en de aangrenzende gebieden. Nationale Plantentuin van België, MeiseGoogle Scholar
  37. Laubertie EA, Wratten SD, Hemptinne J-L (2012) The contribution of potential beneficial insectary plant species to adult hoverfly (Diptera: Syrphidae) fitness. Biol Control 61:1–6. CrossRefGoogle Scholar
  38. Lavorel S, Grigulis K, McIntyre S et al (2008) Assessing functional diversity in the field–methodology matters! Funct Ecol 22:134–147. Google Scholar
  39. Letourneau DK, Jedlicka JA, Bothwell SG, Moreno CR (2009) Effects of natural enemy biodiversity on the suppression of arthropod herbivores in terrestrial ecosystems. Annu Rev Ecol Evol Syst 40:573–592CrossRefGoogle Scholar
  40. Letourneau DK, Armbrecht I, Rivera BS et al (2011) Does plant diversity benefit agroecosystems? A synthetic review. Ecol Appl 21:9–21. CrossRefGoogle Scholar
  41. Lin J (1993) Identification of photoreceptor locations in the compound eye of Coccinella septempunctata Linnaeus (Coleoptera, Coccinellidae). J Insect Physiol 39:555–562. CrossRefGoogle Scholar
  42. Lopes T, Hatt S, Xu Q et al (2016) Wheat (Triticum aestivum L.)—based intercropping systems for biological pest control: a review. Pest Manag Sci 72:2193–2202. CrossRefGoogle Scholar
  43. Lu Z-X, Zhu P-Y, Gurr GM et al (2014) Mechanisms for flowering plants to benefit arthropod natural enemies of insect pests: prospects for enhanced use in agriculture. Insect Sci 21:1–12. CrossRefGoogle Scholar
  44. Lunau K (1992) A new interpretation of flower guide colouration: absorption of ultraviolet light enhances colour saturation. Plant Syst Evol 183:51–65. CrossRefGoogle Scholar
  45. Lundgren JG (2009a) Relationships of natural enemies and non-prey foods. In: Brodeur J (Eds) Progress in biological control. Springer, DordrechtGoogle Scholar
  46. Lundgren JG (2009b) Nutritional aspects of non-prey foods in the life histories of predaceous Coccinellidae. Biol Control 51:294–305. CrossRefGoogle Scholar
  47. Ma G, Ma C-S (2012) Differences in the nocturnal flight activity of insect pests and beneficial predatory insects recorded by light traps: possible use of a beneficial-friendly trapping strategy for controlling insect pests. Eur J Entomol 109:395–401. CrossRefGoogle Scholar
  48. Maredia KM, Gage SH, Landis DA, Wirth TM (1992) Visual response of Coccinella septempunctata (L.), Hippodamia parenthesis (Say), (Coleoptera: Coccinellidae), and Chrysoperla carnea (Stephens), (Neuroptera: Chrysopidae) to colors. Biol Control 2:253–256CrossRefGoogle Scholar
  49. McGill BJ, Enquist BJ, Weiher E, Westoby M (2006) Rebuilding community ecology from functional traits. Trends Ecol Evol 21:178–185. CrossRefGoogle Scholar
  50. Mondor EB, Warren JL (2000) Unconditioned and conditioned responses to colour in the predatory coccinellid, Harmonia axyridis (Coleoptera: Coccinellidae). Eur J Entomol 97:463–467. CrossRefGoogle Scholar
  51. Müller H (1881) Alpenblumen, ihre Befruchtung durch Insekten und ihre Anpassungen an dieselben. Wilhelm Engelmann, LeipzigGoogle Scholar
  52. Nalepa CA (2013) Coccinellidae captured in blacklight traps: Seasonal and diel pattern of the dominant species Harmonia axyridis (Coleoptera: Coccinellidae). Eur J Entomol 110:593–597CrossRefGoogle Scholar
  53. Nave A, Gonçalves F, Crespí AL et al (2016) Evaluation of native plant flower characteristics for conservation biological control of Prays oleae. Bull Entomol Res 106:249–257. CrossRefGoogle Scholar
  54. Oksanen J, Guillaume Blanchet F, Kindt R et al (2015) Vegan: Community Ecology Package. R packageGoogle Scholar
  55. Perovic DJ, Gamez-Virués S, Landis DA et al (2018) Managing biological control services through multi-trophic trait interactions: review and guidelines for implementation at local and landscape scales. Biol Rev 93:306–321. CrossRefGoogle Scholar
  56. Pervez A, Omkar (2011) Ecology of aphidophagous ladybird Propylea species: a review. J Asia Pac Entomol 14:357–365. CrossRefGoogle Scholar
  57. R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  58. Ricci C, Ponti L, Pires A (2005) Migratory flight and pre-diapause feeding of Coccinella septempunctata (Coleoptera) adults in agricultural and mountain ecosystems of Central Italy. Eur J Entomol 102:531–538. CrossRefGoogle Scholar
  59. Roy HE, Adriaens T, Isaac NJB et al (2012) Invasive alien predator causes rapid declines of native European ladybirds. Divers Distrib 18:717–725. CrossRefGoogle Scholar
  60. Roy HE, Brown PMJ, Comont RF et al (2013) Ladybirds. Pelagic Publishing, ExeterGoogle Scholar
  61. Rusch A, Chaplin-Kramer R, Gardiner MM et al (2016) Agricultural landscape simplification reduces natural pest control: a quantitative synthesis. Agric Ecosyst Environ 221:198–204. CrossRefGoogle Scholar
  62. San Martin G (2004) Clé de détermination des Chrysopidae de Belgique. Jeune et Nature asbl, WavreGoogle Scholar
  63. Silberglied RE (1979) Communication in the ultraviolet. Annu Rev Ecol Syst 10:373–398. CrossRefGoogle Scholar
  64. Song B, Liang Y, Liu S et al (2017) Behavioral responses of Aphis citricola (Hemiptera: Aphididae) and its natural enemy Harmonia axyridis (Coleoptera: Coccinellidae) to non-host plant volatiles. Fla Entomol 100:411–421. CrossRefGoogle Scholar
  65. Sutherland JP, Sullivan MS, Poppy GM (1999) The influence of floral character on the foraging behaviour of the hoverfly, Episyrphus balteatus. Entomol Exp Appl 93:157–164. CrossRefGoogle Scholar
  66. Toivonen M, Huusela-Veistola E, Herzon I (2018) Perennial fallow strips support biological pest control in spring cereal in Northern Europe. Biol Control 121:109–118. CrossRefGoogle Scholar
  67. Triltsch H (1999) Food remains in the guts of Coccinella septempunctata (Coleoptera: Coccinellidae) adults and larvae. Eur J Entomol 96:355–364Google Scholar
  68. Tschumi M, Albrecht M, Collatz J et al (2016) Tailored flower strips promote natural enemy biodiversity and pest control in potato crops. J Appl Ecol 53:1169–1176. CrossRefGoogle Scholar
  69. Uyttenbroeck R, Hatt S, Piqueray J et al (2015) Creating perennial flower strips: think functional! Agric Agric Sci Procedia 6:95–101. Google Scholar
  70. Uyttenbroeck R, Hatt S, Paul A et al (2016) Pros and cons of flowers strips for farmers: a review. Biotechnol Agron Soc Environ 20:225–235Google Scholar
  71. Uyttenbroeck R, Piqueray J, Hatt S et al (2017) Increasing plant functional diversity is not the key for supporting pollinators in wildflower strips. Agric Ecosyst Environ 249:144–155. CrossRefGoogle Scholar
  72. van Veen MP (2010) Hoverflies of Northwest Europe: identification keys to the Syrphidae. KNNV Publishing, ZeistCrossRefGoogle Scholar
  73. Van Rijn PCJ, Wäckers FL (2016) Nectar accessibility determines fitness, flower choice and abundance of hoverflies that provide natural pest control. J Appl Ecol 53:925–933. CrossRefGoogle Scholar
  74. Van Rijn PCJ, Kooijman J, Wäckers FL (2013) The contribution of floral resources and honeydew to the performance of predatory hoverflies (Diptera: Syrphidae). Biol Control 67:32–38. CrossRefGoogle Scholar
  75. Vattala HD, Wratten SD, Vattala CB et al (2006) The influence of flower morphology and nectar quality on the longevity of a parasitoid biological control agent. Biol Control 39:179–185. CrossRefGoogle Scholar
  76. Villenave J, Thierry D, Mamun AA et al (2005) The pollens consumed by common green lacewings Chrysoperla spp. (Neuroptera: Chrysopidae) in cabbage crop environment in western France. Eur J Entomol 102:547–552. CrossRefGoogle Scholar
  77. Villenave J, Deutsch B, Lodé T, Rat-Morris E (2006) Pollen preference of the Chrysoperla species (Neuroptera: Chrysopidae) occurring in the crop environment in western France. Eur J Entomol 103:771–777. CrossRefGoogle Scholar
  78. Wäckers FL, Van Rijn PCJ (2012) Pick and mix: selecting flowering plants to meet the requirements of target biological control insects. In: Gurr GM, Wratten SD, Snyder WE, Read DMY (eds) Biodiversity and insect pests: key issues for sustainable management. Wiley, Chichester, pp 139–165CrossRefGoogle Scholar
  79. Weber MG, Porturas LD, Keeler KH (2015) World list of plants with extrafloral nectaries. Accessed 20 Jun 2018
  80. Wratten SD, Bowie MH, Hickman JM et al (2003) Field boundaries as barriers to movement of hover flies (Diptera: Syrphidae) in cultivated land. Oecologia 134:605–611. CrossRefGoogle Scholar
  81. Wratten SD, Gillespie M, Decourtye A et al (2012) Pollinator habitat enhancement: benefits to other ecosystem services. Agric Ecosyst Environ 159:112–122. CrossRefGoogle Scholar
  82. Zhou J, Kuang R, Chen Z et al (2013) Phototactic behavior of Coccinella septempunctata L. (Coleoptera: Coccinellidae). Coleopt Bull 67:33–39. CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • Séverin Hatt
    • 1
    • 2
    • 3
    Email author
  • Roel Uytenbroeck
    • 1
    • 4
  • Thomas Lopes
    • 2
  • Pierre Mouchon
    • 2
    • 5
  • Naoya Osawa
    • 3
  • Julien Piqueray
    • 6
  • Arnaud Monty
    • 4
  • Frédéric Francis
    • 2
  1. 1.Terra–AgricultureIsLife, Gembloux Agro-Bio TechUniversity of LiègeGemblouxBelgium
  2. 2.Functional and Evolutionary Entomology, Terra Research and Teaching Center, Gembloux Agro-Bio TechUniversity of LiègeGemblouxBelgium
  3. 3.Laboratory of Forest Ecology, Faculty of AgricultureKyoto UniversityKyotoJapan
  4. 4.Biodiversity and Landscapes, Terra Research and Teaching Center, Gembloux Agro-Bio TechUniversity of LiègeGemblouxBelgium
  5. 5.Institut Supérieur d’Agriculture de LilleLilleFrance
  6. 6.Natagriwal asblGemblouxBelgium

Personalised recommendations