Woolly Apple Aphid Generalist Predator Feeding Behavior Assessed through Video Observation in an Apple Orchard

  • Robert J. OrpetEmail author
  • David W. Crowder
  • Vincent P. Jones


Generalist predators are considered effective biological control agents in many agroecosystems. However, characterizing the behavior of different generalist predator species in realistic field settings is difficult due to challenges associated with directly observing predation events in the field. Here we video recorded woolly apple aphid (Erisoma lanigerum) (Hemiptera: Aphididae) colonies to directly observe the feeding behavior of their generalist predators during the day and night. To observe European earwigs (Forficula auricularia) (Dermaptera: Forficulidae), which are thought to be key woolly apple aphid predators but were not present at our study location, we released earwigs into the study area. Across 1413 h of video recorded over 4 weeks, earwigs made the most attacks on woolly apple aphid colonies, but coccinellid larvae spent more total time attacking because their individual attacks were longer. Antagonistic interactions between predators were rare, and earwigs never antagonized other predators. However, ants commonly antagonized earwigs, and incidence of ant-earwig antagonistic interactions was negatively correlated with earwig-aphid attack rates. Overall, these results suggest that coccinellid larvae and earwigs differ in their feeding behavior in the field, and provide new evidence that ants may hinder aphid biological control by antagonizing earwigs.


Biological control Eriosoma lanigerum Forficula auricularia formicidae intraguild predation 



We thank assistants Sam Martin and Dayna Dinius. This work was supported by grants from the Washington State Tree Fruit Research Commission, and from USDA National Institute of Food and Agriculture: accession numbers 1014754, 1016563, and award number 2016-38640-25383 through the Western Sustainable Agriculture Research and Education Program under subaward number 200592-445.


  1. Asante SK (1995) Functional responses of the European earwig and two species of coccinellids to densities of Eriosoma lanigerum (Hausmann) (Hemiptera: Aphididae). J Aust Entomol Soc 34:105–109CrossRefGoogle Scholar
  2. Asante SK, Danthanarayana W, Heatwole H (1991) Bionomics and population growth statistics of apterous virginoperae of woolly apple aphid, Eriosoma lanigerum, at constant temperatures. Entomol Exp Appl 60:261–270CrossRefGoogle Scholar
  3. Asante S, Danthanarayana W, Cairns S (1993) Spatial and temporal distribution patterns of Eriosoma lanigerum (Homoptera: Aphididae) on apple. Environ Entomol 22:1060–1065CrossRefGoogle Scholar
  4. Beers EH, Brunner JF, Willett MJ, Warner GM (1993) Orchard pest management: a resource book for the Pacific northwest. Good Fruit Grower, YakimaGoogle Scholar
  5. Beers EH, Cockfield SD, Gontijo LM (2010) Seasonal phenology of woolly apple aphid (Hemiptera: Aphididae) in Central Washington. Environ Entomol 39:286–294CrossRefGoogle Scholar
  6. Bergh JC, Short BD (2008) Ecological and life-history notes on syrphid predators of woolly apple aphid in Virginia, with emphasis on Heringia calcarata. BioControl 53:773–786CrossRefGoogle Scholar
  7. Bergh JC, Stallings JW (2016) Field evaluations of the contribution of predators and the parasitoid, Aphelinus mali, to biological control of woolly apple aphid, Eriosoma lanigerum, in Virginia, USA. BioControl 61:155–165CrossRefGoogle Scholar
  8. Brown MW, Schmitt JJ (1994) Population dynamics of woolly apple aphid (Homoptera: Aphididae) in West Virginia apple orchards. Environ Entomol 23:1182–1188CrossRefGoogle Scholar
  9. Dib H, Jamont M, Sauphanor B, Capowiez Y (2011) Predation potency and intraguild interactions between generalist (Forficula auricularia) and specialist (Episyrphus balteatus) predators of the rosy apple aphid (Dysaphis plantaginea). Biol Control 59:90–97CrossRefGoogle Scholar
  10. Dib H, Jamont M, Sauphanor B, Capowiez Y (2016) Individual and combined effects of the generalist Forficula auricularia and the specialist Episyrphus balteatus on Dysaphis plantaginea – are two predators better than one? Entomol Exp Appl 161:1–10CrossRefGoogle Scholar
  11. Eisner T (1960) Defense mechanism of arthropods. II. The chemical and mechanical weapons of an earwig. Psyche 67:62–70CrossRefGoogle Scholar
  12. Frank SD, Wratten SD, Sandhu HS, Shrewsbury PM (2007) Video analysis to determine how habitat strata affects predator diversity and predation of Epiphyas postvittana (Lepidoptera: Tortricidae) in a vineyard. Biol Control 41:230–236CrossRefGoogle Scholar
  13. Gontijo LM, Cockfield SD, Beers EH (2012) Natural enemies of woolly apple aphid (Hemiptera: Aphididae) in Washington state. Environ Entomol 41:1364–1371CrossRefGoogle Scholar
  14. Gontijo LM, Beers EH, Snyder WE (2015) Complementary suppression of aphids by predators and parasitoids. Biol Control 90:83–91CrossRefGoogle Scholar
  15. Grieshop MJ, Werling B, Buehrer K, Perrone J, Isaacs R, Landis D (2012) Big brother is watching: studying insect predation in the age of digital surveillance. Am Entomol 58:172–182CrossRefGoogle Scholar
  16. Horton DR, Broers DA, Hinojosa T, Lewis TM, Miliczky ER, Lewis RR (2002) Diversity and phenology of predatory arthropods overwintering in cardboard bands placed in pear and apple orchards of Central Washington state. Ann Entomol Soc Am 95:469–480CrossRefGoogle Scholar
  17. Kistner E, Lewis M, Carpenter E et al (2017) Digital video surveillance of natural enemy activity on Diaphorina citri (Hemiptera: Liviidae) colonies infesting citrus in the southern California urban landscape. Biol Control 115:141–151CrossRefGoogle Scholar
  18. Lamb RJ (1975) Effects of dispersion, travel and environmental heterogenity on populations of the earwig Forficula auricularia L. (Dermaptera, Forficulidae). Can J Zool 53:1855–1867CrossRefGoogle Scholar
  19. McLeod JH, Chant DA (1952) Notes on the parasitism and food habits of the European earwig Forficula auricularia L. (Dermaptera: Forficulidae). Can Entomol 84:174–180CrossRefGoogle Scholar
  20. Merfield CN, Wratten SD, Navntoft S (2004) Video analysis of predation by polyphagous invertebrate predators in the laboratory and field. Biol Control 29:5–13CrossRefGoogle Scholar
  21. Meyhöfer R (2001) Intraguild predation by aphidophagous predators on parasitised aphids: the use of multiple video cameras. Entomol Exp Appl 100:77–87CrossRefGoogle Scholar
  22. Miñarro M, Fernández-Mata G, Medina P (2010) Role of ants in structuring the aphid community on apple. Ecol Entomol 35:206–215CrossRefGoogle Scholar
  23. Moerkens R, Leirs H, Peusens G, Gobin B (2009) Are populations of European earwigs, Forficula auricularia, density dependent? Entomol Exp Appl 130:198–206CrossRefGoogle Scholar
  24. Moerkens R, Leirs H, Peusens G, Gobin B (2010) Dispersal of single- and double-brood populations of the European earwig, Forficula auricularia: a mark-recapture experiment. Entomol Exp Appl 137:19–27CrossRefGoogle Scholar
  25. Moerkens R, Gobin B, Peusens G, Helsen H, Hilton R, Dib H, Suckling DM, Leirs H (2011) Optimizing biocontrol using phenological day degree models: the European earwig in pipfruit orchards. Agric For Entomol 13:301–312CrossRefGoogle Scholar
  26. Moerkens R, Leirs H, Peusens G, Beliën T, Gobin B (2012) Natural and human causes of earwig mortality during winter: temperature, parasitoids and soil tillage. J Appl Entomol 136:490–500CrossRefGoogle Scholar
  27. Mueller TF, Blommers LHM, Mols PJM (1988) Earwig (Forficula auricularia) predation on the woolly apple aphid, Eriosoma lanigerum. Entomol Exp Appl 47:145–152CrossRefGoogle Scholar
  28. Naranjo SE, Ellsworth PC, Frisvold GB (2015) Economic value of biological control in integrated pest management of managed plant systems. Annu Rev Entomol 60:621–645CrossRefGoogle Scholar
  29. Nicholas AH, Spooner-Hart RN, Vickers RA (2005) Abundance and natural control of the woolly aphid Eriosoma lanigerum in an Australian apple orchard IPM program. BioControl 50:271–291CrossRefGoogle Scholar
  30. Noppert F, Smits JD, Mols PJM (1987) A laboratory evaluation of the European earwig (Forficula auricularia L.) as a predator of the woolly apple aphid (Eriosoma lanigerum Hausm.). Med Fac Landnouww Rijksuniv Gent 52:413–422Google Scholar
  31. Orpet RJ, Goldberger JR, Crowder DW, Jones VP (2019a) Field evidence and grower perceptions on the roles of an omnivore, European earwig, in apple orchards. Biol Control 132:189–198CrossRefGoogle Scholar
  32. Orpet RJ, Jones VP, Reganold JP, Crowder DW (2019b) Effects of restricting movement between root and canopy populations of woolly apple aphid. PLoS One 14:e0216424CrossRefGoogle Scholar
  33. Piñol J, Espadaler X, Pérez N, Beven K (2009) Testing a new model of aphid abundance with sedentary and non-sedentary predators. Ecol Model 220:2469–2480CrossRefGoogle Scholar
  34. Quarrell SR, Corkrey R, Allen GR (2017) Predictive thresholds for forecasting the compatibility of Forficula auricularia and Aphelinus mali as biological control agents against woolly apple aphid in apple orchards. BioControl 62:243–256CrossRefGoogle Scholar
  35. Rosenheim JA (1998) Higher-order predators and the regulation of insect herbivore populations. Annu Rev Entomol 43:421–447CrossRefGoogle Scholar
  36. Short BD, Bergh JC (2004) Feeding and egg distribution studies of Heringia calcarata (Diptera: Syrphidae), a specialized predator of woolly apple aphid (Homoptera: Eriosomatidae) in Virginia apple orchards. J Econ Entomol 97:813–819CrossRefGoogle Scholar
  37. Smith C, Gardiner M (2013) Oviposition habitat influences egg predation of native and exotic coccinellids by generalist predators. Biol Control 67:235–245CrossRefGoogle Scholar
  38. Straub CS, Finke DL, Snyder WE (2008) Are the conservation of natural enemy biodiversity and biological control compatible goals? Biol Control 45:225–237CrossRefGoogle Scholar
  39. Symondson WOC, Sunderland KD, Greenstone MH (2002) Can generalist predators be effective biocontrol agents? Annu Rev Entomol 47:561–594CrossRefGoogle Scholar
  40. Walton NJ, Grieshop MJ (2016) Video observations of the natural enemies of eggs of codling moth, Cydia pomonella, in apple orchards in Michigan, USA. Entomol Exp Appl 159:375–377CrossRefGoogle Scholar
  41. Weber DC, Lundgren JG (2009) Assessing the trophic ecology of the Coccinellidae: their roles as predators and as prey. Biol Control 51:199–214CrossRefGoogle Scholar
  42. Woltz J, Lee J (2017) Pupation behavior and larval and pupal biocontrol of Drosophila suzukii in the field. Biol Control 110:62–69CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Entomology, Tree Fruit Research and Extension CenterWashington State UniversityWenatcheeUSA
  2. 2.Department of EntomologyWashington State UniversityPullmanUSA

Personalised recommendations