Experimental and Applied Acarology

, Volume 77, Issue 2, pp 133–143 | Cite as

Generalist predator contributions to the control of Tetranychus urticae in strawberry crops documented by PCR-based gut content analysis

  • Stine Kramer JacobsenEmail author
  • Lene Sigsgaard
  • Kristian Hansen
  • James D. Harwood
  • Eric G. Chapman
  • Mónica A. Hurtado
  • Annette B. Jensen


The contribution of generalist insect predators to the control of the two-spotted spider mite, Tetranychus urticae Koch (Acari: Tetranychidae), an herbivorous pest of many crops, is poorly understood. One of the common insect predators in strawberries is the generalist predatory bug Anthocoris nemorum L. (Hemiptera: Anthocoridae), which has the potential to contribute to the control of pest populations. The feeding of adult A. nemorum on T. urticae was assessed by sampling individuals from an organic strawberry field in Denmark, and using PCR gut content analysis to detect remains of T. urticae within their gut. In the lab, we assessed that the DNA half-life detectability was 21.5 h. Significant numbers of field-collected A. nemorum tested positive for T. urticae prey DNA, with very high numbers in June (62.8%) and August (38.8%). This study presents conclusive evidence that the generalist predator A. nemorum can contribute to the decrease of T. urticae densities in strawberry fields, although the actual contribution in the present study is probably limited because predator populations were relatively low compared to T. urticae. The abundance of T. urticae did not increase significantly during the period of sampling, suggesting that a complex of natural enemies can achieve biological control of T. urticae in protected strawberries.


Spider mites Generalist predators Anthocoris nemorum Molecular gut content analysis Predator–prey interactions 



The authors would like to thank Josep A. Jaques (Jaume I University, Castellón, Spain) for collaboration, Helle Sørensen (Data Science Lab, Department of Mathematical Sciences, University of Copenhagen) for statistical support, the grower Søren Larsen for his hospitality, and the anonymous reviewers for their helpful comments to the manuscript. This study is a part of the research project IMBICONT (Improved Biological Control for IPM in Fruits and Berries) (Project number 1024151001) funded by Innovation Fund Denmark.


  1. Agustí N, Unruh TR, Welter SC (2003) Detecting Cacopsylla pyricola (Hemiptera: Psyllidae) in predator guts using COI mitochondrial markers. B Entomol Res 93:179–185CrossRefGoogle Scholar
  2. Athey KJ, Dreyer J, Kowle KA, Penn HJ, Sitvarin MI, Harwood JD (2016) Spring forward: why early season predation matters in agroecosystems. Food Webs 9:25–31CrossRefGoogle Scholar
  3. Björkman C, Liman A-S (2005) Foraging behavior influences the outcome of predator–predator interactions. Ecol Entomol 30:164–169CrossRefGoogle Scholar
  4. Boreau de Roincé CB, Lavigne C, Mandrin J-F, Rollard C, Symondson WOC (2013) Early-season predation on aphids by winter-active spiders in apple orchards revealed by diagnostic PCR. B Entomol Res 103:148–154CrossRefGoogle Scholar
  5. Chapman EG, Romero S, Harwood JD (2010) Maximizing collection and minimizing risk: does vacuum sampling increase the likelihood for misinterpretation of food web connections? Mol Ecol Resour 10:1023–1033CrossRefPubMedGoogle Scholar
  6. Chen Y, Giles KL, Payton ME, Greenstone MH (2000) Identifying key cereal aphid predators by molecular gut analysis. Mol Ecol 9:1887–1898CrossRefPubMedGoogle Scholar
  7. Danmarks Fauna (1907–2004) Dansk naturhistorisk forening, G.E.C. Gad Forlag, Copenhagen, DKGoogle Scholar
  8. Gagnon A-E, Doyon J, Heimpel GE, Brodeur J (2011) Prey DNA detection success following digestion by intraguild predators: influence of prey and predator species. Mol Ecol Resour 11:1022–1032CrossRefPubMedGoogle Scholar
  9. Gomez-Polo P, Alomar O, Castañé C, Agustí N (2016) Molecular tracking of arthropod predator–prey interactions in Mediterranean lettuce crops. Food Webs 9:18–24CrossRefGoogle Scholar
  10. Greenstone MH, Rowley DL, Weber DC, Payton ME, Hawthorne DJ (2007) Feeding mode and prey detectability half-lives in molecular gut-content analysis: an example with two predators of the Colorado potato beetle. B Entomol Res 97:201–209CrossRefGoogle Scholar
  11. Greenstone MH, Payton ME, Weber DC, Simmons AM (2014) The detectability half-life in arthropod predator–prey research: what it is, why we need it, how to measure it, and how to use it. Mol Ecol 23:3799–3813CrossRefPubMedGoogle Scholar
  12. Gulati R (2014) Eco-friendly management of phytophagous mites. In: Abrol DP (ed) Integrated pest management: current concepts and ecological perspective. Elsevier Inc, New York, pp 461–491CrossRefGoogle Scholar
  13. Gurr GM, Wratten SD, Landis DA, You M (2016) Habitat management to suppress pest populations: progress and prospects. Annu Rev Entomol 62:91–109CrossRefPubMedGoogle Scholar
  14. Harwood JD (2008) Are sweep net sampling and pitfall trapping compatible with molecular analysis of predation? Environ Entomol 37:990–995CrossRefPubMedGoogle Scholar
  15. Harwood JD, Sunderland KD, Symondson WOC (2004) Prey selection by linyphiid spiders: molecular tracking of the effects of alternative prey on rates of aphid consumption in the field. Mol Ecol 13:3549–3560CrossRefPubMedGoogle Scholar
  16. Harwood JD, Desneux N, Yoo HJS, Rowley DL, Greenstone MH, Obrycki JJ, O’Neil RJ (2007) Tracking the role of alternative prey in soybean aphid predation by Orius insidiosus: a molecular approach. Mol Ecol 16:4390–4400CrossRefPubMedGoogle Scholar
  17. Hoy MA (1994) Insect molecular genetics: an introduction to principles and applications. Academic Press, San DiegoCrossRefGoogle Scholar
  18. Hukkanen AT, Kokko HI, Buchala AJ, McDougall GJ, Stewart D, Kärenlampi SO, Karjalainen RO (2007) Benzothiadiazole induces the accumulation of phenolics and improves resistance to powdery mildew in strawberries. J Agr Food Chem 55:1862–1870CrossRefGoogle Scholar
  19. Jacobsen SK, Moraes GJ, Sørensen H, Sigsgaard L (2018) Organic cropping practice decreases pest abundance and positively influences predator–prey interactions. Agr Ecosyst Environ (accepted with moderate revisions) Google Scholar
  20. Kadir S, Carey E, Ennahli S (2006) Influence of high tunnel and field conditions on strawberry growth and development. HortScience 41:329–335CrossRefGoogle Scholar
  21. King RA, Read DS, Traugott M, Symondson WOC (2008) Molecular analysis of predation: a review of best practice for DNA-based approaches. Mol Ecol 17:947–963CrossRefPubMedGoogle Scholar
  22. Krey KL, Blubaugh CK, Chapman EG, Lynch CA, Snyder GB, Jensen AS, Fu Z, Prischmann-Voldseth DA, Harwood JD, Snyder WE (2017) Generalist predators consume spider mites despite the presence of alternative prey. Biol Control 115:157–164CrossRefGoogle Scholar
  23. Macfadyen S, Davies AP, Zalucki MP (2015) Assessing the impact of arthropod natural enemies on crop pests at the field scale. Insect Sci 22:20–34CrossRefPubMedGoogle Scholar
  24. Meyling NV, Enkegaard A, Brødsgaard H (2003) Two Anthocoris bugs as predators of glasshouse aphids—voracity and prey preference. Entomol Exp Appl 108:59–70CrossRefGoogle Scholar
  25. Næss ETL (2016) Molecular analysis of predation by Anthocorid bugs on the pear psyllid Cacopsylla pyri (Homoptera, Psyllidae). Master’s thesis, Norwegian university of life sciencesGoogle Scholar
  26. Oelbermann K, Scheu S (2009) Control of aphids on wheat by generalist predators: effects of predator density and the presence of alternative prey. Entomol Exp Appl 132:225–231CrossRefGoogle Scholar
  27. Pérez-Sayas C, Pina T, Gómez-Martínez MA, Camañes G, Ibáñez-Gual MV, Jaques JA, Hurtado MA (2015) Disentangling mite predator–prey relationships by multiplex PCR. Mol Ecol Resour 15:1330–1345CrossRefPubMedGoogle Scholar
  28. R Development Core Team (2016) The R foundation for statistical computing.
  29. Saulich AK, Musolin DL (2009) Seasonal development and ecology of anthocorids (Heteroptera, Anthocoridae). Entomol Rev 89:501–528CrossRefGoogle Scholar
  30. Schmidt JM, Barney SK, Williams MA, Bessin RT, Coolong TW, Harwood JD (2014) Predator–prey trophic relationships in response to organic management practices. Mol Ecol 23:3777–3789CrossRefPubMedGoogle Scholar
  31. Sheppard SK, Harwood JD (2005) Advances in molecular ecology: tracking trophic links through predator–prey food webs. Funct Ecol 19:751–762CrossRefGoogle Scholar
  32. Sheppard SK, Bell J, Sunderland D, Fenlon J, Skervin D, Symondson WOC (2005) Detection of secondary predation by PCR analyses of the gut contents of invertebrate generalist predators. Mol Ecol 14:4461–4468CrossRefPubMedGoogle Scholar
  33. Sigsgaard L (2010) Habitat and prey preference of the two predatory bugs Anthocoris nemorum (L.) and A. nemoralis (Fabricius) (Anthocoridae: Hemiptera-Heteroptera). Biol Control 53:46–54CrossRefGoogle Scholar
  34. Simonsen MLR, Enkegaard A, Bang CN, Sigsgaard L (2010) Anthocoris nemorum (Heteroptera: Anthocoridae) as predator of cabbage pests—voracity and prey preference. Entomol Fennica 21:12–18Google Scholar
  35. Sint D, Raso L, Kaufmann R, Traugott M (2011) Optimizing methods for PCR-based analysis of predation. Mol Ecol Resour 11:795–801CrossRefPubMedGoogle Scholar
  36. Skerninge, DKGoogle Scholar
  37. Skipper L (2013) Danmarks blomstertæger. Danmarks Dyreliv vol, 12. Apollo Booksellers, VesterGoogle Scholar
  38. Sobhy IS, Sarhan AA, Shoukry AA, El-Kady GA, Mandour NS, Reitz SR (2010) Development, consumption rates and reproductive biology of Orius albidipennis reared on various prey. Biocontrol 55:753–765CrossRefGoogle Scholar
  39. Solomon MG, Cross JV, Fitzgerald JD, Campbell CAM, Jolly RL, Olszak RW, Niemczyk E, Vogt H (2000) Biocontrol of pests of apples and pears in northern and central Europe—3. Predators. Biocontrol Sci Techn 10:91–128CrossRefGoogle Scholar
  40. Southwood TRE, Leston D (2005) Land and water bugs of the British Isles. Pisces Conservation, Ltd. HampshireGoogle Scholar
  41. Staudacher K, Jonsson M, Traugott M (2016) Diagnostic PCR assays to unravel food web interactions in cereal crops with focus on biological control of aphids. J Pest Sci 89:281–293CrossRefGoogle Scholar
  42. Sunderland K (1999) Mechanisms underlying the effects of spiders on pest populations. J Arachnol 27:308–316Google Scholar
  43. Symondson WOC (2002) Molecular identification of prey in predator diets. Mol Ecol 11:627–641CrossRefPubMedGoogle Scholar
  44. Symondson WOC, Liddell JE (1995) Decay rates for slug antigens within the carabid predator Pterostichus melanarius monitored with a monoclonal antibody. Entomol Exp Appl 75:245–250CrossRefGoogle Scholar
  45. Symondson WOC, Sunderland KD, Greenstone MH (2002) Can generalist predators be effective biocontrol agents? Annu Rev Entomol 47:561–594CrossRefPubMedGoogle Scholar
  46. Traugott M, Bell J, Raso L, Sint D, Symondson W (2012) Generalist predators disrupt parasitoid aphid control by direct and coincidental intraguild predation. B Entomol Res 102:239–247CrossRefGoogle Scholar
  47. Vrancken K, Trekels H, Thys T, Beliën T, Bylemans D, Demaeght P, Van Leeuwen T, De Clercq P (2015) The presence of beneficial arthropods in organic versus IPM pear orchards and their ability to predate pear suckers. Acta Hort 1094:427–429CrossRefGoogle Scholar
  48. Wysoki M (1985) Control of Tetranychidae in crops. In: Helle W, Sabelis MW (eds) Spider mites: their biology, natural enemies and control, vol 1B. Elsevier Science Publishers, Amsterdam, pp 273–396Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of Plant and Environmental SciencesUniversity of CopenhagenFrederiksbergDenmark
  2. 2.College of Plant Health and MedicineQingdao Agricultural UniversityQingdaoChina
  3. 3.Department of Entomology, Agricultural Science CenterUniversity of KentuckyLexingtonUSA
  4. 4.Department of Agricultural and Environmental SciencesJaume I UniversityCastellón de la PlanaSpain

Personalised recommendations