Abstract
Sown wildflower strips are increasingly being established in Europe for enhancing arthropod conservation and the provision of ecosystem services, including biotic pollination and natural pest control. Here we use floral traits to identify different plant functional effect groups. Floral resources were provided in four experimental levels characterised by a cumulatively increasing flower trait diversity and vegetation stand complexity. The first level consisted of a bare control strip, whilst in each subsequent level three wildflower species with different functional traits were added (Level 0: control; Level 1: three Apiaceae species; Level 2: three Apiaceae and three Fabaceae species; Level 3: three Apiaceae, three Fabaceae species, and Centaurea jacea (Asteraceae), Fagopyrum esculentum (Polygonaceae), Sinapis alba (Brassicaceae)). Plots with sown wildflower strip mixtures were located adjacent to experimental plots of organically-managed tomato crop, which is attacked by multiple pests and partially relies on bees for fruit production, and hence dependent on the provision of pollination and pest control services. Results obtained here show that the inclusion of functionally diverse wildflower species was associated with an augmented availability of floral resources across time, and this increased the abundance of bees and anthocorids throughout the crop season. Several natural enemy groups, such as parasitoids, coccinelids and ground-dwelling predators, were not significantly enhanced by the inclusion of additional flower traits within the strips but the presence of flower resources was important to enhance their conservation in an arable cropping system.
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References
Accinelli G, Lazoni A, Ramilli F et al (2005) Trap crop: an agroecological approach to the management of Lygus rugulipennis on lettuce. Bull Insectol 58:9–14
Anderson A, Carnus T, Helden AJ et al (2013) The influence of conservation field margins in intensively managed grazing land on communities of five arthropod trophic groups. Insect Conserv Divers 6:201–211. doi:10.1111/j.1752-4598.2012.00203.x
Awan M, Wilson L, Hoffmann M (1990) Comparative biology of three geographic populations of Trissolcus basalis (Hymenoptera: Scelionidae). Environ Entomol 19:387–392
Baggen LR, Gurr GM (1998) The Influence of Food on Copidosoma koehleri (Hymenoptera: Encyrtidae), and the use of flowering plants as a habitat management tool to enhance biological control of potato moth, Phthorimaea operculella (Lepidoptera: Gelechiidae). Biol Control 11:9–17. doi:10.1006/bcon.1997.0566
Baggen LR, Gurr GM, Meats A (1999) Flowers in tri-trophic systems: mechanisms allowing selective exploitation by insect natural enemies for conservation biological control. Entomol Exp Appl 91:155–161
Balvanera P, Pfisterer AB, Buchmann N et al (2006) Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecol Lett 9:1146–1156. doi:10.1111/j.1461-0248.2006.00963.x
Balzan MV (2013) Conservation of vegetation and arthropod functional diversity for multi-pest suppression and enhanced crop yield in tomato cropping systems. Scuola Superiore di Studi Universitari e di Perfezionamento Sant’Anna, Pisa
Balzan MV, Moonen A-C (2012) Management strategies for the control of Tuta absoluta (Lepidoptera: Gelechiidae) damage in open-field cultivations of processing tomato in Tuscany (Italy). EPPO Bull 42:217–225. doi:10.1111/epp.2558
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 67:27–31
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
Bàrberi P, Moonen AC, Peruzzi A, Fontanelli M, Raffaelli M (2009) Weed suppression by soil steaming in combination with activating compounds. Weed Res 49:55–66
Bates D, Maechler M, Bolker BM (2013) lme4: linear mixed-effects models using S4 classes. R package version 0.999999-2
Bengtsson J (1998) Which species? What kind of diversity? Which ecosystem function? Some problems in studies of relations between biodiversity and ecosystem function. Appl Soil Ecol 10:191–199
Bensen TA, Temple SR (2008) Trap cropping, planting date, and cowpea variety as potential elements of an integrated pest management strategy for Lygus hesperus in blackeyed cowpea. Crop Prot 27:1343–1353. doi:10.1016/j.cropro.2008.05.002
Benton TG, Bryant DM, Cole LJ, Crick HQP (2002) Linking agricultural practice to insect and bird populations: a historical study over three decades. J Appl Ecol 39:673–687. doi:10.1046/j.1365-2664.2002.00745.x
Bianchi FJJA, Mikos V, Brussaard L et al (2013) Opportunities and limitations for functional agrobiodiversity in the European context. Environ Sci Policy 27:223–231. doi:10.1016/j.envsci.2012.12.014
Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information-theoretic approach. Springer, New York
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
Cardinale BJ, Srivastava DS, Duffy JE et al (2006) Effects of biodiversity on the functioning of trophic groups and ecosystems. Nature 443:989–992. doi:10.1038/nature05202
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
Cassman K, Wood S, Sze Choo P et al (2005) Cultivated Systems. In: Hassan R, Scholes R, Ash N (eds) Ecosystems and human well-being: current state and trends. Island Press, Washington, DC, pp 746–794
Chaney W (1998) Biological control of aphids in lettuce using in-field insectaries. In: Pickett CH, Bugg RL (eds) Enhancing biological control: habitat management to promote natural enemies of agricultural pests. The Regents of the University of California, California, pp 73–84
Chapin FS III, Zavaleta ES, Eviner VT et al (2000) Consequences of changing biodiversity. Nature 405:234–242. doi:10.1038/35012241
Cherry A, Cock M, Berg H, van den Kfir R (2003) Biological control of Helicoverpa armigera in Africa. In: Biological control in IPM systems in Africa. CAB International, Wallingford, UK, pp 329–346
Clarke K (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143
de Lange H, Lahr J, Brouwer J, Faber J (2012) Review of available evidence regarding the vulnerability of off-crop non- target arthropod communities in comparison to in-crop non-target. Support Publication 2012: EN-348
Desneux N, Wajnberg E, Wyckhuys KAG et al (2010) Biological invasion of European tomato crops by Tuta absoluta: ecology, geographic expansion and prospects for biological control. J Pest Sci 83:1–19. doi:10.1007/s10340-010-0321-6
Díaz S, Cabido M (2001) Vive la différence: plant functional diversity matters to ecosystem processes. Trends Ecol Evol 16:646–655
Duffy JE, Cardinale BJ, France KE et al (2007) The functional role of biodiversity in ecosystems: incorporating trophic complexity. Ecol Lett 10:522–538. doi:10.1111/j.1461-0248.2007.01037.x
Fiedler AK, Landis D (2007a) Plant characteristics associated with natural enemy abundance at michigan native plants. Environ Entomol 36:878–886
Fiedler AK, Landis DA (2007b) Attractiveness of michigan native plants to arthropod natural enemies and herbivores. Environ Entomol 36:751–765
Fiedler AK, Landis DA, Wratten SD (2008) Maximizing ecosystem services from conservation biological control: the role of habitat management. Biol Control 45:254–271. doi:10.1016/j.biocontrol.2007.12.009
Flint ML (1998) Integrated pest management for tomatoes, 4th edn. University of California, California
Gallai N, Salles J-M, Settele J, Vaissière BE (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol Econ 68:810–821. doi:10.1016/j.ecolecon.2008.06.014
Garibaldi LA, Aizen MA, Klein A-M et al (2011) Global growth and stability of agricultural yield decrease with pollinator dependence. Proc Natl Acad Sci USA 108:5909–5914. doi:10.1073/pnas.1012431108
Greenleaf SS, Kremen C (2006) Wild bee species increase tomato production and respond differently to surrounding land use in Northern California. Biol Conserv 133:81–87. doi:10.1016/j.biocon.2006.05.025
Gurr GM, Wratten SDSD, Luna JM (2003) Multi-function agricultural biodiversity: pest management and other benefits. Basic Appl Ecol 4:107–116
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
Hof AR, Bright PW (2010) The impact of grassy field margins on macro-invertebrate abundance in adjacent arable fields. Agric Ecosyst Environ 139:280–283. doi:10.1016/j.agee.2010.08.014
Hooper DU, Solan M, Symstad A et al (2002) Species diversity, functional diversity and ecosystem functioning. In: Loreau M, Naeem S, Inchausti P (eds) Biodiversity and ecosystem functioning: synthesis and perspectives. Oxford University Press, Oxford, pp 195–208
Hooper DU, Chapin FS III, Ewel J et al (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–35
Hummel R (2002) Effects of vegetable production system on epigeal arthropod populations. Agric Ecosyst Environ 93:177–188. doi:10.1016/S0167-8809(01)00346-2
Isbell F, Calcagno V, Hector A et al (2011) High plant diversity is needed to maintain ecosystem services. Nature 477:199–202. doi:10.1038/nature10282
Jervis MA, Kidd N, Fitton M et al (1993) Flower-visiting by hymenopteran parasitoids. J Nat Hist 27:67–105
Jolliffe P (2000) The replacement series. J Ecol 88:371–385
Kent M, Coker P (1995) Vegetation description and analysis: a practical approach. Wiley, Chichester
Klein A-M, Vaissière BE, Cane JH et al (2007) Importance of pollinators in changing landscapes for world crops. Proc Biol Sci 274:303–313. doi:10.1098/rspb.2006.3721
Korpela E-L, Hyvönen T, Lindgren S, Kuussaari M (2013) Can pollination services, species diversity and conservation be simultaneously promoted by sown wildflower strips on farmland? Agric Ecosyst Environ 179:18–24. doi:10.1016/j.agee.2013.07.001
Kremen C, Chaplin R (2007) Insects as providers of ecosystem services: crop pollination and pest control. In: Insect conservation biology: proceedings of the royal entomological society’s 23rd symposium, pp 349–382
Lange WH, Bronson L (1981) Insect pests of tomatoes. Annu Rev Entomol 26:345–371. doi:10.1146/annurev.en.26.010181.002021
Lange D, Fernandes WD, Raizer J, Faccenda O (2008) Predacious activity of ants (Hymenoptera: Formicidae) in conventional and in no-till. Agric Syst 51:1199–1207
Lavandero B, Wratten S, Didham R, Gurr GM (2006) Increasing floral diversity for selective enhancement of biological control agents: A double-edged sward? Basic Appl Ecol 7:236–243. doi:10.1016/j.baae.2005.09.004
Legendre P, Legendre L (1998) Numerical ecology, vol 2. Elsevier Science B.V, Amsterdam
Letourneau DK, Jedlicka JAJA, Bothwell SGSG, 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. doi:10.1146/annurev.ecolsys.110308.120320
Letourneau DK, Armbrecht I, Rivera BS et al (2011) Does plant diversity benefit agroecosystems? A synthetic review. Ecol Appl 21:9–21. doi:10.1890/09-2026.1
Loreau M, Hector A (2001) Partitioning selection and complementarity in biodiversity experiments. Nature 412:72–76. doi:10.1038/35083573
Loreau M, Naeem S, Inchausti P et al (2001) Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294:804–808. doi:10.1126/science.1064088
Mansfield S, Elias NV, Lytton-Hitchins JA (2003) Ants as egg predators of Helicoverpa armigera (Hubner)(Lepidoptera: Noctuidae) in Australian cotton crops. Aust J 42:349–351
Masetti A, Lanzoni A, Burgio G (2010) Effects of flowering plants on parasitism of lettuce leafminers (Diptera: Agromyzidae). Biol Control 54:263–269. doi:10.1016/j.biocontrol.2010.05.016
Meek B, Loxton D, Sparks T, Pywell R (2002) The effect of arable field margin composition on invertebrate biodiversity. Biol Conserv 106:259–271. doi:10.1016/S0006-3207(01)00252-X
Memmott J (1999) The structure of a plant-pollinator food web. Ecol Lett 2:276–280. doi:10.1046/j.1461-0248.1999.00087.x
Miñarro M, Prida E (2013) Hedgerows surrounding organic apple orchards in north-west Spain: potential to conserve beneficial insects. Agric For Entomol 15:382–390. doi:10.1111/afe.12025
Mizzel R, Riddle T, Blount A (2008) Trap cropping system to suppress stink bugs in the southern coastal plain. Proc Fla State Hortic Sci 121:377–382
Moonen A-C, Bàrberi P (2008) Functional biodiversity: an agroecosystem approach. Agric Ecosyst Environ 127:7–21. doi:10.1016/j.agee.2008.02.013
Naeem S, Thompson LJ, Lawler SP et al (1994) Declining biodiversity can alter the performance of ecosystem. Nature 368:734–737
Naeem S, Thompson LJ, Lawler SP et al (1995) Empirical evidence that declining species diversity may alter the performance of terrestrial ecosystems. Philos Trans R Soc B Biol Sci 347:249–262. doi:10.1098/rstb.1995.0025
Naeem S, Loreau M, Inchausti P (2002) Biodiversity and ecosystem functioning: the emergence of a synthetic ecological framework. In: Loreau M, Naeem S, Inchausti P (eds) Biodiversity and ecosystem functioning: synthesis and perspectives. Oxford University Press, Oxford, pp 3–17
Naylor RL, Ehrlich PR (1997) Natural pest control and agriculture. In: Daily GC (ed) Nature’s services: societal dependence on natural ecosystems. Island Press, Washington, pp 151–176
Nicholls CI, Altieri MA (2012) Plant biodiversity enhances bees and other insect pollinators in agroecosystems. Agron Sustain Dev, A review. doi:10.1007/s13593-012-0092-y
Noordijk J, Musters CJM, Dijk J, de Snoo GR (2010) Invertebrates in field margins: taxonomic group diversity and functional group abundance in relation to age. Biodivers Conserv 19:3255–3268. doi:10.1007/s10531-010-9890-1
Oksanen J, Guillaume Blanchet F, Kindt R, et al (2013) Vegan: community ecology package. R package version 2.0-7
Olesen JM, Dupont YL, Ehlers BK, Hansen DM (2007) The openness of a flower and its number of flower-visitor species. Taxon 56:729. doi:10.2307/25065857
Otieno M, Woodcock BA, Wilby A et al (2011) Local management and landscape drivers of pollination and biological control services in a Kenyan agro-ecosystem. Biol Conserv 144:2424–2431. doi:10.1016/j.biocon.2011.06.013
Pansa MG, Gutidone L, Tavella L (2012) Distribution and abundance of nymphal parasitoids of Lygus rugulipennis and Adelphocoris lineolatus in northwestern Italy. Bull Insectol 65:81–87
Petanidou T, Potts S (2006) Mutual use of resources in Mediterranean plant–pollinator communities: how specialized are pollination webs. In: Waser N, Ollerton J (eds) Plant–pollinator interact from specialisation to generalisation. The University of Chicago Press, Chicago, pp 221–244
Pisani Gareau TL, Letourneau DK, Shennan C (2013) Relative densities of natural enemy and pest insects within California hedgerows. Environ Entomol 42:688–702. doi:10.1603/EN12317
Pullin A (1997) The challenge of insect conservation. J Insect Conserv 1:1–4
Rea JH, Wratten SD, Sedcole R et al (2002) Trap cropping to manage green vegetable bug Nezara viridula (L.) (Heteroptera: Pentatomidae) in sweet corn in New Zealand. Agric For Entomol 4:101–107. doi:10.1046/j.1461-9563.2002.00130.x
Rollin O, Bretagnolle V, Decourtye A et al (2013) Differences of floral resource use between honey bees and wild bees in an intensive farming system. Agric Ecosyst Environ 179:78–86. doi:10.1016/j.agee.2013.07.007
Rosa García R, Miñarro M (2014) Role of floral resources in the conservation of pollinator communities in cider-apple orchards. Agric Ecosyst Environ 183:118–126. doi:10.1016/j.agee.2013.10.017
Samways MJ (2007) Insect conservation: a synthetic management approach. Annu Entomol Rev 52:465–487
Schwartz MW, Brigham CA, Hoeksema JD et al (2000) Linking biodiversity to ecosystem function: implications for conservation ecology. Oecologia 122:297–305. doi:10.1007/s004420050035
Shackelford G, Steward PR, Benton TG et al (2013) Comparison of pollinators and natural enemies: a meta-analysis of landscape and local effects on abundance and richness in crops. Biol Rev Camb Philos Soc. doi:10.1111/brv.12040
Skirvin DJ, Kravar-Garde L, Reynolds K et al (2011) The effect of within-crop habitat manipulations on the conservation biological control of aphids in field-grown lettuce. Bull Entomol Res 101:623–631. doi:10.1017/S0007485310000659
Smith JF, Luttrell RG, Greene JK, Tingle C (2009) Early-season soybean as a trap crop for stink bugs (Heteroptera: Pentatomidae) in Arkansas’ changing system of soybean production. Environ Entomol 38:450–458
Swezey SL, Nieto DJ, Bryer JA (2007) Control of western tarnished plant bug Lygus hesperus Knight (Hemiptera: Miridae) in California organic strawberries using alfalfa trap crops and tractor-mounted vacuums. Environ Entomol 36:1457–1465
Thomas CFG, Marshall EJP (1999) Arthropod abundance and diversity in differently vegetated margins of arable fields. Agric Ecosyst Environ 72:131–144. doi:10.1016/S0167-8809(98)00169-8
Tillman PG (2006) Susceptibility of pest Nezara viridula (Heteroptera: Pentatomidae) and parasitoid Trichopoda pennipes (Diptera: Tachinidae) to selected insecticides. J Econ Entomol 99:648–657
Tilman D, Wedin D, Knops J (1996) Productivity and sustainability influenced by biodiversity in grassland ecosystems. Nature 379:718–720
Tscharntke T, Tylianakis JM, Wade MR et al (2007) Insect conservation in agricultural landscapes. In: Stewart A, New TR, Lewis O (eds) Insect conservation biology: proceedings of the royal entomological society's 23rd symposium. CABI, Oxford, pp 383–404
Van den Berg H (1993) Natural control of Helicoverpa armigera in smallholder crops in east Africa. PhD thesis, Wageningen University, The Netherlands
Van den Berg H, Cock M (1993) Stage-specific mortality of Helicoverpa armigera in three smallholder crops in Kenya. J Appl Ecol 30:640–653
van Rijn PCJ, van Alebeek F, den Belder E, Wäckers FL, Buurma J, Willemse J, van Gurp H (2008) Functional agro biodiversity in Dutch arable farming: results of a three year pilot. IOBC/WPRS Bull 34:125–128
Vattala H, Wratten S, Phillips C, Wackers FL (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
Wäckers FL (2005) Suitability of (extra-) floral nectar, pollen, and honeydew as insect food sources. Plant-provided food carnivorous insects a protective mutualism and its applications. Cambridge University Press, Cambridge, pp 17–74
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 (eds) Biodiversity and insect pests: key issues for sustainable management. Wiley, Chichester, pp 139–165
Watmough RH, Kfir R (1995) Predation on pupae of Helicoverpa armigera Hbn. (Lep., Noctuidae) and its relation to stem borer numbers in summer grain crops. J Appl Entomol 119:679–688. doi:10.1111/j.1439-0418.1995.tb01358.x
Winkler K, Wäckers F, Bukovinszkine-Kiss G, van Lenteren J (2006) Sugar resources are vital for Diadegma semiclausum fecundity under field conditions. Basic Appl Ecol 7:133–140. doi:10.1016/j.baae.2005.06.001
Winkler K, Wäckers FL, Kaufman LV et al (2009) Nectar exploitation by herbivores and their parasitoids is a function of flower species and relative humidity. Biol Control 50:299–306. doi:10.1016/j.biocontrol.2009.04.009
Woltz JM, Isaacs R, Landis DA (2012) Landscape structure and habitat management differentially influence insect natural enemies in an agricultural landscape. Agric Ecosyst Environ 152:40–49. doi:10.1016/j.agee.2012.02.008
Wratten SD, Gillespie M, Decourtye A et al (2012) Pollinator habitat enhancement: benefits to other ecosystem services. Agric Ecosyst Environ 159:112–122. doi:10.1016/j.agee.2012.06.020
Yardim E, Edwards C (2002) Effects of weed control practices on surface-dwelling arthropod predators in tomato agroecosystems. Phytoparasitica 30:379–386
Acknowledgments
This research study is supported by the European Commission FP7 collaborative project “Strategies for Organic and Low-input Integrated Breeding and Management (SOLIBAM–FP7–KBBE No. 245058)”. The authors are grateful to Giacomo Nardi (SSSUP) for technical field assistance, Ruggero Petacchi (SSSUP) for assistance in the lab and Paolo Bàrberi (SSSUP) who is responsible for the Agroecology group activities under the FP7 project SOLIBAM. We are also grateful to the staff of the Interdepartmental Centre for Agroenvironmental Research ‘E. Avanzi’ of the University of Pisa for their technical assistance.
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Balzan, M.V., Bocci, G. & Moonen, AC. 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 (2014). https://doi.org/10.1007/s10841-014-9680-2
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DOI: https://doi.org/10.1007/s10841-014-9680-2