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Phenology, life table analysis and temperature requirements of the invasive brown marmorated stink bug, Halyomorpha halys, in Europe

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Abstract

The invasive Halyomorpha halys was accidentally introduced into Switzerland around 2004 and has recently established in the neighbouring countries of France and Italy. To better understand the population dynamics of this pest in Europe, the phenology, reproductive biology and temperature requirements of Swiss H. halys populations were investigated. Overwintered adults became active in April, but peak oviposition was not observed before early July. Individual females laid on average 79 eggs (maximum of 160). The oviposition period lasted from mid-June to end of September. Eggs laid in August and September did not result in offspring due to the low temperatures in autumn. Under natural fluctuating temperatures, development from egg to adult lasted between 60 and 131 days. The first new generation of adults did not occur before mid-August when the photoperiod was already below 15 h, which likely initiated diapause and suppressed the reproductive activity of new generation adults. Under controlled conditions of 20, 25 and 30 °C, Swiss H. halys populations developed within 75.8, 42.3 and 33.2 days from egg to adult, respectively. No development was possible at or below 15 and at or above 35 °C. The number of degree days required for completion of development from egg to adult was 588.24 DD. Under semi-natural conditions, total mortality of Swiss H. halys populations was 86.7 % with a net reproductive rate of 5.69, indicating growing populations. In Switzerland, H. halys is univoltine, but if it continues to spread into the Mediterranean area two generations per year could be expected.

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References

  • Arakawa R, Namura Y (2002) Effects of temperature on development of three Trissolcus spp. (Hymenoptera: Scelionidae), egg parasitoids of the brown marmorated stink bug, Halyomorpha halys (Hemiptera: Pentatomidae). Entomol Sci 5:215–218

    Google Scholar 

  • Arnold K (2009) Halyomorpha halys (Stål, 1855), eine für die europäische Fauna neu nachgewiesene Wanzenart (Insecta: Heteroptera: Pentatomidae: Cappaeini). Mitt Thüringer Entomol 16:19

    Google Scholar 

  • Ascerno ME (1991) Insect phenology and integrated pest management. J Arboric 17:13–15

    Google Scholar 

  • Bellows TS Jr, Van Driesche RG, Elkinton JS (1992) Life-table construction and analysis in the evaluation of natural enemies. Annu Rev Entomol 37:587–612

    Article  Google Scholar 

  • Bradshaw WE, Zani PA, Holzapfel CM (2004) Adaptation to temperate climates. Evolution 58:1748–1762

    Article  PubMed  Google Scholar 

  • Briere JF, Pracros P, Le Roux AY, Pierre JS (1999) A novel rate model of temperature-dependent development for arthropods. Environ Entomol 28:22–29

    Google Scholar 

  • Calabria G, Máca J, Bächli G, Serra L, Pascual M (2012) First records of the potential pest species Drosophila suzukii (Diptera: Drosophilidae) in Europe. J Appl Entomol 136:139–147

    Article  Google Scholar 

  • Callot H, Brua C (2013) Halyomorpha halys (Stål, 1855), la Punaise diabolique, nouvelle espèce pour la faune de France (Heteroptera Pentatomidae). L’Entomologiste 69:69–71

    Google Scholar 

  • Campbell A, Frazer BD, Gilbert N, Gutierrez AP, Mackauer M (1974) Temperature requirements of some aphids and their parasites. J Appl Ecol 11:431–438

    Article  Google Scholar 

  • EPPO (2013) EPPO Reporting Service No 5—Pest & Diseases, pp 10–11

  • Fujiie A (1985) Seasonal life cycle of Halyomorpha mista. Bull Chiba Agric Exp Stn 26:87–93

    Google Scholar 

  • Gariepy TD, Fraser H, Scott-Dupree CD (2013a) Brown marmorated stink bug (Hemiptera: Pentatomidae) in Canada: recent establishment, occurrence, and pest status in Southern Ontario. Can Entomol. doi:10.3752/cjai.2013.24

    Google Scholar 

  • Gariepy TD, Haye T, Zhang J (2013b) Occurrence, genetic diversity, and potential pathways of entry of Halyomorpha halys in newly-invaded areas of Canada and Switzerland. J Pest Sci. doi:10.1007/s10340-013-0529-3

    Google Scholar 

  • Haye T, Wyniger D (2013) Current distribution of Halyomorpha halys in Europe. http://www.halyomorphahalys.com. Accessed Nov 2013

  • Haye T, Mason PG, Dosdall L, Kuhlmann U (2010) Mortality factors affecting the cabbage seedpod weevil, Ceutorhynchus obstrictus (Marsham), in its area of origin: a life table analysis. Biol Control 54:331–341

    Article  Google Scholar 

  • Heckmann R (2012) Erster Nachweis von Halyomorpha halys (STÅL, 1855) (Heteroptera: Pentatomidae) für Deutschland. Heteropteron 36:17–18

    Google Scholar 

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

    Google Scholar 

  • Hoffmann WE (1931) A pentatomid pest of growing bean in south China. Peking Nat Hist Bull 5:25–26

    Google Scholar 

  • Hokkanen HMT (1993) Overwintering survival and spring emergence in Meligethes aeneus: effects of body weight, crowding, and soil treatment with Beauveria bassiana. Entomol Exp Appl 67:241–246

    Article  Google Scholar 

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

    Google Scholar 

  • Kawada H, Kitamura C (1983) The reproductive behaviour of the brown marmorated stink bug, Halyomorpha mista Uhler (Heteroptera: Pentatomidae). I. Observation of mating behavior and multiple copulation. Appl Entomol Zool 18:234–242

    Google Scholar 

  • Kenis M, Rabitsch W, Auger-Rozenberg MA, Roques A (2007) How can alien species inventories and interception data help us prevent insect invasions? Bull Entomol Res 97:489–502

    Article  CAS  PubMed  Google Scholar 

  • Kenis M, Nacambo S, Leuthardt FLG, di Domenico F, Haye T (2013) The box tree moth, Cydalima perspectalis, in Europe: Horticultural pest or environmental disaster? Alien 33:38–41

    Google Scholar 

  • Kiritani K (1997) The low development threshold temperature and the thermal constant in insects, mites, and nematodes in Japan. Misc Publ Nat Inst Agro-Environ Sci 21:1–72

    Google Scholar 

  • Lee DH, Short BD, Joseph SV, Bergh JC, Leskey TC (2013) Review of the biology, ecology, and management of Halyomorpha halys (Hemiptera: Pentatomidae) in China, Japan, and the Republic of Korea. Environ Entomol 42:627–641

    Article  PubMed  Google Scholar 

  • Leskey TC, Hamilton GC, Nielsen AL et al (2012a) Pest status of the brown marmorated stink bug, Halyomorpha halys in the USA. Outlooks Pest Manag 23:218–226

    Article  Google Scholar 

  • Leskey TC, Lee DH, Short BD, Wright SE (2012b) Impact of insecticides on the invasive Halyomorpha halys (Hemiptera: Pentatomidae): analysis of insecticide lethality. J Econ Entomol 105:1726–1735

    Article  CAS  PubMed  Google Scholar 

  • Leskey TC, Short BD, Butler BR, Wright SE (2012c) 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 2012:1–14

    Article  Google Scholar 

  • Leskey TC, Wright SE, Short BD, Khrimian A (2012d) Development of behaviorally based monitoring tools for the brown marmorated stink bug, Halyomorpha halys (Stål) (Heteroptera: Pentatomidae) in commercial tree fruit orchards. J Entomol Sci 47:76–85

    Google Scholar 

  • Mueller G, Luescher IL, Schmidt M (2011) New data on the incidence of household arthropod pests and new invasive pests in Zurich (Switzerland). Proceedings of the Seventh International Conference on Urban Pests, pp.99–104

  • 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

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Northeastern IPM Center (2013a) Where is BMSB? State by state. http://www.stopbmsb.org/where-is-bmsb/state-by-state/. Accessed 21 Nov 2013

  • Northeastern IPM (2013b) Host plants of the brown marmorated stink bug in the U.S. http://www.stopbmsb.org/where-is-bmsb/host-plants/. Accessed Jan 2014

  • Sauer C (2012) Die Marmorierte Baumwanze tritt neu im Deutschschweizer Gemüsebau auf. Extension Gemüsebau, Forschungsanstalt Agroscope Changins-Wädenswil, Gemüsebau Info 28(12):4–5

    Google Scholar 

  • Slobodkin LB (1962) Growth and regulation of population animal populations. Holt, Rinehart and Winston, New York

    Google Scholar 

  • Southwood TRE, Henderson PA (2000) Ecological methods. Blackwell, Oxford

    Google Scholar 

  • Talamas EJ, Buffington M, Hoelmer K (2013) New synonymy of Trissolcus halyomorphae Yang. J Hymenopt Res 33:113–117

    Article  Google Scholar 

  • United States Apple Association (2010) Asian pest inflicting substantial losses, raising alarm in eastern apple orchards. Apple News 41:488

    Google Scholar 

  • Van Driesche R, Hoddle M, Center T (2008) Control of pests and weeds by natural enemies: an introduction to biological control. Blackwell Publishing, Malden

    Google Scholar 

  • Watanabe M (1980) Study of the life cycle of the brown marmorated stink bug, Halyomorpha mista, by observing ovary development. Insectarium 17:168–173

    Google Scholar 

  • Wermelinger B, Wyniger D, Forster B (2008) First records of an invasive bug in Europe: Halyomorpha halys Stal (Heteroptera: Pentatomidae), a new pest on woody ornamentals and fruit trees? Mitt Schweiz Entomol Ges 81:1–8

    Google Scholar 

  • Werner DJ (2011) Die Amerikanische Koniferen-Samen- Wanze Leptoglossus occidentalis (Heteroptera: Coreidae) als Neozoon in Europa und in Deutschland: Ausbreitung und Biologie. Entomol heute 23:31–68

    Google Scholar 

  • Wyniger D, Kment P (2010) Key for the separation of Halyomorpha halys (Stål) from similar-appearing pentatomids (Insecta: Heteroptera: Pentatomidae) occurring in Central Europe, with new Swiss records. Mitt Schweiz Entomol Ges 83:261–270

    Google Scholar 

  • Xu J, Fonseca DM, Hamilton GC, Hoelmer KA, Nielsen AL (2013) Tracing the origin of US brown marmorated stink bugs, Halyomorpha halys. Biol Invasions. doi:10.1007/s10530-013-0510-3

    Google Scholar 

  • Yanagi T, Hagihara Y (1980) Ecology of the brown marmorated stink bug. Plant Prot 34:315–321

    Google Scholar 

  • Yang ZQ, Yao YX, Qiu LF, Li ZF (2009) A new species of Trissolcus (Hymenoptera: Scelionidae) parasitizing eggs of Halyomorpha halys (Heteroptera: Pentatomidae) in China with comments on its biology. Ann Entomol Soc Am 102:39–47

    Article  Google Scholar 

  • Zhang CT, Li DL, Su HF, Xu GL (1993) A study on the biological characteristics of Halyomorpha picus and Erthesina fullo. For Res 6:271–275

    Google Scholar 

  • 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  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

The authors are grateful to all Swiss homeowners who kindly allowed us to collect specimens on their property. We would like to thank Alyson Carter and Léna Durocher-Granger for technical assistance in the field and in the laboratory.

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Correspondence to T. Haye.

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Communicated by M. Traugott.

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Haye, T., Abdallah, S., Gariepy, T. et al. Phenology, life table analysis and temperature requirements of the invasive brown marmorated stink bug, Halyomorpha halys, in Europe. J Pest Sci 87, 407–418 (2014). https://doi.org/10.1007/s10340-014-0560-z

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