Journal of Pest Science

, Volume 88, Issue 3, pp 461–468 | Cite as

Fruit availability influences the seasonal abundance of invasive stink bugs in ornamental tree nurseries

  • Holly M. MartinsonEmail author
  • P. Dilip Venugopal
  • Erik J. Bergmann
  • Paula M. Shrewsbury
  • Michael J. Raupp
Rapid Communication


Invasive plant-feeding insects cause billions of dollars in economics losses annually around the world. Understanding how they utilize different host plants directly informs their management. The highly invasive brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), has destroyed crops and invaded homes since its discovery in the U.S. in the mid-1990s. In this study, we test the hypothesis that in diverse resource environments, the presence and maturity of fruits on trees influences the abundance of H. halys. Observational surveys of the abundance of H. halys life stages (egg masses, nymphs, and adults) on 3884 trees of 223 cultivars in woody plant nurseries revealed that fruit maturity was a strong predictor of the seasonal abundance and within-tree distribution of H. halys. We next explicitly tested whether fruits themselves were the key resource for H. halys through a manipulative field experiment. Removal of fruits from trees suppressed stink bug abundance throughout the season. Despite being considered a broad feeding generalist, our results highlight that in landscapes with highly heterogeneous and ephemeral resources, H. halys specializes on finding mature fruits. Therefore, H. halys can be controlled by designing landscapes with fruitless varieties of popular trees, exploiting phenological mismatches between the pest and its host plants, and through targeted management of H. halys on fruiting trees in the landscape.


Fruit phenology Halyomorpha halys Invasive species Ornamental plants Resource heterogeneity 



We are grateful to Steve Black and Kelly Lewis for field access and to Stokes Aker, Kevin Beiter, Caroline Brodo, Sean Harris, Colleen McMullen, Dylan Reisinger, Christopher Riley, Kris Keochinda, and Ryan Wallace for field assistance. This work was supported by funds from the USDA National Institute of Food and Agriculture McIntire-Stennis Project (Project No. 1003486) and the USDA NIFA Specialty Crop Research Initiative (Award 2011-51181-30937).


  1. Aukema JE, Leung B, Kovacs K et al (2011) Economic impacts of non-native forest insects in the continental United States. PLoS One 6:e24587. doi: 10.1371/journal.pone.0024587 PubMedCentralCrossRefPubMedGoogle Scholar
  2. Bates D, Maechler M, Bolker B, Walker S (2014) lme4: linear mixed-effects models using Eigen and S4. R package version 1.1–7Google Scholar
  3. Behmer ST (2009) Insect herbivore nutrient regulation. Annu Rev Entomol 54:165–187. doi: 10.1146/annurev.ento.54.110807.090537 CrossRefPubMedGoogle Scholar
  4. Behmer ST, Simpson SJ, Raubenheimer D (2002) Herbivore foraging in chemically heterogeneous environments: nutrients and secondary metabolites. Ecology 83:2489–2501. doi: 10.1890/0012-9658(2002)083[2489:HFICHE]2.0.CO;2
  5. Bergmann EJ, Bernhard KM, Bernon G, et al (2014) Host plants of the brown marmorated stink bug in the U.S. BMSB IPM working group & Northeastern IPM centerGoogle Scholar
  6. Bernays EA, Minkenberg OPJM (1997) Insect herbivores: different reasons for being a generalist. Ecology 78:1157–1169. doi: 10.2307/2265866
  7. Bolker BM, Brooks ME, Clark CJ et al (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135. doi: 10.1016/j.tree.2008.10.008 CrossRefPubMedGoogle Scholar
  8. Carvalheiro LG, Buckley YM, Memmott J (2010) Diet breadth influences how the impact of invasive plants is propagated through food webs. Ecology 91:1063–1074. doi: 10.1890/08-2092.1 CrossRefPubMedGoogle Scholar
  9. Cesari M, Maistrello L, Ganzerli F et al (2014) A pest alien invasion in progress: potential pathways of origin of the brown marmorated stink bug Halyomorpha halys populations in Italy. J Pest Sci 88:1–7. doi: 10.1007/s10340-014-0634-y CrossRefGoogle Scholar
  10. Desurmont GA, Pearse IS (2014) Alien plants versus alien herbivores: does it matter who is non-native in a novel trophic interaction? Curr Opin Insect Sci 2:20–25. doi: 10.1016/j.cois.2014.06.006 CrossRefGoogle Scholar
  11. Desurmont GA, Donoghue MJ, Clement WL, Agrawal AA (2011) Evolutionary history predicts plant defense against an invasive pest. Proc Natl Acad Sci 108:7070–7074. doi: 10.1073/pnas.1102891108 PubMedCentralCrossRefPubMedGoogle Scholar
  12. Eubanks MD, Denno RF (1999) The ecological consequences of variation in plants and prey for an omnivorous insect. Ecology 80:1253–1266. doi: 10.1890/0012-9658(1999)080[1253:TECOVI]2.0.CO;2
  13. Eubanks MD, Styrsky JD, Denno RF (2003) The evolution of omnivory in heteropteran insects. Ecology 84:2549–2556. doi: 10.1890/02-0396 CrossRefGoogle Scholar
  14. Fagan WF, Siemann E, Mitter C et al (2002) Nitrogen in insects: implications for trophic complexity and species diversification. Am Nat 160:784–802. doi: 10.1086/343879 CrossRefPubMedGoogle Scholar
  15. Forister ML, Wilson JS (2013) The population ecology of novel plant–herbivore interactions. Oikos 122:657–666. doi: 10.1111/j.1600-0706.2013.00251.x CrossRefGoogle Scholar
  16. Fox J (2003) Effect displays in R for generalised linear models. J Stat Softw 8:1–27Google Scholar
  17. Fox J, Wiesberg S (2011) An R companion to applied regression, 2nd edn. Sage Publications, Thousand OaksGoogle Scholar
  18. Freeland WJ, Janzen DH (1974) Strategies in herbivory by mammals: the role of plant secondary compounds. Am Nat 108:269–289CrossRefGoogle Scholar
  19. Gandhi KJ, Herms DA (2010) Direct and indirect effects of alien insect herbivores on ecological processes and interactions in forests of eastern North America. Biol Invasions 12:389–405. doi: 10.1007/s10530-009-9627-9 CrossRefGoogle Scholar
  20. 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. doi: 10.1007/s10340-013-0529-3 CrossRefGoogle Scholar
  21. Guglielmo CG, Karasov WH, Jakubas WJ (1996) Nutritional costs of a plant secondary metabolite explain selective foraging by ruffed grouse. Ecology 77:1103–1115. doi: 10.2307/2265579 CrossRefGoogle Scholar
  22. 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 87:407–418. doi: 10.1007/s10340-014-0560-z Google Scholar
  23. 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 105:225–237Google Scholar
  24. Holtz T, Kamminga KL (2010) Qualitative analysis of the pest risk potential of the brown marmorated stink bug (BMSB), Halyomorpha halys (Stål), in the United States. USDA APHIS PPQGoogle Scholar
  25. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363. doi: 10.1002/bimj.200810425 CrossRefPubMedGoogle Scholar
  26. Inkley DB (2012) Characteristics of home invasion by the brown marmorated stink bug (Hemiptera: Pentatomidae). J Entomol Sci 47:125–130Google Scholar
  27. Kennedy GG, Storer NP (2000) Life systems of polyphagous arthropod pests in temporally unstable cropping systems. Annu Rev Entomol 45:467–493. doi: 10.1146/annurev.ento.45.1.467 CrossRefPubMedGoogle Scholar
  28. Leskey TC, Hamilton GC, Nielsen AL et al (2012) Pest status of the brown marmorated stink bug, Halyomorpha halys in the USA. Outlooks Pest Manag 23:218–226. doi: 10.1564/23oct07 CrossRefGoogle Scholar
  29. Liebhold AM, MacDonald WL, Bergdahl D, Mastro VC (1995) Invasion by exotic forest pests: a threat to forest ecosystems. For Sci 41:a0001–z0001Google Scholar
  30. Mattson WJ Jr (1980) Herbivory in relation to plant nitrogen content. Annu Rev Ecol Syst 11:119–161CrossRefGoogle Scholar
  31. Nielsen AL, Hamilton GC (2009) Life history of the invasive species Halyomorpha halys (Hemiptera: Pentatomidae) in northeastern United States. Ann Entomol Soc Am 102:608–616. doi: 10.1603/008.102.0405 CrossRefGoogle Scholar
  32. Panizzi AR (1997) Wild hosts of Pentatomids: ecological significance and role in their pest status on crops. Annu Rev Entomol 42:99–122. doi: 10.1146/annurev.ento.42.1.99 CrossRefPubMedGoogle Scholar
  33. Parker JD, Burkepile DE, Hay ME (2006) Opposing effects of native and exotic herbivores on plant invasions. Science 311:1459–1461. doi: 10.1126/science.1121407 CrossRefPubMedGoogle Scholar
  34. Pearse IS, Altermatt F (2013) Predicting novel trophic interactions in a non-native world. Ecol Lett 16:1088–1094. doi: 10.1111/ele.12143 CrossRefPubMedGoogle Scholar
  35. Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52:273–288. doi: 10.1016/j.ecolecon.2004.10.002 CrossRefGoogle Scholar
  36. Pinheiro JC, Bates DM (2000) Mixed effects models in S and S-Plus. Springer, New YorkCrossRefGoogle Scholar
  37. R Core Team (2014) R: A language and environment for statistical computing. R foundation for statistical computing, ViennaGoogle Scholar
  38. Rice KB, Bergh CJ, Bergmann EJ et al (2014) Biology, ecology, and management of brown marmorated stink bug (Hemiptera: Pentatomidae). J Integr Pest Manag 5:1–13. doi: 10.1603/IPM14002 CrossRefGoogle Scholar
  39. Sala OE, Chapin FS et al (2000) Global Biodiversity Scenarios for the Year 2100. Science 287:1770–1774. doi: 10.1126/science.287.5459.1770 CrossRefPubMedGoogle Scholar
  40. Simpson SJ, Raubenheimer D (1993) A multi-level analysis of feeding behaviour: the geometry of nutritional decisions. Philos Trans R Soc Lond B Biol Sci 342:381–402. doi: 10.1098/rstb.1993.0166 CrossRefGoogle Scholar
  41. Venugopal PD, Coffey PL, Dively GP, Lamp WO (2014) Adjacent habitat influence on stink bug (Hemiptera: Pentatomidae) densities and the associated damage at field corn and soybean edges. PLoS One 9:e109917. doi: 10.1371/journal.pone.0109917 PubMedCentralCrossRefPubMedGoogle Scholar
  42. Venugopal PD, Martinson HM, Bergmann EJ et al (2015) Edge effects influence the abundance of the invasive Halyomorpha halys (Hemiptera: Pentatomidae) in woody plant nurseries. Environ Entomol 44:474–479. doi: 10.1093/ee/nvv061 Google Scholar
  43. Vitousek PM (1994) Beyond global warming: ecology and global change. Ecology 75:1861–1876. doi: 10.2307/1941591 CrossRefGoogle Scholar
  44. Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer, New YorkCrossRefGoogle Scholar
  45. Wiman NG, Walton VM, Shearer PW et al (2015) Factors affecting flight capacity of brown marmorated stink bug, Halyomorpha halys (Hemiptera: Pentatomidae). J Pest Sci 88:37–47. doi: 10.1007/s10340-014-0582-6 Google Scholar
  46. Zuur AF, Ieno EN, Walker N et al (2009) Mixed effects models and extensions in ecology with R. Springer, New YorkCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Holly M. Martinson
    • 1
    Email author
  • P. Dilip Venugopal
    • 1
  • Erik J. Bergmann
    • 1
  • Paula M. Shrewsbury
    • 1
  • Michael J. Raupp
    • 1
  1. 1.Department of EntomologyUniversity of MarylandCollege ParkUSA

Personalised recommendations