Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Landscape complexity and field margin vegetation diversity enhance natural enemies and reduce herbivory by Lepidoptera pests on tomato crop


Agricultural intensification may lead to higher pest pressure through the loss of natural plant assemblages, and associated reduction in natural enemy diversity, while providing increased crop area. We investigate the influence of field margin vegetation and landscape complexity on natural enemy diversity and crop damage caused by two Lepidoptera tomato pests (Tuta absoluta and Noctuidae). At the local scale, fields were bordered with herbaceous field margins of varying vegetation diversity. At the landscape scale, these fields were set in landscapes with increasing landscape complexity. Margin vegetation diversity was higher in landscapes with lower arable land cover, and was associated with increased floral resources and enemy diversity, with the latter being negatively related to T. absoluta-caused fruit injury. Total crop damage increased with arable land cover. These results imply that the suitability of farming practices for the conservation of natural enemies and pest control services is influenced by the landscape context.

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

Fig. 1
Fig. 2
Fig. 3


  1. Augustin S, Guichard S, Svatos A, Gilbert M (2004) Monitoring the regional spread of the invasive leafminer Cameraria ohridella (Lepidoptera: Gracillariidae) by damage assessment and pheromone trapping. Environ Entomol 33:1584–1592

  2. Baker WL, Cai Y (1992) The r.le programs for multiscale analysis of landscape structure using the GRASS geographical information system. Landsc Ecol 7:291–302

  3. 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

  4. Balzan MMV, 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

  5. 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

  6. 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

  7. Carlesi S, Bocci G, Moonen A, Frumento P, Bàrberi P (2013) Urban sprawl and land abandonment affect the functional response traits of maize weed communities in a heterogeneous landscape. Agric Ecosyst Environ 166:76–85

  8. 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

  9. Chaplin-Kramer R, Kremen C (2012) Pest control experiments show benefits of complexity at landscape and local scales. Ecol Appl 22:1936–1948

  10. Chaplin-Kramer R, O’Rourke ME, Blitzer EJ, Kremen C (2011) A meta-analysis of crop pest and natural enemy response to landscape complexity. Ecol Lett 14:922–932

  11. Core Team R (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

  12. Elmqvist T, Maltby E, Barker T, Mortimer M, Perrings C, Aronson J, De Groot R, Fitter A, Mace G, Norberg J, Pinto IS, Ring I (2010) Biodiversity, ecosystems and ecosystem services. In: Kumar P (ed) The economics of ecosystems and biodiversity. Earthscan, London and Washington, pp 41–104

  13. Fiedler AK, Landis D (2007) Plant characteristics associated with natural enemy abundance at Michigan native plants. Environ Entomol 36:878–886

  14. Finch S, Collier RH (2000) Host-plant selection by insects—a theory based on “appropriate/inappropriate landings” by pest insects of cruciferous plants. Entomol Exp Appl 96:91–102

  15. Finke DL, Denno R (2002) Intraguild predation diminished in complex-structured vegetation: implications for prey suppression. Ecology 83:643–652

  16. Fournier DA, Skaug HJ, Ancheta J, Ianelli J, Magnusson A, Maunder MN, Nielsen A, Sibert J (2012) AD model builder: using automatic differentiation for statistical inference of highly parameterized complex nonlinear models. Optim Methods Softw 27:233–249

  17. Gabriel D, Thies C, Tscharntke T (2005) Local diversity of arable weeds increases with landscape complexity. Perspect Plant Ecol Evol Syst 7:85–93

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

  19. 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

  20. Jonsson M, Buckley HL, Case BS, Wratten SD, Hale RJ, Didham RK (2012) Agricultural intensification drives landscape-context effects on host-parasitoid interactions in agroecosystems. J Appl Ecol 49:706–714

  21. Langellotto GA, Denno RF (2004) Responses of invertebrate natural enemies to complex-structured habitats: a meta-analytical synthesis. Oecologia 139:1–10

  22. Letourneau DK, Armbrecht I, Rivera BS, Lerma JM, Carmona EJ, Daza MC, Escobar S, Galindo V, Gutiérrez C, López SD, Mejía JL (2011) Does plant diversity benefit agroecosystems? A synthetic review. Ecol Appl 21:9–21

  23. Letourneau DK, Goldstein B (2001) Pest damage and arthropod community structure in organic vs. conventional tomato production in California. J Appl Ecol 38(3):557–570

  24. Martin EA, Reineking B, Seo B, Steffan-Dewenter I (2013) Natural enemy interactions constrain pest control in complex agricultural landscapes. Proc Natl Acad Sci USA 110:5534–5539

  25. Meehan TD, Werling BP, Landis DA, Gratton C (2011) Agricultural landscape simplification and insecticide use in the Midwestern United States. Proc Natl Acad Sci USA 108:11500–11505

  26. Memmott J (1999) The structure of a plant-pollinator food web. Ecol Lett 2(5):276–280

  27. Millar RB, Anderson MJ (2004) Remedies for pseudoreplication. Fish Res 70:397–407

  28. Oberski D (2014) Analysis of structural equation models. J Stat Softw 57:1–27

  29. Poveda K, Martinez E, Kersch-Becker M, Bonilla MA, Tscharntke T (2012) Landscape simplification and altitude affect biodiversity, herbivory and Andean potato yield. J Appl Ecol 49:513–522

  30. Ricci B, Franck P, Toubon J-F, Bouvier J-C, Sauphanor B, Lavigne C (2008) The influence of landscape on insect pest dynamics: a case study in southeastern France. Landsc Ecol 24(3):337–349

  31. Root R (1973) Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica oleracea). Ecol Monogr 43(1):95–124

  32. Rosseel Y (2012) lavaan: an R Package for structural equation. J Stat Softw 48:1–36

  33. Sarthou J-P, Badoz A, Vaissière B, Chevallier A, Rusch A (2014) Local more than landscape parameters structure natural enemy communities during their overwintering in semi-natural habitats. Agric Ecosyst Environ 194:17–28

  34. Satorra A, Bentler PM (2001) A scaled difference chi-square test statistic for moment structure analysis. Psychometrika 66:507–514

  35. Scalercio S, Brandmayr P, Iannotta N, Petacchi R, Boccaccio L (2012) Correlations between landscape attributes and ecological traits of Lepidoptera communities in olive groves. Eur J Entomol 109:207–216

  36. Shackelford G, Steward PR, Benton TG, Kunin WE, Potts SG, Biesmeijer JC, Sait SM (2013) Comparison of pollinators and natural enemies: a meta-analysis of landscape and local effects on abundance and richness in crops. Biol Rev CambPhilosSoc 88:1002–1021

  37. Skaug H, Fournier D, Nielsen A, Magnusson A, Bolker BM (2013) Generalized Linear Mixed Models using AD model builder. R package version 0.7.3

  38. Straub CS, Finke DL, Snyder WE (2008) Are the conservation of natural enemy biodiversity and biological control compatible goals? Biol Control 45:225–237

  39. Thies C, Roschewitz I, Tscharntke T (2005) The landscape context of cereal aphid–parasitoid interactions. Proc R Soc B Biol Sci 272:203–210

  40. Tscharntke T, Klein A-M, Kruess A, Steffan-Dewenter I, Thies C (2005) Landscape perspectives on agricultural intensification and biodiversity—ecosystem service management. Ecol Lett 8:857–874

  41. Tscharntke T, Bommarco R, Clough Y, Crist TO, Kleijn D, Rand TA, Tylianakis JM, van Nouhuys S, Vidal S (2007) Conservation biological control and enemy diversity on a landscape scale. Biol Control 43:294–309

  42. Veres A, Petit S, Conord C, Lavigne C (2013) Does landscape composition affect pest abundance and their control by natural enemies? A review. Agric Ecosyst Environ 166:110–117

  43. Vollhardt IMG, Tscharntke T, Wäckers FL, Bianchi FJ, Thies C (2008) Diversity of cereal aphid parasitoids in simple and complex landscapes. Agric Ecosyst Environ 126:289–292

  44. 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

  45. Wissinger SA (1997) Cyclic colonization in predictably ephemeral habitats: a template for biological control in annual crop systems. Biol Control 10:4–15

  46. 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

  47. Wright S (1934) The method of path coefficients. Ann Math Stat 5:161–215

  48. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York

Download references


We would like to thank Souzy Rouphael, Stefano Carlesi, Ruggero Petacchi and Levent Hançerli for their assistance during this study. We are thankful to Martin Entling (University of Koblenz-Landau, Germany) for comments on a previous version of the manuscript. We are very grateful to the farmers who allowed us to conduct this experiment in their fields. MVB received a PhD scholarship from the Scuola Superiore Sant’Anna within the International Doctoral Programme in Agrobiodiversity.

Author information

Correspondence to Mario V. Balzan.

Additional information

Handling Editor: Dirk Babendreier.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 1002 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Balzan, M.V., Bocci, G. & Moonen, A. Landscape complexity and field margin vegetation diversity enhance natural enemies and reduce herbivory by Lepidoptera pests on tomato crop. BioControl 61, 141–154 (2016). https://doi.org/10.1007/s10526-015-9711-2

Download citation


  • Conservation biological control
  • Landscape ecology
  • Multiple pest management
  • Noctuidae
  • Solanum lycopersicum
  • Tuta absoluta