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

Abstract

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.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  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 132–144

    Google 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 155–177

    Google 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 37:283–292

    Article  Google 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

    Article  Google Scholar 

  5. Castane C, Alomar O, Riudavets J (2003) Potential risk of damage to zucchinis caused by mirid bugs. IOBC/WPRS Bull 26:135–138

    Google Scholar 

  6. Castane C, Arno J, Gabarra R, Alomar O (2011) Plant damage to vegetable crops by zoophytophagous mirid predators. Biol Control 59:22–29

    Article  Google 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 1–17

    Google Scholar 

  8. Coll M, Guershon M (2002) Omnivory in terrestrial arthropods: mixing plant and prey diets. Annu Rev Entomol 47:267–297

    CAS  Article  PubMed  Google Scholar 

  9. Diehl S, Feissel M (2000) Effects of enrichment on three-level food chains with omnivory. Am Nat 155:200–218

    CAS  PubMed  Google 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 148–177

    Google Scholar 

  11. Fauvel G (1999) Diversity of Heteroptera in agroecosystems: role of sustainability and bioindication. Agric Ecosyst Environ 74:275–303

    Article  Google 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 52:175–191

    Article  Google 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 102:341–348

    Article  Google 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 25:380–386

    Article  Google 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 71–100

    Google 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 20:236–246

    Article  Google 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 11–35

    Google 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 103:1663–1669

    Article  Google 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 343–374

    Google Scholar 

  21. Lucas E, Alomar O (2001) Macrolophus caliginosus (Wagner) as an intraguild prey for the zoophytophagous Dicyphus tamaninii Wagner (Heteroptera: Miridae). Biol Control 20:147–152

    Article  Google 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 95:1123–1129

    Article  PubMed  Google 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 59:61–67

    Article  Google 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 104:737–743

    Article  Google Scholar 

  25. Lucas E, Fréchette B, Alomar O (2009) Resource quality, resource availability, and intraguild predation among omnivorous mirids. Biocontrol Sci Technol 19:555–572

    Article  Google 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 88:155–162

    Article  Google Scholar 

  27. Montserrat M, Albajes R, Castane C (2004) Behavioral responses of three plant-inhabiting predators to different prey densities. Biol Control 30:256–264

    Article  Google 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 87:133–141

    Article  Google 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 57–93

    Google Scholar 

  30. Parent B (1967) Population studies of phytophagous mites and predators on apple in southwestern Quebec. Can Entomol 99:771–778

    Article  Google Scholar 

  31. Preisser EL, Bolnick DI, Benard MF (2005) Scared to death? The effects of intimidation and consumption in predator-prey interactions. Ecology 86:501–509

    Article  Google Scholar 

  32. Pumarino L, Alomar O, Agusti N (2011) Development of specific ITS markers for plant DNA identification within herbivorous insects. Bull Entomol Res 101:271–276

    CAS  Article  PubMed  Google 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 94:33–38

    CAS  Article  PubMed  Google Scholar 

  34. Sanchez JA (2008) Factors influencing zoophytophagy in the plant bug Nesidiocoris tenuis (Heteroptera: Miridae). Agric For Entomol 10:75–80

    Article  Google Scholar 

  35. Sanchez JA, Lacasa A (2008) Impact of the zoophytophagous plant bug Nesidiocoris tenuis (Heteroptera: Miridae) on tomato yield. J Econ Entomol 101:1864–1870

    CAS  Article  PubMed  Google 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 112:7–19

    Article  Google Scholar 

  37. SAS Institute Inc (2013) JMP®, Version 11. SAS Institute Inc, Cary

    Google 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 131–169

    Google 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 110:59–65

    Google 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 99:414–420

    CAS  Article  PubMed  Google 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 110:243–248

    Article  Google Scholar 

  42. Stigter H (1996) Campylomma verbasci, a new pest on apple in The Netherlands (Heteroptera: Miridae). IOBC/WPRS Bull 19:140–144

    Google Scholar 

  43. Strawinski K (1964) Zoophagism of terrestrial Hemiptera–Heteroptera occuring in Poland. Ekol Pol-Pol J Ecol 12:429–452

    Google 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 119–140

    Google 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 121:737–744

    CAS  Article  Google Scholar 

  46. Wheeler AG (2000) Predacious Plant Bugs (Miridae). In: Schaefer CW, Panizzi AR (eds) Heteroptera of economic importance. CRC Press, New York, pp 657–693

    Google Scholar 

Download references

Acknowledgments

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.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Olivier Aubry.

Additional information

Communicated by T. Haye.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Aubry, O., Cormier, D., Chouinard, G. et al. Influence of extraguild prey and intraguild predators on the phytophagy of the zoophytophagous bug Campylomma verbasci . J Pest Sci 90, 287–297 (2017). https://doi.org/10.1007/s10340-016-0765-4

Download citation

Keywords

  • Hemiptera
  • Miridae
  • Aphididae
  • Tetranychidae
  • Coccinellidae
  • Omnivory