Effect of flower traits and hosts on the abundance of parasitoids in perennial multiple species wildflower strips sown within oilseed rape (Brassica napus) crops
[en] Reducing the use of insecticides is an important issue for agriculture today. Sowing wildflower strips along field margins or within crops represents a promising tool to support natural enemy populations in agricultural landscapes and, thus, enhance conservation biological control. However, it is important to sow appropriate flower species that attract natural enemies efficiently. The presence of prey and hosts may also guide natural enemies to wildflower strips, potentially preventing them from migrating into adjacent crops. Here, we assessed how seven flower traits, along with the abundance of pollen beetles (Meligethes spp., Coleoptera: Nitidulidae) and true weevils (Ceutorhynchus spp., Coleoptera: Curculionidae), affect the density of parasitoids of these two coleopterans in wildflower strips sown in an oilseed rape field in Gembloux (Belgium). Only flower traits, not host (i.e. pollen beetles and true weevils) abundance, significantly affected the density of parasitoids. Flower colour, ultraviolet reflectance and nectar availability were the main drivers affecting parasitoids. These results demonstrate how parasitoids of oilseed rape pests react to flower cues under field conditions. Similar analyses on the pests and natural enemies of other crops are expected to help to develop perennial flower mixtures able to enhance biological control throughout a rotation system.
Research center :
TERRA Teaching and Research Centre - TERRA
Disciplines :
Environmental sciences & ecology Agriculture & agronomy Entomology & pest control
Author, co-author :
Hatt, Séverin ; Université de Liège - ULiège > R&D Direction : Chercheurs ULiège en mobilité
Uyttenbroeck, Roel ; Université de Liège - ULiège > Ingénierie des biosystèmes (Biose) > Biodiversité et Paysage
Chevalier Mendes Lopes, Thomas; Gembloux Agro‑Bio Tech, University of Liège, Gembloux, Belgium > Department of Agronomy, Biology and Chemistry > Functional and Evolutionary Entomology
Chen, Julian; Chinese Academy of Agricultural Sciences > Institute of Plant Protection > State Key Laboratory for Biology of Plant Diseases and Insect Pests
Piqueray, Julien; Natagriwal Asbl
Monty, Arnaud ; Université de Liège - ULiège > Ingénierie des biosystèmes (Biose) > Biodiversité et Paysage
Francis, Frédéric ; Université de Liège - ULiège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Gestion durable des bio-agresseurs
Language :
English
Title :
Effect of flower traits and hosts on the abundance of parasitoids in perennial multiple species wildflower strips sown within oilseed rape (Brassica napus) crops
Baldi I, Cordier S, Coumoul X et al (2013) Pesticides: effets sur la santé. INSERM Institut national de la santé et de la recherche médicale, Paris
Balzan MV, Moonen A-C (2014) Field margin vegetation enhances biological control and crop damage suppression from multiple pests in organic tomato fields. Entomol Exp Appl 150:45–65. doi:10.1111/eea.12142
Balzan MV, Wäckers FL (2013) Flowers to selectively enhance the fitness of a host-feeding parasitoid: adult feeding by Tuta absoluta and its parasitoid Necremnus artynes. Biol Control 67:21–31. doi:10.1016/j.biocontrol.2013.06.006
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. doi:10.1007/s10841-014-9680-2
Barbosa PA (1998) Conservation biological control. Academic Press, San Diego
Begum M, Gurr GM, Wratten SD, Nicol HI (2004) Flower color affects tri-trophic-level biocontrol interactions. Biol Control 30:584–590. doi:10.1016/j.biocontrol.2004.03.005
Bianchi FJJA, Wäckers F (2008) Effects of flower attractiveness and nectar availability in field margins on biological control by parasitoids. Biol Control 46:400–408. doi:10.1016/j.biocontrol.2008.04.010
Borcard D, Gillet F, Legendre P (2011) Numerical ecology with R. Springer, New York
Botta-Dukát Z (2005) Rao’s quadratic entropy as a measure of functional diversity based on multiple traits. J Veg Sci 16:533–540. doi:10.1111/j.1654-1103.2005.tb02393.x
Büchi R (2002) Mortality of pollen beetle (Meligethes spp.) larvae due to predators and parasitoids in rape fields and the effect of conservation strips. Agric Ecosyst Environ 90:255–263. doi:10.1016/S0167-8809(01)00213-4
Campbell AJ, Biesmeijer JC, Varma V, Wäckers FL (2012) Realising multiple ecosystem services based on the response of three beneficial insect groups to floral traits and trait diversity. Basic Appl Ecol 13:363–370. doi:10.1016/j.baae.2012.04.003
Carrié RJG, George DR, Wäckers FL (2012) Selection of floral resources to optimise conservation of agriculturally-functional insect groups. J Insect Conserv 16:635–640. doi:10.1007/s10841-012-9508-x
Chittka L, Shmida A, Troje N, Menzel R (1994) Ultraviolet as a component of flower reflections, and the colour perception of Hymenoptera. Vision Res 34:1489–1508. doi:10.1016/0042-6989(94)90151-1
Colignon P, Hastir P, Gaspar C, Francis F (2001) Effects of insecticide treatments on insect density and diversity in vegetable open fields. Meded Van Fac Landbouwkd En Toegepaste Biol Wet Rijksuniv Te Gent 66:403–411
Cook SM, Skellern MP, Döring TF, Pickett JA (2013) Red oilseed rape? The potential for manipulation of petal colour in control strategies for the pollen beetle (Meligethes aeneus). Arthropod-Plant Interact 7:249–258. doi:10.1007/s11829-013-9252-5
Core Team R (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Dı́az S, Cabido M (2001) Vive la différence: plant functional diversity matters to ecosystem processes. Trends Ecol Evol 16:646–655. doi:10.1016/S0169-5347(01)02283-2
Döring TF, Archetti M, Hardie J (2009) Autumn leaves seen through herbivore eyes. Proc R Soc Lond B Biol Sci 276:121–127. doi:10.1098/rspb.2008.0858
Döring TF, Skellern M, Watts N, Cook SM (2012) Colour choice behaviour in the pollen beetle Meligethes aeneus (Coleoptera: nitidulidae). Physiol Entomol 37:360–368. doi:10.1111/j.1365-3032.2012.00850.x
Ekroos J, Olsson O, Rundlöf M et al (2014) Optimizing agri-environment schemes for biodiversity, ecosystem services or both? Biol Conserv 172:65–71. doi:10.1016/j.biocon.2014.02.013
European Commission (2005) Agri-environment measures. Overview on general principles, types of measures and application. European Commission, Directorate General for Agriculture and Rural Development
Ferguson AW, Williams IH, Castle LM, Skellern MP (2010) Key parasitoids of the pests of oilseed rape in Europe: A guide to their identification. In: Williams IH (ed) Biocontrol-Based Integrated Management of Oilseed Rape Pests. Springer, The Netherlands, pp 77–114
Fiedler AK, Landis DA (2007a) Plant Characteristics Associated with Natural Enemy Abundance at Michigan Native Plants. Environ Entomol 36:878–886. doi:10.1093/ee/36.4.878
Fiedler AK, Landis DA (2007b) Attractiveness of Michigan native plants to arthropod natural enemies and herbivores. Environ Entomol 36:751–765. doi:10.1093/ee/36.4.751
Free JB, Williams IH (1978) The responses of the pollen beetle, Meligethes aeneus, and the seed weevil, Ceuthorhynchus assimilis, to oil-seed rape, Brassica napus, and other plants. J Appl Ecol 15:761–774. doi:10.2307/2402773
Geiger F, Bengtsson J, Berendse F et al (2010) Persistent negative effects of pesticides on biodiversity and biological control potential on European farmland. Basic Appl Ecol 11:97–105. doi:10.1016/j.baae.2009.12.001
Gibbons D, Morrissey C, Mineau P (2015) A review of the direct and indirect effects of neonicotinoids and fipronil on vertebrate wildlife. Environ Sci Pollut Res 22:103–118. doi:10.1007/s11356-014-3180-5
Haaland C, Naisbit RE, Bersier L-F (2011) Sown wildflower strips for insect conservation: a review. Insect Conserv Divers 4:60–80. doi:10.1111/j.1752-4598.2010.00098.x
Hanson HI, Smith HG, Hedlund K (2015) Agricultural management reduces emergence of pollen beetle parasitoids. Agric Ecosyst Environ 205:9–14. doi:10.1016/j.agee.2015.03.001
Hatt S, Uyttenbroeck R, Lopes T et al (2015) Do wildflower strips favor insect pest populations at field margins? Agric Agric Sci Procedia 6:30–37. doi:10.1016/j.aaspro.2015.08.034
Horton DR, Broers DA, Lewis RR et al (2003) Effects of mowing frequency on densities of natural enemies in three Pacific Northwest pear orchards. Entomol Exp Appl 106:135–145. doi:10.1046/j.1570-7458.2003.00018.x
Idris AB, Grafius E (1995) Wildflowers as nectar sources for Diadegma insulare (Hymenoptera: ichneumonidae), a parasitoid of diamondback moth (Lepidoptera: Yponomeutidae). Environ Entomol 24:1726–1735. doi:10.1093/ee/24.6.1726
Jervis MA, Kidd NAC, Fitton MG et al (1993) Flower-visiting by hymenopteran parasitoids. J Nat Hist 27:67–105. doi:10.1080/00222939300770051
Jönsson M (2005) Responses to oilseed rape and cotton volatiles in insect herbivores and parasitoids. Doctoral thesis, Swedish University of Agricultural Sciences
Kattge J, Díaz S, Lavorel S et al (2011) TRY—a global database of plant traits. Glob Change Biol 17:2905–2935. doi:10.1111/j.1365-2486.2011.02451.x
Kirk-Spriggs AH (1996) Pollen beetles: Coleoptera: Kateretidae and Nitidulidae: Meligethinae. Royal Entomological Society, London
Krebs JR, Wilson JD, Bradbury RB, Siriwardena GM (1999) The second Silent Spring? Nature 400:611–612. doi:10.1038/23127
Laliberté E, Legendre P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299–305. doi:10.1890/08-2244.1
Laliberté E, Legendre P, Shipley B (2014) FD: measuring functional diversity from multiple traits, and other tools for functional ecology. R package
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, Meise
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
Landis DA, Wratten SD, Gurr GM (2000) Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu Rev Entomol 45:175–201. doi:10.1146/annurev.ento.45.1.175
Lavorel S, Garnier E (2002) Predicting changes in community composition and ecosystem functioning from plant traits: revisiting the Holy Grail. Funct Ecol 16:545–556. doi:10.1046/j.1365-2435.2002.00664.x
Lavorel S, Grigulis K, McIntyre S et al (2008) Assessing functional diversity in the field–methodology matters! Funct Ecol 22:134–147. doi:10.1111/j.1365-2435.2007.01339.x
Lundgren JG (2009) Relationships of natural enemies and non-prey foods. Progress in Biological Control, Springer, The Netherlands
Morris MG (2008) True Weevils (Part II): (Coleoptera: Curculionidae, Ceutorhynchinae). Royal Entomological Society, London
Müller H (1881) Alpenblumen, ihre Befruchtung durch Insekten und ihre Anpassungen an dieselben. W. Engelmann, Leipzig
Nilsson C (2003) Parasitoids of the pollen beetles. In: Alford DV (ed) Biocontrol of oilseed rape pests. Blackwell, Oxford, pp 73–86
Oksanen J, Guillaume Blanchet F, Kindt R, et al (2015) Vegan: community ecology package. R package
Ômura H, Honda K, Hayashi N (1999) Chemical and chromatic bases for preferential visiting by the cabbage butterfly, Pieris rapae, to rape flowers. J Chem Ecol 25:1895–1906. doi:10.1023/A:1020990018111
Patt JM, Hamilton GC, Lashomb JH (1997) Foraging success of parasitoid wasps on flowers: interplay of insect morphology, floral architecture and searching behavior. Entomol Exp Appl 83:21–30. doi:10.1046/j.1570-7458.1997.00153.x
Rand TA, Tylianakis JM, Tscharntke T (2006) Spillover edge effects: the dispersal of agriculturally subsidized insect natural enemies into adjacent natural habitats. Ecol Lett 9:603–614. doi:10.1111/j.1461-0248.2006.00911.x
Rusch A, Bommarco R, Jonsson M et al (2013) Flow and stability of natural pest control services depend on complexity and crop rotation at the landscape scale. J Appl Ecol 50:345–354. doi:10.1111/1365-2664.12055
Sivinski J, Wahl D, Holler T et al (2011) Conserving natural enemies with flowering plants: estimating floral attractiveness to parasitic Hymenoptera and attraction’s relationship to flower and plant morphology. Biol Control 58:208–214. doi:10.1016/j.biocontrol.2011.05.002
Tscharntke T, Karp DS, Chaplin-Kramer R et al (2016) When natural habitat fails to enhance biological pest control – Five hypotheses. Biol Conserv In press. doi:10.1016/j.biocon.2016.10.001
Tschumi M, Albrecht M, Entling MH, Jacot K (2015) High effectiveness of tailored flower strips in reducing pests and crop plant damage. Proc R Soc B 282:20151369. doi:10.1098/rspb.2015.1369
Tschumi M, Albrecht M, Bärtschi C et al (2016) Perennial, species-rich wildflower strips enhance pest control and crop yield. Agric Ecosyst Environ 220:97–103. doi:10.1016/j.agee.2016.01.001
Ulber B (2003) Parasitoids of Ceutorhynchid stem weevils. In: Alford DV (ed) Biocontrol of oilseed rape pests. Blackwell, Oxford, UK, pp 87–96
Ulber B, Williams IH, Luik A et al (2010) Parasitoids of oilseed rape pests in Europe: Key species for conservation biocontrol. In: Williams IH (ed) Biocontrol-Based Integrated Management of Oilseed Rape Pests. Springer, The Netherlands, pp 45–76
Uyttenbroeck R, Hatt S, Piqueray J et al (2015) Creating perennial flower strips: think functional! Agric Agric Sci Procedia 6:95–101. doi:10.1016/j.aaspro.2015.08.044
Uyttenbroeck R, Hatt S, Paul A et al (2016) Pros and cons of flowers strips for farmers: a review. Biotechnol Agron Soc Environ 20:225–235
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. doi:10.1111/1365-2664.12605
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. doi:10.1016/j.biocontrol.2006.06.003
Violle C, Navas M-L, Vile D et al (2007) Let the concept of trait be functional! Oikos 116:882–892. doi:10.1111/j.0030-1299.2007.15559.x
Wäckers FL (1994) The effect of food deprivation on the innate visual and olfactory preferences in the parasitoid Cotesia rubecula. J Insect Physiol 40:641–649. doi:10.1016/0022-1910(94)90091-4
Williams IH (2003) Parasitoids of the cabbage seed weevil. In: Alford DV (ed) Biocontrol of Oilseed Rape Pests. Blackwell, Oxford, pp 97–112
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, The Netherlands, pp 1–43
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, The Netherlands, pp 215–244
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. doi:10.1007/s00442-002-1128-9
