Skip to main content

Advertisement

Log in

Flowering banker plants for the delivery of multiple agroecosystem services

  • Original Paper
  • Published:
Arthropod-Plant Interactions Aims and scope Submit manuscript

Abstract

Ecosystem services provided by agricultural ecosystems include natural pest control and pollination, and these are important to ensure crop productivity. This study investigates the use of the banker plant Calendula officinalis L. to provide multiple ecosystem services by increasing the abundance of natural enemies for biological control of tomato pests, providing forage resources to wild bees, and improving crop yield. C. officinalis was selected for this experiment as it is used as a banker plant for Dicyphini (Hemiptera: Miridae) predators. Strips of flowering C. officinalis were established in the field edges of tomato fields and arthropod visitation to C. officinalis strips and tomato was measured. Crop damage from multiple pests of tomato was assessed in fields with C. officinalis strips and control sites. The contribution of pollination to crop yield was assessed through a pollinator exclusion experiment. The inclusion of C. officinalis in tomato fields was associated with increased abundance of Dicyphini, parasitoids, bees and other arthropod groups within these strips. A reduction in the total leaf crop damage from Lepidoptera pests was recorded in fields with C. officinalis strips. Increased fruit set and biomass were recorded in open-pollinated tomato but this was not significantly different between control and C. officinalis fields. Results presented here demonstrate that the inclusion of a companion plant can improve the conservation of beneficial arthropods and the delivery of agroecosystem services but efficacy is likely to be improved with the addition of plants, with different functional traits, and with improved attractiveness to crop pollinators.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abian YVF, Andau NAS, Ruggisser ODTB et al (2014) Plant diversity in a nutshell: testing for small-scale effects on trap nesting wild bees and wasps. Ecosphere 5:18. doi:10.1890/ES13-00375.1

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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. doi:10.1007/s10841-014-9680-2

    Google Scholar 

  • Balzan MV, Bocci G, Moonen A-C (2016a) Landscape complexity and field margin vegetation diversity enhance natural enemies and reduce herbivory by Lepidoptera pests on tomato crop. Biocontrol 61:141–154

    Article  Google Scholar 

  • Balzan MV, Bocci G, Moonen A (2016b) Utilisation of plant functional diversity in wild flower strips for the delivery of multiple agroecosystem services. Entomol Exp Appl 158:304–319

    Article  Google Scholar 

  • Bartomeus I, Potts SG, Steffan-Dewenter I et al (2014) Contribution of insect pollinators to crop yield and quality varies with agricultural intensification. PeerJ 2:e328

    Article  PubMed  PubMed Central  Google Scholar 

  • Bennett EM, Peterson GD, Gordon LJ (2009) Understanding relationships among multiple ecosystem services. Ecol Lett 12:1394–1404. doi:10.1111/j.1461-0248.2009.01387.x

    Article  PubMed  Google Scholar 

  • Bianchi FJJA, Booji CJH, Tscharntke T (2006) Sustainable pest regulation in agricultural landscapes: a review on landscape composition, biodiversity and natural pest control. Proc R Soc Lond B 273:1715–1727

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Biondi A, Zappalà L, Di Mauro A et al (2015) Can alternative host plant and prey affect phytophagy and biological control by the zoophytophagous mirid Nesidiocoris tenuis? Biocontrol. doi:10.1007/s10526-015-9700-5

    Google Scholar 

  • Blaauw BR, Isaacs R (2014) Flower plantings increase wild bee abundance and the pollination services provided to a pollination-dependent crop. J Appl Ecol 51:890–898. doi:10.1111/1365-2664.12257

    Article  Google Scholar 

  • Bommarco R, Kleijn D, Potts SG (2013) Ecological intensification: harnessing ecosystem services for food security. Trends Ecol Evol 28:230–238. doi:10.1016/j.tree.2012.10.012

    Article  PubMed  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information-theoretic approach. Springer, New York

    Google Scholar 

  • Calvo F, Lorente M, Stansly P (2012) Preplant release of Nesidiocoris tenuis and supplementary tactics for control of Tuta absoluta and Bemisa tabaci in greenhouse tomato. Entomol Exp Appl 142:111–119. doi:10.1111/j.1570-7458.2012.01238.x

    Article  Google Scholar 

  • Carreck NL, Williams IH (2002) Food for insect pollinators on farmland: insect visits to flowers of annual seed mixtures. J Insect Conserv 6:13–23. doi:10.1023/a:1015764925536

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Carvalheiro LG, Seymour CL, Nicolson SW, Veldtman R (2012) Creating patches of native flowers facilitates crop pollination in large agricultural fields: mango as a case study. J Appl Ecol 49:1373–1383. doi:10.1111/j.1365-2664.2012.02217.x

    Article  Google Scholar 

  • Castañé C, Arnó J, Gabarra R, Alomar O (2011) Plant damage to vegetable crops by zoophytophagous mirid predators. Biol Control 59:22–29. doi:10.1016/j.biocontrol.2011.03.007

    Article  Google Scholar 

  • Chailleux A, Bearez P, Pizzol J et al (2013) Potential for combined use of parasitoids and generalist predators for biological control of the key invasive tomato pest Tuta absoluta. J Pest Sci 86:533–541. doi:10.1007/s10340-013-0498-6

    Article  Google Scholar 

  • Classen A, Peters MK, Ferger SW et al (2014) Complementary ecosystem services provided by pest predators and pollinators increase quantity and quality of coffee yields. Proc Biol Sci 281:20133148

    Article  PubMed  PubMed Central  Google Scholar 

  • Colley MR, Luna JM (2000) Relative attractiveness of potential beneficial insectary plants to aphidophagous hoverflies (Diptera: syrphidae). Environ Entomol 29:1054–1059. doi:10.1603/0046-225X-29.5.1054

    Article  Google Scholar 

  • Corbet SA, Bee J, Dasmahapatra K et al (2001) Native or exotic? Double or single? Evaluating plants for pollinator-friendly gardens. Ann Bot 87:219. doi:10.1006/anbo.2000.1322

    Article  Google Scholar 

  • Dandria D, Catania A (2009) Tuta absoluta (Povolny, 1994), an important agricultural pest in Malta. Gelechiidae, Lepidoptera

    Google Scholar 

  • 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

    Article  Google Scholar 

  • FAO (2006) Malta water resources review. Food and Agriculture Organization, Rome

    Google Scholar 

  • Foley JA, Ramankutty N, Brauman KA et al (2011) Solutions for a cultivated planet. Nature 478:337–342

    Article  CAS  PubMed  Google Scholar 

  • Fournier DA, Skaug HJ, Ancheta J et al (2012) AD Model Builder: using automatic differentiation for statistical inference of highly parameterized complex nonlinear models. Optim Methods Softw 27:233–249. doi:10.1080/10556788.2011.597854

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Goslee SC, Urban DL (2007) The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw 22:1–19

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Grez A, Zaviezo T, Gardiner M (2014) Local predator composition and landscape affects biological control of aphids in alfalfa fields. Biol Control 76:1–9

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biometrical J 50:346–363

    Article  Google Scholar 

  • Huallacháin DÓ, Anderson A, Fritch R et al (2014) Field margins: a comparison of establishment methods and effects on hymenopteran parasitoid communities. Insect Conserv Divers 7:289–307. doi:10.1111/icad.12053

    Article  Google Scholar 

  • Huang N, Enkegaard A (2011) The banker plant method in biological control. CRC Crit Rev Plant Sci 30:259–278

    Article  Google Scholar 

  • Ingegno BL, Pansa MG, Tavella L (2011) Plant preference in the zoophytophagous generalist predator Macrolophus pygmaeus (Heteroptera: Miridae). Biol Control. doi:10.1016/j.biocontrol.2011.06.003

    Google Scholar 

  • Iverson AL, Marín LE, Ennis KK et al (2014) Do polycultures promote win-wins or trade-offs in agricultural ecosystem services? A meta-analysis. J Appl Ecol 51:1593–1602. doi:10.1111/1365-2664.12334

    Article  Google Scholar 

  • Jonsson M, Wratten SD, Landis DA, Gurr GM (2008) Recent advances in conservation biological control of arthropods by arthropods. Biol Control 45:172–175. doi:10.1016/j.biocontrol.2008.01.006

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Lambion J (2011) Functional biodiversity in Southern France: a method to enhance predatory mirid bug populations. Acta Hortic 915:165–170

    Article  Google Scholar 

  • Lambion J (2014) Flower strips as winter shelters for predatory miridae bugs. Acta Hortic 1041:149–156

    Article  Google Scholar 

  • Lange WH, Bronson L (1981) Insect pests of tomatoes. Annu Rev Entomol 26:345–371. doi:10.1146/annurev.en.26.010181.002021

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Maes J, Paracchini ML, Zulian G (2011) A European assessment of the provision of ecosystem services: towards an atlas of ecosystem services. Joint Research Centre, JRC Scientific and Technical Reports No EUR 24750 EN—2011, Publications Office of the European Union

  • Maselou DA, Perdikis DC, Sabelis MW, Fantinou AA (2015) Plant resources as a factor altering emergent multi-predator effects. PLoS ONE 10:e0138764. doi:10.1371/journal.pone.0138764

    Article  PubMed  PubMed Central  Google Scholar 

  • Mifsud D, Mangion M, Azzopardi E et al (2011) Aphids associated with shrubs, herbaceous plants and crops in the Maltese Archipelago. Bulletin of the Entomological Society of Malta 4:5–53

    Google Scholar 

  • 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

    Google Scholar 

  • Nicholls CI, Altieri MA (2013) Plant biodiversity enhances bees and other insect pollinators in agroecosystems. A review. Agron Sustain Dev 33:257–274. doi:10.1007/s13593-012-0092

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Perdikis D, Lucas E, Garantonakis N et al (2014) Intraguild predation and sublethal interactions between two zoophytophagous mirids, Macrolophus pygmaeus and Nesidiocoris tenuis. Biol Control 70:35–41. doi:10.1016/j.biocontrol.2013.12.003

    Article  Google Scholar 

  • Pereira ALC, Taques TC, Valim JOS et al (2015) The management of bee communities by intercropping with flowering basil (Ocimum basilicum) enhances pollination and yield of bell pepper (Capsicum annuum). J Insect Conserv 19:479–486. doi:10.1007/s10841-015-9768-3

    Article  Google Scholar 

  • R Core Team (2015) R: a language and environment for statistical computing

  • 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

    Article  Google Scholar 

  • Saliba L (1963) Insect pests of crop plants in the Maltese Islands. Department of Agriculture, Malta

    Google Scholar 

  • Sanchez JA (2009) Density thresholds for Nesidiocoris tenuis (Heteroptera: Miridae) in tomato crops. Biol Control 51:493–498. doi:10.1016/j.biocontrol.2009.09.006

    Article  Google Scholar 

  • Sanchez JA, La-Spina M, Lacasa A (2014) Numerical response of Nesidiocoris tenuis (Hemiptera: Miridae) preying on Tuta absoluta (Lepidoptera: Gelechiidae) in tomato crops. Eur J Entomol 111:1–9. doi:10.14411/eje.2014.041

    Article  Google Scholar 

  • Scheper J, Holzschuh A, Kuussaari M et al (2013) Environmental factors driving the effectiveness of European agri-environmental measures in mitigating pollinator loss—a meta-analysis. Ecol Lett 16:912–920. doi:10.1111/ele.12128

    Article  PubMed  Google Scholar 

  • 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 88:1002–1021

    Article  PubMed  Google Scholar 

  • Skaug H, Fournier D, Nielsen A, et al. (2013) Generalized linear mixed models using AD Model Builder. R package version 0.7.3

  • Storkey J, Döring T, Baddeley J et al (2015) Engineering a plant community to deliver multiple ecosystem services. Ecol Appl 25:1034–1043

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Urbaneja A, Tapia G, Stansly P (2005) Influence of host plant and prey availability on developmental time and surviorship of Nesidiocoris tenius (Het.: Miridae). Biocontrol Sci Technol 15:513–518. doi:10.1080/09583150500088777

    Article  Google Scholar 

  • Wäckers FL, van Rijn PCJ (2005) Food for protection: an introduction. In: van Rijn PCJ, Wäckers FL, Bruin J (eds) Plant-provided food for carnivorous insects: a protective mutualism and its applications. Cambridge University Press, Cambridge, pp 1–14

    Chapter  Google Scholar 

  • 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

    Article  Google Scholar 

  • Zappala L, Biondi A, Alma A, Al-Jboory I (2013) Natural enemies of the South American moth, Tuta absoluta, in Europe, North Africa and Middle East, and their potential use in pest control strategies. J Pest Sci. doi:10.1007/s10340-013-0531-9

    Google Scholar 

  • Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Statistics for biology and health. Springer-Verlag, New York

    Book  Google Scholar 

Download references

Acknowledgements

I would like to thank Deryn Haidon, Rowena Calleja and Mario Ellul (Institute of Applied Sciences, MCAST) and Joseph Borg, Darren Borg and the staff of the Għammieri Experimental Farm (Ministry for Sustainable Development, the Environment and Climate Change), for their technical assistance. I am grateful to Barbara L. Ingegno and Luciana Tavella (Università degli Studi di Torino) for the identification of the Dicyphini. Grateful thanks to two anonymous reviewers for comments and suggestions.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mario V. Balzan.

Additional information

Handling Editor: Robert Glinwood.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 149 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Balzan, M.V. Flowering banker plants for the delivery of multiple agroecosystem services. Arthropod-Plant Interactions 11, 743–754 (2017). https://doi.org/10.1007/s11829-017-9544-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11829-017-9544-2

Keywords

Navigation