Skip to main content

Advertisement

SpringerLink
Log in

Monitoring of the invasive Halyomorpha halys, a new key pest of fruit orchards in northern Italy

  • Original Paper
  • Published:
Journal of Pest Science Aims and scope Submit manuscript

Abstract

Halyomorpha halys is an invasive polyphagous pest with a high negative impact on fruit orchards and other agricultural crops in the USA. In Italy, it was first detected in 2012 in Emilia Romagna, a northern region that is among the major European tree fruit production areas. A specific monitoring programme using active techniques was carried out in pear orchards and adjacent uncultivated areas between 2014 and 2016 to assess the abundance, seasonality and impact of H. halys and other phytophagous Heteroptera in the field. It emerged that just a few years after first discovery, this invasive species already largely outnumbers all the other Heteroptera and that it is a season-long pest for pear crops. Severe yield losses are reported in different farms, especially on the orchard borders, with more than 50% deformed fruits. Mirids are mostly found in the grassy areas and crops, and the other phytophagous Heteroptera, only occasionally detected in the orchard trees, occur mainly on hedges and other crops. Our survey demonstrates for the first time the great damaging potential of H. halys as a new key pest of orchards in southern Europe. The study also identified the patterns of seasonal abundance of adults and nymphs in the orchards and their uncultivated surroundings, providing baseline data for the development of specific strategies for sustainable management.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Acebes-Doria AL, Leskey TC, Bergh JC (2016) Host plant effects on Halyomorpha halys (Hemiptera: Pentatomidae) nymphal development and survivorship. Environ Entomol 45:663–670

    Article  Google Scholar 

  • Bakken AJ, Schoof SC, Bickerton M et al (2015) Occurrence of brown marmorated stink bug (Hemiptera: Pentatomidae) on wild hosts in nonmanaged woodlands and soybean fields in North Carolina and Virginia. Environ Entomol 44:1011–1021

    Article  CAS  PubMed  Google Scholar 

  • Bariselli M, Bugiani R, Maistrello L (2016) Distribution and damage caused by Halyomorpha halys in Italy. EPPO Bull 46:332–334

    Article  Google Scholar 

  • Blaauw BR, Polk D, Nielsen AL (2015) IPM-CPR for peaches: incorporating behaviorally-based methods to manage Halyomorpha halys and key pests in peach. Pest Manag Sci 71:1513–1522

    Article  CAS  PubMed  Google Scholar 

  • Blaauw BR, Jones VP, Nielsen AL (2016) Utilizing immunomarking techniques to track Halyomorpha halys (Hemiptera: Pentatomidae) movement and distribution within a peach orchard. PeerJ 4:e1997. doi:10.7717/peerj.1997

    Article  PubMed  PubMed Central  Google Scholar 

  • Boivin G, Stewart RK (1983) Seasonal development and interplant movements of phytophagous mirids (Hemiptera: Miridae) on alternate host plants in and around an apple orchard. Ann Entomol Soc Am 76:776–780

    Article  Google Scholar 

  • Bortolotti P, Caruso S, Nannini R, et al (2012) Strategie per il contenimento dei Rincoti Miridi, agenti di deformazioni dei frutti di pero. In: Brunelli A, Canova A, Collina M (eds) Atti delle Giornate Fitopatologiche. CLUEB, Bologna, pp 139–142

  • Bro R, Smilde AK (2014) Principal component analysis. Anal Methods 6:2812–2831

    Article  CAS  Google Scholar 

  • Casoli L, Montermini A (2010) Risultati preliminari relativi ad un’indagine sulla popolazione di rincoti miridi in pereti della provincia di Reggio Emilia. In: Brunelli A, Canova A, Collina M (eds) Atti delle Giornate Fitopatologiche. CLUEB, Bologna, pp 87–88

  • Casoli L, Bortolotti P, Caruso S, et al (2012) Indagine su presenza e biologia di rincoti miridi in relazione alle deformazioni dei frutti, in pereti della provincia di Reggio Emilia. In: Brunelli A, Canova A, Collina M (eds) Atti delle Giornate Fitopatologiche. CLUEB, Bologna, pp 433–438

  • Cini A, Ioriatti C, Anfora G (2012) A review of the invasion of Drosophila suzukii in Europe and a draft research agenda for integrated pest management. Bull Insectology 65:149–160

    Google Scholar 

  • Costi E, Haye T, Maistrello L (2017) Biological parameters of the invasive brown marmorated stink bug, Halyomorpha halys, in southern Europe. J Pest Sci. doi:10.1007/s10340-017-0899-z

  • CREA (2015) Annuario dell’agricoltura italiana 2014. Consiglio per la ricerca in agricoltura e l’analisi dell’economia agraria, Roma

    Google Scholar 

  • Dioli P, Leo P, Maistrello L (2016) Prime segnalazioni in Spagna e in Sardegna della specie aliena Halyomorpha halys (Stål, 1855) e note sulla sua distribuzione in Europa (Hemiptera, Pentatomidae). Rev Gaditana Entomol 7:539–548

    Google Scholar 

  • EUROSTAT (2017) The fruit and vegetable sector in the EU—a statistical overview—Statistics Explained. http://ec.europa.eu/eurostat/statistics-explained/index.php/The_fruit_and_vegetable_sector_in_the_EU_-_a_statistical_overview#Fruit:_holdings.2C_areas_and_production. Accessed 15 Jan 2017

  • Fanfani R, Pieri R (2016) Il sistema agro-alimentare dell’Emilia-Romagna. Rapporto 2015. Unione regionale delle Camere di commercio dell’Emilia-Romagna Regione Emilia-Romagna, Assessorato agricoltura, caccia e pesca, Bologna

  • Fleury D, Mauffette Y, Methot S, Vincent C (2010) Activity of Lygus lineolaris (Heteroptera: Miridae) adults monitored around the periphery and inside a commercial vineyard. Eur J Entomol 107:527–534

    Article  Google Scholar 

  • 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 

  • 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

    Article  Google Scholar 

  • Haye T, Gariepy T, Hoelmer K et al (2015) Range expansion of the invasive brown marmorated stinkbug, Halyomorpha halys: an increasing threat to field, fruit and vegetable crops worldwide. J Pest Sci 88:665–673

    Article  Google Scholar 

  • 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 

  • Joseph SV, Stallings JW, Leskey TC et al (2014) Spatial distribution of brown marmorated stink bug (Hemiptera: Pentatomidae) injury at harvest in mid-Atlantic apple orchards. J Econ Entomol 107:1839–1848

    Article  PubMed  Google Scholar 

  • Kondorosy E, Markó V, Cross J (2010) Heteropteran fauna of apple orchards in south-east England. Acta Phytopathol Entomol Hung 45:173–193

    Article  Google Scholar 

  • Lee D-H, Short BD, Joseph SV et al (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 D-H, 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 J Entomol. doi:10.1155/2012/535062

    Google Scholar 

  • Leskey TC, Short BD, Lee D-H (2014) Efficacy of insecticide residues on adult Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) mortality and injury in apple and peach orchards. Pest Manag Sci 70:1097–1104

    Article  CAS  PubMed  Google Scholar 

  • Macavei L, Bǎeţan R, Oltean I et al (2015) First detection of Halyomorpha halys, a new invasive species with a high potential of damage on agricultural crops in Romania. Lucr Stiintifice Ser Agron 58:105–108

    Google Scholar 

  • Maistrello L, Dioli P, Bariselli M et al (2016) Citizen science and early detection of invasive species: phenology of first occurrences of Halyomorpha halys in southern Europe. Biol Invasions 18:3109–3116

    Article  Google Scholar 

  • Massart DL, Vandeginste BGM, Buydens LMC et al (1997) Handbook of chemometrics and qualimetrics. Elsevier, Amsterdam

    Google Scholar 

  • Maurel JP, Blaye G, Valladares L et al (2016) Halyomorpha halys (Stål, 1855), la punaise diabolique en France, à Toulouse (Heteroptera; Pentatomidae). Carnets Nat 3:21–25

    Google Scholar 

  • Milonas PG, Partsinevelos GK (2014) First report of brown marmorated stink bug Halyomorpha halys Stål (Hemiptera: Pentatomidae) in Greece. EPPO Bull 44:183–186. doi:10.1111/epp.12129

    Article  Google Scholar 

  • Mityushev IM (2016) First record of marmorated bug detection in Russia. Zashchita Karantin Rasteniĭ 3:48

    Google Scholar 

  • Morrison WR III, Lee D-H, Short BD, et al (2016) Establishing the behavioral basis for an attract-and-kill strategy to manage the invasive Halyomorpha halys in apple orchards. J Pest Sci 89:81–96. doi:10.1007/s10340-015-0679-6

  • Nielsen AL, Hamilton GC (2009a) Life history of the invasive species Halyomorpha halys (Hemiptera: Pentatomidae) in northeastern US. Ann Entomol Soc Am 102:608–616

    Article  Google Scholar 

  • Nielsen AL, Hamilton GC (2009b) Seasonal occurrence and impact of Halyomorpha halys (Hemiptera: Pentatomidae) in tree fruit. J Econ Entomol 102:1133–1140

    Article  PubMed  Google Scholar 

  • 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 

  • Rabitsch W, Friebe GJ (2015) From the west and from the east? First records of Halyomorpha halys (Stål, 1855) (Hemiptera: Heteroptera: Pentatomidae) in Vorarlberg and Vienna. Beitr Entomof 16:115–139

    Google Scholar 

  • Regione Emilia Romagna (2016) Disciplinari di produzione integrata vegetale—Produzioni agroalimentari—E-R Agricoltura e pesca. http://agricoltura.regione.emilia-romagna.it/produzioni-agroalimentari/temi/disciplinari-produzione-integrata. Accessed 29 Dec 2016

  • Simov N (2016) The invasive brown marmorated stink bug Halyomorpha halys (Stål 1855 (Heteroptera: Pentatomidae) already in Bulgaria. Ecol Montenegrina 9:51–53

    Google Scholar 

  • Tavella L, Arzone A, Alma A, Galliano A (1996) IPM application in peach orchards against Lygus rugulipennis Poppius. In: Polesny F, Muller W, Olszak RW (eds) Iobc/Wprs and Ishs International Conference on Integrated Fruit Production, Proceedings of the Meeting. International Society Horticultural Science, Leuven 1, pp 160–164

  • USDA-NIFA SCRI (2017) Stop BMSB. Biology, ecology, and management of brown marmorated stink bug in specialty crop. In: Stop BMSB. http://www.stopbmsb.org. Accessed 20 Jan 2017

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This research was partially supported by the grant “Innovative tools and protocols for monitoring and sustainable control of the alien stink bug Halyomorpha halys, a new phytosanitary threat, and of other harmful heteropterans for the fruit crops of the territory of Modena” (2013.065) of “Fondazione Cassa di Risparmio di Modena”. The farm owners and the following producers associations of Modena Province are thanked for their support: Agrintesa, Fruit Modena Group, ApoFuit, Cipof, ItalFrutta, Sant’Adriano, Consorzio Agrario dell’Emilia. We are also grateful to the students and trainees who participated in the fieldwork. The anonymous referees are thanked for their suggestions useful to improve the manuscript.

Author information

Authors and Affiliations

  1. Dipartimento di Scienze della Vita, Università di Modena e Reggio Emilia, Via G. Amendola 2, 42122, Reggio Emilia, Italy

    Lara Maistrello, Elena Costi, Sara Bortolini, Laura Macavei, Giorgia Foca & Alessandro Ulrici

  2. Consorzio Fitosanitario di Modena, Via Santi Venceslao 14, 41123, Modena, Italy

    Giacomo Vaccari, Stefano Caruso, Pier Paolo Bortolotti, Roberta Nannini & Massimo Fornaciari

  3. Consorzio Fitosanitario di Reggio Emilia, Via Gualerzi 32, 42124, Reggio Emilia, Italy

    Luca Casoli

  4. Servizio Fitosanitario Regione Emilia Romagna, Via di Corticella 133, 40128, Bologna, Italy

    Gian Lorenzo Mazzoli

  5. Museo Civico di Storia Naturale di Milano, Corso Venezia 55, 20121, Milan, Italy

    Paride Dioli

Authors
  1. Lara Maistrello
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Giacomo Vaccari
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Stefano Caruso
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Elena Costi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sara Bortolini
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Laura Macavei
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Giorgia Foca
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Alessandro Ulrici
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Pier Paolo Bortolotti
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Roberta Nannini
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Luca Casoli
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Massimo Fornaciari
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Gian Lorenzo Mazzoli
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Paride Dioli
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lara Maistrello.

Ethics declarations

Conflict of interest

All authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals (vertebrate) performed by any of the authors.

Informed consent

Informed consent was obtained from all individual participants included in the study

Additional information

Communicated by D. C. Weber.

Special Issue: The brown marmorated stink bug Halyomorpha halys an emerging pest of global concern.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Maistrello, L., Vaccari, G., Caruso, S. et al. Monitoring of the invasive Halyomorpha halys, a new key pest of fruit orchards in northern Italy. J Pest Sci 90, 1231–1244 (2017). https://doi.org/10.1007/s10340-017-0896-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10340-017-0896-2

Keywords

Search

Navigation