Abstract
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.
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References
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. https://doi.org/10.1016/j.aspen.2010.07.004
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. https://doi.org/10.1093/aesa/83.4.817
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. https://doi.org/10.3390/insects9030114
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. https://doi.org/10.1007/s10841-014-9680-2
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. https://doi.org/10.1111/eea.12403
Barbosa PA (1998) Conservation biological control. Academic Press, San Diego
Berkvens N, Bonte J, Berkvens D et al (2008) Pollen as an alternative food for Harmonia axyridis. Biocontrol 53:201–210. https://doi.org/10.1007/s10526-007-9128-7
Borcard D, Gillet F, Legendre P (2011) Numerical ecology with R. Springer, New York
Briscoe AD, Chittka L (2001) The evolution of colour vision in insects. Annu Rev Entomol 46:471–510. https://doi.org/10.1146/annurev.ento.46.1.471
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 29:2349–2355
Crowder DW, Northfield TD, Strand MR, Snyder WE (2010) Organic agriculture promotes evenness and natural pest control. Nature 466:109–113. https://doi.org/10.1038/nature09183
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. https://doi.org/10.1002/ece3.1917
Díaz S, Cabido M (2001) Vive la différence: plant functional diversity matters to ecosystem processes. Trends Ecol Evol 16:646–655. https://doi.org/10.1016/S0169-5347(01)02283-2
Fiedler AK, Landis DA (2007) Plant characteristics associated with natural enemy abundance at Michigan native plants. Environ Entomol 36:878–886. https://doi.org/10.1093/ee/36.4.878
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 91:943–955
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. https://doi.org/10.1007/s13593-011-0036-y
Grettenberger IM, Tooker JF (2017) Variety mixtures of wheat influence aphid populations and attract an aphid predator. Arthr Plant Interact 11:133–146. https://doi.org/10.1007/s11829-016-9477-1
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. https://doi.org/10.1016/j.ecoleng.2016.10.080
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. https://doi.org/10.1007/s11829-017-9567-8
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. https://doi.org/10.14411/eje.2017.010
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. https://doi.org/10.1016/j.scitotenv.2017.11.296
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. https://doi.org/10.1007/s10530-010-9935-0
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. https://doi.org/10.1002/ps.4318
Institut Royal Météorologique (2014) Spring 2014. https://www.meteo.be/meteo/view/fr/14270142-Printemps+2014.html. Accessed 27 Sep 2018
Institut Royal Météorologique (2015) Spring 2015. https://www.meteo.be/meteo/view/fr/19891896-Printemps+2015.html. Accessed 27 Sep 2018
Jones CE, Buchmann SL (1974) Ultraviolet floral patterns as functional orientation cues in Hymenopterous pollination systems. Anim Behav 22:481–485. https://doi.org/10.1016/S0003-3472(74)80047-3
Jonsson M, Kaartinen R, Straub CS (2017) Relationships between natural enemy diversity and biological control. Curr Opin Insect Sci 20:1–6. https://doi.org/10.1016/j.cois.2017.01.001
Kattge J, Díaz S, Lavorel S et al (2011) TRY—a global database of plant traits. Glob Chang Biol 17:2905–2935. https://doi.org/10.1111/j.1365-2486.2011.02451.x
Kevan P, Giurfa M, Chittka L (1996) Why are there so many and so few white flowers? Trends Plant Sci 1:280–284. https://doi.org/10.1016/1360-1385(96)20008-1
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. https://doi.org/10.1007/s10340-016-0785-0
Kolz S, Kühn I, Durka W (2002) BIOLFLOR - Eine Datenbank zu biologisch-ökologischen Merkmalen der Gefäßpflanzen in Deutschland. Bundesamt für Naturschutz, Bonn
Koski MH, Ashman T-L (2014) Dissecting pollinator responses to a ubiquitous ultraviolet floral pattern in the wild. Funct Ecol 28:868–877. https://doi.org/10.1111/1365-2435.12242
Kral K, Stelzl M (1998) Daily visual sensitivity pattern in the green lacewing Chrysoperla carnea (Neuroptera: Chrysopidae). Eur J Entomol 95:327–333
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. https://cran.r-project.org/package=FD
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, Meise
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. https://doi.org/10.1016/j.biocontrol.2011.12.010
Lavorel S, Grigulis K, McIntyre S et al (2008) Assessing functional diversity in the field–methodology matters! Funct Ecol 22:134–147. https://doi.org/10.1111/j.1365-2435.2007.01339.x
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 40:573–592
Letourneau DK, Armbrecht I, Rivera BS et al (2011) Does plant diversity benefit agroecosystems? A synthetic review. Ecol Appl 21:9–21. https://doi.org/10.1890/09-2026.1
Lin J (1993) Identification of photoreceptor locations in the compound eye of Coccinella septempunctata Linnaeus (Coleoptera, Coccinellidae). J Insect Physiol 39:555–562. https://doi.org/10.1016/0022-1910(93)90037-R
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. https://doi.org/10.1002/ps.4332
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. https://doi.org/10.1111/1744-7917.12000
Lunau K (1992) A new interpretation of flower guide colouration: absorption of ultraviolet light enhances colour saturation. Plant Syst Evol 183:51–65. https://doi.org/10.1007/BF00937735
Lundgren JG (2009a) Relationships of natural enemies and non-prey foods. In: Brodeur J (Eds) Progress in biological control. Springer, Dordrecht
Lundgren JG (2009b) Nutritional aspects of non-prey foods in the life histories of predaceous Coccinellidae. Biol Control 51:294–305. https://doi.org/10.1016/j.biocontrol.2009.05.016
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. https://doi.org/10.14411/eje.2012.051
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 2:253–256
McGill BJ, Enquist BJ, Weiher E, Westoby M (2006) Rebuilding community ecology from functional traits. Trends Ecol Evol 21:178–185. https://doi.org/10.1016/j.tree.2006.02.002
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. https://doi.org/10.14411/eje.2000.071
Müller H (1881) Alpenblumen, ihre Befruchtung durch Insekten und ihre Anpassungen an dieselben. Wilhelm Engelmann, Leipzig
Nalepa CA (2013) Coccinellidae captured in blacklight traps: Seasonal and diel pattern of the dominant species Harmonia axyridis (Coleoptera: Coccinellidae). Eur J Entomol 110:593–597
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. https://doi.org/10.1017/S0007485315001091
Oksanen J, Guillaume Blanchet F, Kindt R et al (2015) Vegan: Community Ecology Package. R package
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. https://doi.org/10.1111/brv.12346
Pervez A, Omkar (2011) Ecology of aphidophagous ladybird Propylea species: a review. J Asia Pac Entomol 14:357–365. https://doi.org/10.1016/j.aspen.2011.01.001
R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
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. https://doi.org/10.14411/eje.2005.076
Roy HE, Adriaens T, Isaac NJB et al (2012) Invasive alien predator causes rapid declines of native European ladybirds. Divers Distrib 18:717–725. https://doi.org/10.1111/j.1472-4642.2012.00883.x
Roy HE, Brown PMJ, Comont RF et al (2013) Ladybirds. Pelagic Publishing, Exeter
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. https://doi.org/10.1016/j.agee.2016.01.039
San Martin G (2004) Clé de détermination des Chrysopidae de Belgique. Jeune et Nature asbl, Wavre
Silberglied RE (1979) Communication in the ultraviolet. Annu Rev Ecol Syst 10:373–398. https://doi.org/10.1146/annurev.es.10.110179.002105
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. https://doi.org/10.1653/024.100.0202
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. https://doi.org/10.1046/j.1570-7458.1999.00574.x
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. https://doi.org/10.1016/j.biocontrol.2018.02.015
Triltsch H (1999) Food remains in the guts of Coccinella septempunctata (Coleoptera: Coccinellidae) adults and larvae. Eur J Entomol 96:355–364
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. https://doi.org/10.1111/1365-2664.12653
Uyttenbroeck R, Hatt S, Piqueray J et al (2015) Creating perennial flower strips: think functional! Agric Agric Sci Procedia 6:95–101. https://doi.org/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
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. https://doi.org/10.1016/j.agee.2017.08.014
van Veen MP (2010) Hoverflies of Northwest Europe: identification keys to the Syrphidae. KNNV Publishing, Zeist
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. https://doi.org/10.1111/1365-2664.12605
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. https://doi.org/10.1016/j.biocontrol.2013.06.014
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. https://doi.org/10.1016/j.biocontrol.2006.06.003
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. https://doi.org/10.14411/eje.2005.078
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. https://doi.org/10.14411/eje.2006.104
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 139–165
Weber MG, Porturas LD, Keeler KH (2015) World list of plants with extrafloral nectaries. http://www.extrafloralnectaries.org. Accessed 20 Jun 2018
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. https://doi.org/10.1007/s00442-002-1128-9
Wratten SD, Gillespie M, Decourtye A et al (2012) Pollinator habitat enhancement: benefits to other ecosystem services. Agric Ecosyst Environ 159:112–122. https://doi.org/10.1016/j.agee.2012.06.020
Zhou J, Kuang R, Chen Z et al (2013) Phototactic behavior of Coccinella septempunctata L. (Coleoptera: Coccinellidae). Coleopt Bull 67:33–39. https://doi.org/10.1649/072.067.0108
Acknowledgements
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 (http://www.try-db.org) 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).
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Hatt, S., Uytenbroeck, R., Lopes, T. et al. Identification of flower functional traits affecting abundance of generalist predators in perennial multiple species wildflower strips. Arthropod-Plant Interactions 13, 127–137 (2019). https://doi.org/10.1007/s11829-018-9652-7
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DOI: https://doi.org/10.1007/s11829-018-9652-7