Skip to main content

Factors affecting flight capacity of brown marmorated stink bug, Halyomorpha halys (Hemiptera: Pentatomidae)

Abstract

Brown marmorated stink bug, Halyomorpha halys (Stål) is a highly destructive invasive pest of annual and perennial crops in the eastern United States and is an increasing threat to agriculture in the Pacific Northwest. Flight mills were used to examine flight capacity of H. halys in order to better understand its invasive characteristics. Specifically, we examined generational, sexual, and phenotypical effects on flight distance, frequency, velocity, and diel flight patterns of field-collected H. halys from two seasons. There was a clear dichotomy in total flight distance for insects that flew 5 km or less and those that flew more than 5 km in 24 h. The tendency for long distance flight of H. halys changed over the course of a given season, peaking at the end of the growing season. Summer generation H. halys flew farther and faster than overwintered adults, but not as frequently. Males and females had similar numbers of flights, but females went farther. Pre-flight weight of insects was correlated flight activity of adults in terms of speed, frequency, and distance. Overwintered H. halys lost a greater proportion of their pre-flight body weight during the assay than did the summer generation adults. Despite many limitations extrapolating flight mill data to the field, this study nonetheless provided evidence that H. halys has the capacity for long distance flight, particularly in the summer generation. The nutritional status and fat reserves of overwintered versus summer generation adults are discussed as potential explanations for the flight patterns found in this study.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  1. Armes N, Cooter R (1991) Effects of age and mated status on flight potential of Helicoverpa armigera (Lepidoptera: Noctuidae). Phys Entomol 16:131–144

    Article  Google Scholar 

  2. Chapman RF (1998) The insects: structure and function. Cambridge University Press, Cambridge

    Book  Google Scholar 

  3. Chown S (2002) Respiratory water loss in insects. Comp Biochem Physiol A 133:791–804

    Article  CAS  Google Scholar 

  4. Cockbain A (1961a) Fuel utilization and duration of tethered flight in Aphis fabae Scop. J Exp Biol 38:163–174

    CAS  Google Scholar 

  5. Cockbain A (1961b) Water relationships of Aphis fabae Scop. during tethered flight. J Exp Biol 38:175–180

    CAS  Google Scholar 

  6. Desena M, Clark J, Edman J, Symington S, Scott T, Clark G, Peters T (1999) Potential for aging female Aedes aegypti (Diptera: Culicidae) by gas chromatographic analysis of cuticular hydrocarbons, including a field evaluation. J Med Entomol 36:811–823

    Article  CAS  PubMed  Google Scholar 

  7. Funayama K (2004) Importance of apple fruits as food for the brown-marmorated stink bug, Halyomorpha halys (Stål) (Heteroptera: Pentatomidae). Appl Entomol Zool 39:617–623

    Article  Google Scholar 

  8. Funayama K (2012) Nutritional states of post-overwintering adults of the brown marmorated stink bug, Halyomorpha halys (Stål) (Heteroptera: Pentatomidae). Jpn J Appl Entomol Zool 56:12–15

    Article  Google Scholar 

  9. Gariepy TD, Haye T, Fraser H, Zhang J (2014) Occurrence, genetic diversity, and potential pathways of entry of Halyomorpha halys in newly invaded areas of Canada and Switzerland. J Pest Sci 87:17–28

    Article  Google Scholar 

  10. Gatehouse AG, Zhang X-X (1995) Migratory potential in insects: variation in an uncertain environment. In: Drake VA, Gatehouse AG (eds) Insect migration: tracking resources through space and time. Cambridge University Press, New York, pp 193–243

    Google Scholar 

  11. Hamilton GC (2009) Brown marmorated stink bug. Am Entomol 55:19–20

    Article  Google Scholar 

  12. Haye T, Abdallah S, Gariepy T, Wyniger D (2014) Phenology, life table analysis and temperature requirements of the invasive brown marmorated stink bug, Halyomorpha halys, in Europe. J Pest Sci. doi:10.1007/s10340-014-0560-z

    Google Scholar 

  13. Heinrich B (1971) Temperature regulation of the sphinx moth, Manduca sexta I. flight energetics and body temperature during free and tethered flight. J Exp Biol 54:141–152

    CAS  PubMed  Google Scholar 

  14. Hocking B (1953) The intrinsic range and speed of insect flight. Trans R Entomol Soc Lond 104:223–345

    Google Scholar 

  15. Hoebeke ER, Carter ME (2003) Halyomorpha halys (Stål) (Heteroptera: Pentatomidae): a polyphagous plant pest from Asia newly detected in North America. Proc Entomol Soc Wash 105:225–237

    Google Scholar 

  16. Hoffmann W (1931) A pentatomid pest of growing beans in South China. Pek Nat Hist Bull 5:25–26

    Google Scholar 

  17. Holtz T, Kamminga K. 2010. Qualitative analysis of the pest risk potential of the brown marmorated stink bug (BMSB), Halyomorpha halys (Stål), in the United States. United States Department of Agriculture: APHIS - PPQ

  18. Inkley DB (2012) Characteristics of home invasion by the brown marmorated stink bug (Hemiptera: Pentatomidae). J Entomol Sci 47:125–130

    Google Scholar 

  19. Jactel H, Gaillard J (2009) A preliminary study of the dispersal potential of Ips sexdentatus (Boern) (Col., Scolytidae) with an automatically recording flight mill. J Appl Entomol 112:138–145

    Article  Google Scholar 

  20. James DG, Faulder RJ, Warren GN (1990) Phenology of reproductive status, weight, and lipid reserves of Biprorulus bibax (Hemiptera: Pentatomidae). Environ Entomol 19:1710–1715

    Article  Google Scholar 

  21. Jianxin C, Wanzhi C (2009) Flight patterns of Cletus rusticus (Stål) (Hemiptera: Coreidae). In: WRI World Cong. Comp. Sci. Eng., vol. 1, IEEE, pp 617–621

  22. Johnson C (1963) Physiological factors in insect migration by flight. Nature 198:423–427

    Article  Google Scholar 

  23. Jones VP, Smith TJ, Naranjo S (2010) Insect ecology and behavior: laboratory flight mill studies. http://entomology.tfrec.wsu.edu/VPJ_Lab/Flight-Mill.html.  Accessed 26 March 2014

  24. Khrimian A, Shearer PW, Zhang A, Hamilton GC, Aldrich JR (2007) Field trapping of the invasive brown marmorated stink bug, Halyomorpha halys, with geometric isomers of methyl 2,4,6-decatrienoate. J Agric Food Chem 56:197–203

    Article  PubMed  Google Scholar 

  25. Krogh A, Weis-Fogh T (1952) A roundabout for studying sustained flight of locusts. J Exp Biol 29:211–219

    Google Scholar 

  26. Krupke CH, Brunner JF, Doerr MD, Kahn AD (2001) Field attraction of consperse stink bug Euschistus conspersus (Hemiptera: Pentatomidae) to synthetic pheromone-baited host plants. J Econ Entomol 94:1500–1505

    Article  CAS  PubMed  Google Scholar 

  27. Lee KC, Kang CH, Lee DW, Lee SM, Park GC, Chon HJ (2002) Seasonal occurrence trends of hemipteran bug pests monitored by mercury light and aggregation pheromone traps in sweet persimmon orchards. Korean J Appl Entomol 41:233–238

    Article  Google Scholar 

  28. Lee D-H, Wright SE, Boiteau G, Vincent C, Leskey TC (2013) Effectiveness of glues for harmonic radar tag attachment on Halyomorpha halys (Hemiptera: Pentatomidae) and their impact on adult survivorship and mobility. Environ Entomol 42:515–523

    Article  PubMed  Google Scholar 

  29. Leskey TC, Short B, Butler B, Wright SE (2012a) Impact of the invasive brown marmorated stink bug, Halyomorpha halys (Stål). In: Mid-Atlantic tree fruit orchards in the United States: case studies of commercial management. Psyche 2012, pp 14

  30. Leskey TC, Hamilton GC, Nielsen AL, Polk DF, Rodriguez-Saona C, Bergh JC, Herbert DA, Kuhar TP, Pfeiffer D, Dively GP, Hooks CR, Raupp MJ, Shrewsbury PM, Krawczyk G, Shearer PW, Whalen J, Koplinka-Loehr C, Myers E, Inkley D, Hoelmer KA, Lee D-H, Wright SE (2012b) Pest status of the brown marmorated stink bug, Halyomorpha halys (Stål) in the USA. Outlook Pest Manag 23:218–226

    Article  Google Scholar 

  31. Martinson HM, Raupp MJ, Shrewsbury PJ (2013) Invasive stink bug wounds trees, liberates sugars, and facilitates native Hymenoptera. Ann Entomol Soc Am 106:47–52

    Article  Google Scholar 

  32. McPherson JE, McPherson R (2000) Stink bugs of economic importance in America north of Mexico. CRC Press, New York

    Book  Google Scholar 

  33. Millar JG, McBrien HM, McElfresh JS (2010) Field trials of aggregation pheromones for the stink bugs Chlorochroa uhleri and Chlorochroa sayi (Hemiptera: Pentatomidae). J Econ Entomol 103:1603–1612

    Article  CAS  PubMed  Google Scholar 

  34. Naranjo S (1990) Comparative flight behavior of Diabrotica virgifera virgifera and Diabrotica barberi in the laboratory. Entomol Exp Appl 55:79–90

    Article  Google Scholar 

  35. Nelson DR, Charlet LD (2003) Cuticular hydrocarbons of the sunflower beetle, Zygogramma exclamationis. Comp Biochem Physiol B 135:273–284

    Article  PubMed  Google Scholar 

  36. Nelson DR, Lee RE (2004) Cuticular lipids and desiccation resistance in overwintering larvae of the goldenrod gall fly, Eurosta solidaginis (Diptera: Tephritidae). Comp Biochem Physiol B 138:313–320

    Article  PubMed  Google Scholar 

  37. Nicolson SW, Louw GN (1982) Simultaneous measurement of evaporative water loss, oxygen consumption, and thoracic temperature during flight in a carpenter bee. J Exp Zool 222:287–296

    Article  Google Scholar 

  38. Nielsen A, Hamilton G (2009) Seasonal occurrence and impact of Halyomorpha halys (Hemiptera: Pentatomidae) in tree fruit. J Econ Entomol 102:1133–1140

    Article  PubMed  Google Scholar 

  39. Nielsen A, Hamilton G, Matadha D (2008) Developmental rate estimation and life table analysis for Halyomorpha halys (Hemiptera: Pentatomidae). Environ Entomol 37:348–355

    Article  PubMed  Google Scholar 

  40. Nielsen AL, Hamilton GC, Shearer PW (2011) Seasonal phenology and monitoring of the non-native Halyomorpha halys (Hemiptera: Pentatomidae) in soybean. Environ Entomol 40:231–238

    Article  Google Scholar 

  41. Niva CC, Takeda M (2002) Color changes in Halyomorpha brevis (Heteroptera: Pentatomidae) correlated with distribution of pteridines: regulation by environmental and physiological factors. Comp Biochem Physiol B 132:653–660

    Article  PubMed  Google Scholar 

  42. Niva CC, Takeda M (2003) Effects of photoperiod, temperature and melatonin on nymphal development, polyphenism and reproduction in Halyomorpha halys (Heteroptera: Pentatomidae). Zool Sci 20:963–970

    Article  CAS  PubMed  Google Scholar 

  43. Oregon Department of Agriculture (2010) Pest alert: brown marmorated stink bug. http://oregon.gov/ODA/PLANT/docs/pdf/ippm_bmsb_alert2010.pdf. Accessed 26 March 2014

  44. Panizzi A, Mcpherson J, James D, Javahery M, Mcpherson R (2000) Stink bugs (Pentatomidae). In: Schaefer CW, Panizzi AR (eds) Heteroptera of economic importance. CRC Press, New York

    Google Scholar 

  45. Pfeiffer D, Leskey TC, Burrack H (2012) Threatening the harvest: The threat from three invasive insects in late season vineyards. In: Bostanian N, Vincent C, Isaacs R (eds) Arthropod management in vineyards. Springer, New York, pp 449–474

    Chapter  Google Scholar 

  46. R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, ISBN 3-900051-07-0

  47. Riley J, Downham M, Cooter R (1997) Comparison of the performance of Cicadulina leafhoppers on flight mills with that to be expected in free flight. Entomol Exp Appl 83:317–322

    Article  Google Scholar 

  48. Sappington TW, Showers WB (1992) Lack of translation of density-induced morphological polyphenism to long-duration flight behavior of black cutworm (Lepidoptera: Noctuidae). Ann Entomol Soc Am 85:188–194

    Article  Google Scholar 

  49. Schumacher P, Weyeneth A, Weber D, Dorn S (2008) Long flights in Cydia pomonella L. (Lepidoptera: Tortricidae) measured by a flight mill: influence of sex, mated status and age. Phys Entomol 22:149–160

    Article  Google Scholar 

  50. Shearer PW, Wiman NG (2013) Voltinism of Oregon populations of brown marmorated stink bug, Halyomorpha halys. Unpublished raw data

  51. Shearer PW, Wiman NG (2014) Brown marmorated stink bug. In: Hollingsworth (ed) Pacific Northwest insect management handbook, Oregon State University, University of Idaho, and Washington State University Extension, http://uspest.org/pnw/insects

  52. Smith TJ (2012) Effects of flight and sublethal pesticide residues on codling moth, Cydia pomonella (L), obliquebanded leafroller, Choristoneura rosaceana (Harris), and convergent ladybird beetle, Hippodamia convergens (Guérin-Méneville). Master of Science Thesis, Washington State University, Pullman

  53. Tanaka K, Yamanaka T (2009) Factors affecting flight activity of Ophraella communa (Coleoptera: Chrysomelidae), an exotic insect in Japan. Environ Entomol 38:235–241

    Article  PubMed  Google Scholar 

  54. Taylor RA, Bauer LS, Poland TM, Windell KN (2010) Flight performance of Agrilus planipennis (Coleoptera: Buprestidae) on a flight mill and in free flight. J Insect Behav 23:128–148

    Article  Google Scholar 

  55. Tindall KV, Fothergill K, McCormack B (2012) Halyomorpha halys (Hemiptera: Pentatomidae): a first Kansas record. J Kans Entomol Soc 85:169

    Article  Google Scholar 

  56. USDA National Agricultural Statistics Service (NASS) (2011) Agricultural statistics 2011. United States Government Printing Office, Washington DC

    Google Scholar 

  57. Watanabe M, Arakawa R, Shinagawa Y, Okazawa T (1994) Anti-invading methods against the brown marmorated stink bug, Halyomorpha mista, in houses. Jpn J Sanit Zool 45:311–317

    Google Scholar 

  58. Xu J, Fonseca DM, Hamilton GC, Hoelmer KA, Nielsen AL (2014) Tracing the origin of US brown marmorated stink bugs, Halyomorpha halys. Biol Invasions 16:153–166

    Article  CAS  Google Scholar 

  59. Zhu G, Bu W, Gao Y, Liu G (2012) Potential geographic distribution of brown marmorated stink bug invasion (Halyomorpha halys). PLoS ONE 7:e31246

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Wyatt Rice-Narusch for help with flight mill assembly, Erika Maslen and Chris Hedstrom for assisting with field collections, and Teah Smith for technical assistance with the flight mills. Thanks to Doo-Hyung Lee for comments that improved this manuscript. This research was supported by Agriculture and Food Research Initiative Specialty Crop Research Initiative Competitive Grant no. 2011-51181-30937 from the USDA National Institute of Food and Agriculture.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Nik G. Wiman.

Additional information

Communicated by T. Haye.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Wiman, N.G., Walton, V.M., Shearer, P.W. et al. Factors affecting flight capacity of brown marmorated stink bug, Halyomorpha halys (Hemiptera: Pentatomidae). J Pest Sci 88, 37–47 (2015). https://doi.org/10.1007/s10340-014-0582-6

Download citation

Keywords

  • Flight mill
  • Dispersal
  • Invasive species
  • BMSB