Journal of Pest Science

, Volume 90, Issue 1, pp 287–297 | Cite as

Influence of extraguild prey and intraguild predators on the phytophagy of the zoophytophagous bug Campylomma verbasci

  • Olivier AubryEmail author
  • Daniel Cormier
  • Gérald Chouinard
  • Eric Lucas
Original Paper


The mullein bug, Campylomma verbasci (Meyer-Dür) (Hemiptera: Miridae), a palearctic zoophytophagous insect or plant-feeding predator, is common in apple orchards of North America. The aim of this study was to evaluate the influence of the biotic environment (extraguild prey and intraguild predators) on the phytophagy of this zoophytophagous bug. We hypothesized that (1) the presence of extraguild prey should reduce the intensity of phytophagy by the mullein bug and that (2) the presence of intraguild predators should reduce the intensity of phytophagy by the mullein bug as an intraguild prey. Phytophagy was evaluated by observing (1) mullein bug feeding punctures in the laboratory and (2) apple fruit damage by mullein bug in the field. Two extraguild prey types were tested: Aphis pomi De Geer (Hemiptera: Aphididae) and Panonychus ulmi (Koch) (Acari: Tetranychidae), at four densities each (zero, four, eight, and 16). Seven combinations of insects were tested using one mullein bug nymph with or without an intraguild predator (coccinellid). Our results confirm the first hypothesis, but only partially confirm the second. The number of feeding punctures only decreased in the presence of some intraguild predators.


Hemiptera Miridae Aphididae Tetranychidae Coccinellidae Omnivory 



We are grateful to Caroline Belle, Mathieu Ratelle, and David Chouinard for their technical assistance, Jonathan Veilleux for linguistic revision of the manuscript, and Michèle Grenier for statistical analysis. We also thank two anonymous reviewers for valuable comments on this manuscript. This study was funded by a grant from the Programme de soutien à l’innovation en agroalimentaire du Ministère de l’Agriculture, des Pêcheries et de l’Alimentation du Québec (Quebec, Canada), and a Natural Sciences and Engineering Research Council of Canada discovery grant to E. Lucas.


  1. Albajes R, Castane C, Gabarra R, Alomar O (2006) Risks of plant damage caused by natural enemies introduced for arthropod biological control. In: Bigler F, Babendreier D, Kuhlmann U (eds) Environmental impact of invertebrates for biological control of arthropods: methods and risk assessment. CABI Publishing, Cambridge, pp 132–144CrossRefGoogle Scholar
  2. Alomar O, Albajes R (1996) Greenhouse whitefly (Homoptera: Aleyrodidae) predation and tomato fruit injury by the zoophytophagous predator Dicyphus tamaninii (Heteroptera: Miridae). In: Alomar O, Wiedenmann RN (eds) Zoophytophagous Heteroptera: implications for life history and integrated pest management. Thomas Say Publications, Lanham, pp 155–177Google Scholar
  3. Arnoldi D, Stewart RK, Boivin G (1992) Predatory mirids of the green apple aphid Aphis pomi, the two-spotted spider mite Tetranychus urticae and the European red mite Panonychus ulmi in apple orchards in Quebec. Entomophaga 37:283–292CrossRefGoogle Scholar
  4. Aubry O, Cormier D, Chouinard G, Lucas E (2015) Influence of plant, animal and mixed resources on development of the zoophytophagous plant bug Campylomma verbasci (Hemiptera: Miridae). Biocontrol Sci Technol 25:1426–1442. doi: 10.1080/09583157.2015.1061098 CrossRefGoogle Scholar
  5. Castane C, Alomar O, Riudavets J (2003) Potential risk of damage to zucchinis caused by mirid bugs. IOBC/WPRS Bull 26:135–138Google Scholar
  6. Castane C, Arno J, Gabarra R, Alomar O (2011) Plant damage to vegetable crops by zoophytophagous mirid predators. Biol Control 59:22–29CrossRefGoogle Scholar
  7. Cohen AC (1996) Plant feeding by predatory Heteroptera: evolutionary and adaptational aspects of trophic switching. In: Alomar O, Wiedenmann RN (eds) Zoophytophagous Heteroptera: implications for life history and integrated pest management. Thomas Say Publications, Lanham, pp 1–17Google Scholar
  8. Coll M, Guershon M (2002) Omnivory in terrestrial arthropods: mixing plant and prey diets. Annu Rev Entomol 47:267–297CrossRefPubMedGoogle Scholar
  9. Diehl S, Feissel M (2000) Effects of enrichment on three-level food chains with omnivory. Am Nat 155:200–218PubMedGoogle Scholar
  10. Eubanks MD, Styrsky JD (2005) Effects of plant feeding on the performance of omnivorous predators. In: Wackers FL, van Rijn PCJ, Bruin J (eds) Plant-provided food and herbivore–carnivore interactions. Cambridge University Press, New York, pp 148–177CrossRefGoogle Scholar
  11. Fauvel G (1999) Diversity of Heteroptera in agroecosystems: role of sustainability and bioindication. Agric Ecosyst Environ 74:275–303CrossRefGoogle Scholar
  12. Frechette B, Rojo S, Alomar O, Lucas E (2007) Intraguild Predation between syrphids and mirids: who is the prey? Who is the predator? Biocontrol 52:175–191CrossRefGoogle Scholar
  13. Gabarra R, Alomar O, Castane C, Goula M, Albajes R (2004) Movement of greenhouse whitefly and its predators between in- and outside of Mediterranean greenhouses. Agric Ecosyst Environ 102:341–348CrossRefGoogle Scholar
  14. Gillespie DR, McGregor RR (2000) The functions of plant feeding in the omnivorous predator Dicyphus hesperus: water places limit on predation. Ecol Entomol 25:380–386CrossRefGoogle Scholar
  15. Gillespie DR, Roitberg BD (2006) Inter-guild influences on intra-guild predation in plant-feeding omnivores. In: Brodeur J, Boivin G (eds) Trophic and guild interactions in biological control. Springer, Dordrecht, pp 71–100CrossRefGoogle Scholar
  16. Han P, Dong Y, Lavoir AV, Adamowicz S, Bearez P, Wajnberg E, Desneux N (2015) Effect of plant nitrogen and water status on the foraging behavior and fitness of an omnivorous arthropod. Ecol Evol. doi: 10.1002/ece3.1788 Google Scholar
  17. Hindayana D, Meyhofer R, Scholz D, Poehling HM (2001) Intraguild predation among the hoverfly Episyrphus balteatus de Geer (Diptera: Syrphidae) and other aphidophagous predators. Biol Control 20:236–246CrossRefGoogle Scholar
  18. Hori K (2000) Possible causes of disease symptoms resulting from the feeding of phytophagous Heteroptera. In: Schaefer CW, Panizzi AR (eds) Heteroptera of economic importance. CRC Press, New York, pp 11–35Google Scholar
  19. Lord FT (1971) Laboratory tests to compare the predatory value of six mirid species in each stage of development against the winter eggs of the European red mite, Panonychus ulmi (Acari: Tetranychidae). Can Entomol 103:1663–1669CrossRefGoogle Scholar
  20. Lucas E (2012) Intraguild interactions. In: Hodek I, van Emden HF, Honek A (eds) Ecology and behaviour of the ladybird beetles (Coccinellidae). Blackwell Publishing, Chichester, pp 343–374CrossRefGoogle Scholar
  21. Lucas E, Alomar O (2001) Macrolophus caliginosus (Wagner) as an intraguild prey for the zoophytophagous Dicyphus tamaninii Wagner (Heteroptera: Miridae). Biol Control 20:147–152CrossRefGoogle Scholar
  22. Lucas E, Alomar O (2002) Impact of Macrolophus caliginosus presence on damage production by Dicyphus tamaninii (Heteroptera: Miridae) on tomato fruits. J Econ Entomol 95:1123–1129CrossRefPubMedGoogle Scholar
  23. Lucas E, Rosenheim JA (2011) Influence of extraguild prey density on intraguild predation by heteropteran predators: a review of the evidence and a case study. Biol Control 59:61–67CrossRefGoogle Scholar
  24. Lucas E, Vincent C, Labrie G, Chouinard G, Fournier F, Pelletier F, Bostanian NJ, Coderre D, Mignault M-P, Lafontaine P (2007) The multicolored Asian ladybeetle Harmonia axyridis (Coleoptera: Coccinellidae) in Quebec agroecosystems ten years after its arrival. Eur J Entomol 104:737–743CrossRefGoogle Scholar
  25. Lucas E, Fréchette B, Alomar O (2009) Resource quality, resource availability, and intraguild predation among omnivorous mirids. Biocontrol Sci Technol 19:555–572CrossRefGoogle Scholar
  26. Mirande L, Desneux N, Haramboure M, Schneider MI (2015) Intraguild predation between an exotic and a native coccinellid in Argentina: the role of prey density. J Pest Sci 88:155–162CrossRefGoogle Scholar
  27. Montserrat M, Albajes R, Castane C (2004) Behavioral responses of three plant-inhabiting predators to different prey densities. Biol Control 30:256–264CrossRefGoogle Scholar
  28. Moreno-Ripoll R, Gabarra R, Symondson WOC, King RA, Agusti N (2014) Do the interactions among natural enemies compromise the biological control of the whitefly Bemisia tabaci? J Pest Sci 87:133–141CrossRefGoogle Scholar
  29. Naranjo SE, Gibson RL (1996) Phytophagy in predaceous Heteroptera: effects on life history and population dynamics. In: Alomar O, Wiedenmann RN (eds) Zoophytophagous Heteroptera: implications for life history and integrated pest management. Thomas Say Publications, Lanham, pp 57–93Google Scholar
  30. Parent B (1967) Population studies of phytophagous mites and predators on apple in southwestern Quebec. Can Entomol 99:771–778CrossRefGoogle Scholar
  31. Preisser EL, Bolnick DI, Benard MF (2005) Scared to death? The effects of intimidation and consumption in predator-prey interactions. Ecology 86:501–509CrossRefGoogle Scholar
  32. Pumarino L, Alomar O, Agusti N (2011) Development of specific ITS markers for plant DNA identification within herbivorous insects. Bull Entomol Res 101:271–276CrossRefPubMedGoogle Scholar
  33. Reding ME, Beers EH, Brunner JF, Dunley JE (2001) Influence of timing and prey availability on fruit damage to apple by Campylomma verbasci (Hemiptera: Miridae). J Econ Entomol 94:33–38CrossRefPubMedGoogle Scholar
  34. Sanchez JA (2008) Factors influencing zoophytophagy in the plant bug Nesidiocoris tenuis (Heteroptera: Miridae). Agric For Entomol 10:75–80CrossRefGoogle Scholar
  35. Sanchez JA, Lacasa A (2008) Impact of the zoophytophagous plant bug Nesidiocoris tenuis (Heteroptera: Miridae) on tomato yield. J Econ Entomol 101:1864–1870CrossRefPubMedGoogle Scholar
  36. Sanchez JA, Gillespie DR, McGregor RR (2004) Plant preference in relation to life history traits in the zoophytophagous predator Dicyphus hesperus. Entomol Exp Appl 112:7–19CrossRefGoogle Scholar
  37. SAS Institute Inc (2013) JMP®, Version 11. SAS Institute Inc, CaryGoogle Scholar
  38. Schmidt JM, Taylor JR, Rosenheim JA (1998) Cannibalism and intraguild predation in the predatory Heteroptera. In: Coll M, Ruberson JR (eds) Predatory Heteroptera: their ecology and use in biological control. Thomas Say Publications in Entomology, Lanham, pp 131–169Google Scholar
  39. Sengonca C, Saleh A, Blasse RP (2003) Investigations on the potential damage caused to cucumber fruit by the polyphagous predatory bug Dicyphus tamaninii Wagner (Heteroptera: Miridae) under different nutritional conditions. J Plant Dis Protect 110:59–65Google Scholar
  40. Shipp JL, Wang K (2006) Evaluation of Dicyphus hesperus (Heteroptera: Miridae) for biological control of Frankliniella occidentalis (Thysanoptera: Thripidae) on greenhouse tomato. J Econ Entomol 99:414–420CrossRefPubMedGoogle Scholar
  41. Sinia A, Roitberg B, McGregor RR, Gillespie DR (2004) Prey feeding increases water stress in the omnivorous predator Dicyphus hesperus. Entomol Exp Appl 110:243–248CrossRefGoogle Scholar
  42. Stigter H (1996) Campylomma verbasci, a new pest on apple in The Netherlands (Heteroptera: Miridae). IOBC/WPRS Bull 19:140–144Google Scholar
  43. Strawinski K (1964) Zoophagism of terrestrial Hemiptera–Heteroptera occuring in Poland. Ekol Pol-Pol J Ecol 12:429–452Google Scholar
  44. Thistlewood HMA, Smith RF (1996) Management of the Mullein Bug, Campylomma verbasci (Heteroptera: Miridae), in Pome Fruit Orchards of Canada. In: Alomar O, Wiedenmann RN (eds) Zoophytophagous Heteroptera: implications for life history and integrated pest management. Thomas Say Publications, Lanham, pp 119–140Google Scholar
  45. Thistlewood HMA, Borden JH, Smith RF, Pierce HD, McMullen RD (1989) Evidence for a sex pheromone in the mullein bug, Campylomma verbasci (Meyer) (Heteroptera: Miridae). Can Entomol 121:737–744CrossRefGoogle Scholar
  46. Wheeler AG (2000) Predacious Plant Bugs (Miridae). In: Schaefer CW, Panizzi AR (eds) Heteroptera of economic importance. CRC Press, New York, pp 657–693CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Département des Sciences BiologiquesUniversité du Québec à MontréalMontréalCanada
  2. 2.Institut de recherche et de développement en agroenvironnementSaint-Bruno-de-MontarvilleCanada

Personalised recommendations