Effects of shrub crop interplanting on apple pest ecology in a temperate agroforestry system

Abstract

Pest control by wild arthropods is an important ecosystem service in fruit crops, especially due to markets that value minimal pesticide use. Techniques to augment on-farm habitat for wild arthropods have focused on flowering ground cover planted within orchards and hedgerows on field borders. However, natural enemies found in groundcover often do not favor tree canopy habitat. Conversely, while hedgerows can effectively provide natural enemies that prefer woody microhabitats, their impact diminishes away from field edges. Shrub crops interplanted within orchards could resolve both problems, providing woody habitat for natural enemies directly adjacent to target crop trees. In a multi-layer agroforestry system in Illinois, we vacuum sampled arthropod communities across layers and recorded vegetation characteristics and pest damage on apples. Using generalized linear models, information theoretic model selection, and non-metric multidimensional scaling, we evaluated the effects of three shrub treatments (raspberries, hazelnuts, and both species) on pest and natural enemy guilds in apple trees and shrubs, and on the frequency of pest damage on apples. Shrub composition was an important predictor of arthropod communities on shrubs. However, shrub treatment had only minor impacts on arthropods in apple canopies, indicating the habitats are less similar than anticipated. While two arthropod guilds in apple canopies were linked to pest damage frequency, neither was sensitive to changes in the shrub layer. Results suggest that shrub crop interplanting does not inherently resolve the ecological complexities that impede existing approaches in conservation biological control.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Anderson DR (2007) Model based inference in the life sciences: a primer on evidence. Springer Science & Business Media, New York

    Google Scholar 

  2. Arnault I (2016) Foliar application of microdoses of sucrose to reduce codling moth Cydia pomonella L. (Lepidoptera: Tortricidae) damage to apple trees. Pest Manag Sci 72:1901–1909

    Article  CAS  PubMed  Google Scholar 

  3. Begg GS et al (2016) A functional overview of conservation biological control. Crop Protect 97:145–158

    Article  Google Scholar 

  4. Bolker B, Team R (2010) bbmle: Tools for general maximum likelihood estimation R package version 09 5

  5. Bortolotto O et al (2016) Distance from the edge of forest fragments influence the abundance of aphidophagous hoverflies (Diptera: Syrphidae) in wheat fields. Acta Sci Agron 38:157–164

    Article  Google Scholar 

  6. Brose U (2003) Bottom-up control of carabid beetle communities in early successional wetlands: mediated by vegetation structure or plant diversity? Oecologia 135:407–413

    Article  CAS  PubMed  Google Scholar 

  7. Brown M, Glenn D (1999) Ground cover plants and selective insecticides as pest management tools in apple orchards. J Econ Entomol 92:899–905

    Article  Google Scholar 

  8. Brown M, Mathews C (2007) Conservation biological control of rosy apple aphid, Dysaphis plantaginea (Passerini), in eastern North America.”. Environ Entomol 36:1131–1139

    Article  CAS  PubMed  Google Scholar 

  9. Bugg RL, Waddington C (1994) Using cover crops to manage arthropod pests of orchards: a review Agric. Ecosyst Environ 50:11–28

    Article  Google Scholar 

  10. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information–theoretic approach. Springer Science & Business Media, New York

    Google Scholar 

  11. Calabuig A, Garcia-Marí F, Pekas A (2015) Ants in citrus: impact on the abundance, species richness, diversity and community structure of predators and parasitoids. Agric Ecosyst Environ 213:178–185

    Article  Google Scholar 

  12. Coli WM, Ciurlino RA, Hosmer T (1994) Effect of understory and border vegetation composition on phytophagous and predatory mites in Massachusetts commercial apple orchards. Agric Ecosyst Environ 50:49–60

    Article  Google Scholar 

  13. Daubenmire R (1959) A canopy-coverage method of vegetational analysis. Northwest Sci 33:43–64

    Google Scholar 

  14. Debras J-F, Senoussi R, Rieux R, Buisson E, Dutoit T (2008) Spatial distribution of an arthropod community in a pear orchard (southern France): identification of a hedge effect. Agric Ecosyst Environ 127:166–176

    Article  Google Scholar 

  15. Denno RF, Peterson MA (2000) Caught between the devil and the deep blue sea, mobile planthoppers elude natural enemies and deteriorating host plants. Am Entomol 46:95–109

    Article  Google Scholar 

  16. Denno RF, Gratton C, Peterson MA, Langellotto GA, Finke DL, Huberty AF (2002) Bottom-up forces mediate natural-enemy impact in a phytophagous insect community. Ecology 83:1443–1458

    Article  Google Scholar 

  17. Dong J et al (2005) Evaluation of the Lucerne cover crop for improving biological control of Lyonetia clerkella (Lepidoptera: Lyonetiidae) by means of augmenting its predators in peach orchards. Great Lakes Entomol 28:186–199

    Google Scholar 

  18. Eilers EJ, Klein A-M (2009) Landscape context and management effects on an important insect pest and its natural enemies in almond. Biol Control 51:388–394

    Article  Google Scholar 

  19. Erlandson LW, Obrycki JJ (2010) Predation of immature and adult Empoasca fabae (Harris)(Hemiptera: Cicadellidae) by three species of predatory insects. J Kans Entomol Soc 83:1–6

    Article  Google Scholar 

  20. Fréchette B, Cormier D, Chouinard G, Vanoosthuyse F, Lucas E (2008) Apple aphid, Aphis spp. (Hemiptera: Aphididae), and predator populations in an apple orchard at the non-bearing stage: the impact of ground cover and cultivar Eur. J Entomol 105:521

    Google Scholar 

  21. Gareau TLP, Letourneau DK, Shennan C (2013) Relative densities of natural enemy and pest insects within California hedgerows. Environ Entomol 42:688–702

    Article  PubMed  Google Scholar 

  22. Grettenberger IM, Tooker JF (2016) Variety mixtures of wheat influence aphid populations and attract an aphid predator. Arthropod Plant Interact 11:133–146

    Article  Google Scholar 

  23. Haddad NM, Tilman D, Haarstad J, Ritchie M, Knops JM (2001) Contrasting effects of plant richness and composition on insect communities: a field experiment. Am Nat 158:17–35

    Article  CAS  PubMed  Google Scholar 

  24. Horton DR, Jones VP, Unruh TR (2009) Use of a new immunomarking method to assess movement by generalist predators between a cover crop and tree canopy in a pear orchard. Am Entomol 55:49–56

    Article  Google Scholar 

  25. Janssen A, Sabelis MW, Magalhães S, Montserrat M, Van der Hammen T (2007) Habitat structure affects intraguild predation. Ecology 88:2713–2719

    Article  PubMed  Google Scholar 

  26. Knops JM et al (1999) Effects of plant species richness on invasion dynamics, disease outbreaks, insect abundances and diversity. Ecol Lett 2:286–293

    Article  Google Scholar 

  27. Koricheva J, Mulder CP, Schmid B, Joshi J, Huss-Danell K (2000) Numerical responses of different trophic groups of invertebrates to manipulations of plant diversity in grasslands. Oecologia 125:271–282

    Article  PubMed  Google Scholar 

  28. Lamp WO, Nielsen GR, Danielson SD (1994) Patterns among host plants of potato leafhopper, Empoasca fabae (Homoptera: Cicadellidae). J Kans Entomol Soc 67:354–368

    Google Scholar 

  29. Landis DA, Wratten SD, Gurr GM (2000) Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu Rev Entomol 45:175–201

    Article  CAS  PubMed  Google Scholar 

  30. Lenth RV, Hervé M (2013) lsmeans: Least-squares means R package version 2:11

  31. Letourneau DK et al (2011) Does plant diversity benefit agroecosystems? A synthetic review. Ecol Appl 21:9–21

    Article  PubMed  Google Scholar 

  32. Lovell ST, Dupraz C, Gold M, Jose S, Revord R, Stanek E, Wolz KJ (2017) Temperate agroforestry research: considering multifunctional woody polycultures and the design of long-term field trials. Agrofor Syst. https://doi.org/10.1007/s10457-017-0087-4

    Article  Google Scholar 

  33. Madsen HF, Jack ID (1966) The relation of thrips to pansy spot on apples. Can Entomol 98:903–908

    Article  Google Scholar 

  34. Markó V, Jenser G, Mihályi K, Hegyi T, Balázs K (2012) Flowers for better pest control? Effects of apple orchard groundcover management on mites (Acari), leafminers (Lepidoptera, Scitellidae), and fruit pest. Biocontrol Sci Technol 22:39–60

    Article  Google Scholar 

  35. Miliczky E et al (2007) Spatial patterns of western flower thrips (Thysanoptera: Thripidae) in apple orchards and associated fruit damage. J Entomol Soc B. C. 104:25–34

    Google Scholar 

  36. Morandin L, Long R, Pease C, Kremen C (2011) Hedgerows enhance beneficial insects on farms in California’s Central Valley. Calif Agric 65:197–201

    Article  Google Scholar 

  37. Oksanen J, Kindt R, Legendre P, O’Hara B, Stevens MHH, Oksanen MJ, Suggests M (2007) The vegan package. Commun Ecol Packag 10:631–637

    Google Scholar 

  38. Otte D (1976) Species richness patterns of New World desert grasshoppers in relation to plant diversity. J Biogeogr 3:197–209

    Article  Google Scholar 

  39. Paredes D, Cayuela L, Campos M (2013) Synergistic effects of ground cover and adjacent vegetation on natural enemies of olive insect pests. Agric Ecosyst Environ 173:72–80

    Article  Google Scholar 

  40. Paredes D, Cayuela L, Gurr GM, Campos M (2015) Is ground cover vegetation an effective biological control enhancement strategy against olive pests? PLoS ONE 10:e0117265

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. R Core Team (2016) A language and environment for statistical computing. R Foundation for statistical computing, 2015; Vienna, Austria

  42. Rieux R, Simon S, Defrance H (1999) Role of hedgerows and ground cover management on arthropod populations in pear orchards. Agric Ecosyst Env 73:119–127

    Article  Google Scholar 

  43. Russell EP (1989) Enemies hypothesis: a review of the effect of vegetational diversity on predatory insects and parasitoids. Env Entomol 18:590–599

    Article  Google Scholar 

  44. Sigsgaard L et al (2017) Mass release of Trichogramma evanescens and T cacoeciae can reduce damage by the apple codling moth Cydia pomonella in organic orchards under pheromone disruption. Insects 8:41

    Article  PubMed Central  Google Scholar 

  45. Silva E, Franco J, Vasconcelos T, Branco M (2010) Effect of ground cover vegetation on the abundance and diversity of beneficial arthropods in citrus orchards. Bull Entomol Res 100:489–499

    Article  CAS  PubMed  Google Scholar 

  46. Simon S, Bouvier J-C, Debras J-F, Sauphanor B (2010) Biodiversity and pest management in orchard systems. A review. Agron Sustain Dev 30:139–152

    Article  Google Scholar 

  47. Stewart AJ, Wright AF (1995) A new inexpensive suction apparatus for sampling arthropods in grassland. Ecol Entomol 20:98–102

    Article  Google Scholar 

  48. Straub CS et al (2013) Influence of nonhost plant diversity and natural enemies on the potato leafhopper, Empoasca fabae, and pea aphid, Acyrthosiphon pisum, in alfalfa. J Pest Sci 86:235–244

    Article  Google Scholar 

  49. Tscharntke T et al (2016) When natural habitat fails to enhance biological pest control—Five hypotheses. Biol Conserv 204:449–458

    Article  Google Scholar 

  50. Tuovinen T (1994) Influence of surrounding trees and bushes on the phytoseiid mite fauna on apple orchard trees in Finland Agric. Ecosyst Environ 50:39–47

    Article  Google Scholar 

  51. Unruh TR, Pfannenstiel RS, Peters C, Brunner JF, Jones VP (2012) Parasitism of leafrollers in Washington fruit orchards is enhanced by perimeter plantings of rose and strawberry. Biol Control 62:162–172

    Article  Google Scholar 

  52. Venables WN, Ripley BD (2013) Modern applied statistics with S-PLUS. Springer Science & Business Media, New York

    Google Scholar 

  53. Wilson S, Smith J, Purcell A III (1993) An inexpensive vacuum collector for insect sampling. Entomol News 104:203–208

    Google Scholar 

  54. Wolz KJ, Branham BE, DeLucia EH (2018a) Reduced nitrogen losses after conversion of row crop agriculture to alley cropping with mixed fruit and nut trees Agric. Ecosyst Environ 258:172–181

    Article  Google Scholar 

  55. Wolz KJ et al (2018b) Frontiers in alley cropping: transformative solutions for temperate agriculture. Glob Change Biol 24:883–894

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the Agroecology and Sustainable Agriculture Program at the University of Illinois Urbana-Champaign and the National Institute of Food and Agriculture, United States Department of Agriculture, under Award Number ILLU-875-918. Funding sources had no involvement in the conception, design, or implementation of the study. We’d also like to thank Alex Hiatt, Di Ye, Nisarg Shah, Iris Daiber, Kat Rola, and Victoria Wallace, the field and lab technicians who helped conduct this research, as well as Ron Revord, Dane Nelson, and Alex Hiatt, who established and managed our research site, and Jane Capozelli, Jaime Coon, Samniqueka Halsey, Scott Nelson, Timothy Swartz, Lawrence Hanks, Brenda Molano-Flores, and Michelle Wander for comments on the manuscript.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Adam J. Kranz.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Kranz, A.J., Wolz, K.J. & Miller, J.R. Effects of shrub crop interplanting on apple pest ecology in a temperate agroforestry system. Agroforest Syst 93, 1179–1189 (2019). https://doi.org/10.1007/s10457-018-0224-8

Download citation

Keywords

  • Alley cropping
  • Conservation biological control
  • Intercropping
  • Natural enemies
  • Polyculture
  • Structural diversity