Journal of Pest Science

, Volume 92, Issue 1, pp 353–359 | Cite as

Effectiveness of Torymus sinensis: a successful long-term control of the Asian chestnut gall wasp in Italy

  • Chiara FerraciniEmail author
  • Ester Ferrari
  • Marianna Pontini
  • Matteo A. Saladini
  • Alberto Alma
Original Paper


The biocontrol agent Torymus sinensis has been released into Japan, the USA, and Europe to suppress the Asian chestnut gall wasp, Dryocosmus kuriphilus. In this study, we provide a quantitative assessment of T. sinensis effectiveness for suppressing gall wasp infestations in Northwest Italy by annually evaluating the percentage of chestnuts infested by D. kuriphilus (infestation rate) and the number of T. sinensis adults that emerged per 100 galls (emergence index) over a 9-year period. We recorded the number of T. sinensis adults emerging from a total of 64,000 galls collected from 23 sampling sites. We found that T. sinensis strongly reduced the D. kuriphilus population, as demonstrated by reduced galls and an increased T. sinensis emergence index. Specifically, in Northwest Italy, the infestation rate was nearly zero 9 years after release of the parasitoid with no evidence of resurgence in infestation levels. In 2012, the number of T. sinensis females emerging per 100 galls was approximately 20 times higher than in 2009. Overall, T. sinensis proved to be an outstanding biocontrol agent, and its success highlights how the classical biological control approach may represent a cost-effective tool for managing an exotic invasive pest.


Torymus sinensis Dryocosmus kuriphilus Classical biological control Invasive exotic pests 



The authors are grateful to Elvio Bellini (Chestnut Study and Documentation Centre), Lindsay K. Nova Hernández, Greta Pastorino, Cristina Pogolotti, and Ambra Quacchia for their precious help and cooperation in the laboratory and field activities, and to Daniela Di Silvestro and Giuseppe Siccardi of the Phytosanitary Service of Abruzzo and Liguria, respectively, for their cooperation. The authors would like to thank the referees for their valuable comments which helped to improve the manuscript.


This study was partially funded by the Ministry of Agricultural, Food and Forestry Policies (Lobiocin and Bioinfocast projects).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Human and animal rights

All the insect rearing and experiments were conducted in accordance with the legislation and guidelines of the European Union for the protection of animals used for scientific purposes ( All experimental protocols using insects were approved by the ad hoc Committee of DISAFA of the University of Torino.

Supplementary material

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Supplementary material 1 (DOCX 16 kb)
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Supplementary material 2 (DOCX 14 kb)
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Supplementary material 3 (DOCX 16 kb)


  1. Aebi A, Schönenberger N, Melika G, Quacchia A, Alma A, Stone GN (2007) Native introduced parasitoids attacking the invasive chestnut gall wasp Dryocosmus kuriphilus. EPPO Bull 37:166–171CrossRefGoogle Scholar
  2. Alma A, Ferracini C, Sartor C, Ferrari E, Botta R (2014) Il cinipide orientale del castagno: lotta biologica e sensibilità varietale. Italus Hortus 21:15–29Google Scholar
  3. Armentano G (2016) Cinipide del castagno: resta critica la situazione in alcune regioni. Inf Agrario 72(33):64–65Google Scholar
  4. Battisti A, Benvegnù I, Colombari F, Haack RA (2014) Invasion by the chestnut gall wasp in Italy causes significant yield loss in Castanea sativa nut production. Agric For Entomol 16:75–79CrossRefGoogle Scholar
  5. Bernardo U, Nugnes F, Gualtieri L, Scarpato S, Gargiulo G, Griffo R (2017) Cinipide del castagno, cresce il controllo biologico in Campania. Inf Agrario 73(27):51–53Google Scholar
  6. Borowiec N, Thaon M, Brancaccio L, Warot S, Vercken E, Fauvergue X, Ris N, Malausa JC (2014) Classical biological control against the chestnut gall wasp Dryocosmus kuriphilus (Hymenoptera, Cynipidae) in France. Plant Prot Q 29:7–10Google Scholar
  7. Bosio G, Armando M, Moriya S (2013) Verso il controllo biologico del cinipide del castagno. Inf Agrario 69(14):60–64Google Scholar
  8. Brussino G, Bosio G, Baudino M, Giordano R, Ramello F, Melika G (2002) Pericoloso insetto esotico per il castagno europeo. Inf Agrario 58(37):59–61Google Scholar
  9. Calabria G, Máca J, Bächli G, Serra L, Pascual M (2010) First records of the potential pest species Drosophila suzukii (Diptera: Drosophilidae) in Europe. J Appl Entomol 136:139–147CrossRefGoogle Scholar
  10. Clewley GD, Eschen R, Shaw RH, Wright DJ (2012) The effectiveness of classical biological control of invasive plants. J Appl Ecol 49:1287–1295CrossRefGoogle Scholar
  11. Cock MJ, Murphy ST, Kairo MT, Thompson E, Murphy RJ, Francis AW (2016) Trends in the classical biological control of insect pests by insects: an update of the BIOCAT database. Biocontrol 61:349–363CrossRefGoogle Scholar
  12. Colombari F, Battisti A (2016a) Native and introduced parasitoids in the biocontrol of Dryocosmus kuriphilus in Veneto (Italy). EPPO Bull 46:275–285CrossRefGoogle Scholar
  13. Colombari F, Battisti A (2016b) Spread of the introduced biocontrol agent Torymus sinensis in north-eastern Italy: dispersal through active flight or assisted by wind? Biocontrol 61:127–139CrossRefGoogle Scholar
  14. Cooper WR, Rieske LK (2007) Community associates of an exotic gallmaker, Dryocosmus kuriphilus (Hymenoptera: Cynipidae), in Eastern North America. Ann Entomol Soc Am 100:236–244CrossRefGoogle Scholar
  15. Cooper WR, Rieske LK (2011) A native and an introduced parasitoid utilize an exotic gall-maker host. Biocontrol 56:725–734CrossRefGoogle Scholar
  16. DeBach P (1964) Biological control of insect pests and weeds. Chapman & Hall, LondonGoogle Scholar
  17. DiTomaso JM, Van Steenwyk RA, Nowierski RM, Vollmer JL, Lane E, Chilton E, Burch P, Cowan PE, Zimmerman K, Dionigi CP (2017) Enhancing the effectiveness of biological control programs of invasive species through a more comprehensive pest management approach. Pest Manag Sci 73:9–13CrossRefGoogle Scholar
  18. EPPO (2014) First report of Popillia japonica in Italy. EPPO Reporting Service 10Google Scholar
  19. EPPO (2016) PQR—EPPO database on quarantine pests (available online). Accessed 21 March 2018
  20. Ferracini C, Ferrari E, Saladini MA, Pontini M, Corradetti M, Alma A (2015a) Non-target host risk assessment for the parasitoid Torymus sinensis. Biocontrol 60:583–594CrossRefGoogle Scholar
  21. Ferracini C, Gonella E, Ferrari E, Saladini MA, Picciau L, Tota F, Pontini M, Alma A (2015b) Novel insight in the life cycle of Torymus sinensis, biocontrol agent of the chestnut gall wasp. Biocontrol 60:169–177CrossRefGoogle Scholar
  22. Ferracini C, Ferrari E, Pontini M, Hernández Nova LK, Saladini MA, Alma A (2017) Post-release evaluation of non-target effects of Torymus sinensis, the biological control agent of Dryocosmus kuriphilus in Italy. Biocontrol 62:445–456CrossRefGoogle Scholar
  23. Ferracini C, Bertolino S, Bernardo U, Bonsignore C, Faccoli M, Ferrari E, Lupi D, Maini S, Mazzon L, Nugnes F, Rocco A, Santi F, Tavella L (2018) Do Torymus sinensis (Hymenoptera: Torymidae) and agroforestry system affect native parasitoids associated with the Asian chestnut gall wasp? Biol Control 121:36–43CrossRefGoogle Scholar
  24. Gehring E, Bellosi E, Quacchia A, Conedera M (2018) Assessing the impact of Dryocosmus kuriphilus on the chestnut tree: branch architecture matters. J Pest Sci 91:189–202CrossRefGoogle Scholar
  25. Gerber E, Schaffner U (2016) Review of invertebrate biological control agents introduced into Europe. CABI Publishing, WallingfordCrossRefGoogle Scholar
  26. Gyoutoku Y, Uemura M (1985) Ecology and biological control of the chestnut gall wasp, Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae), 1. Damage and parasitization in Kumamoto prefecture [Japan]. Proc Assoc Plant Prot Kyushu 31:213–215CrossRefGoogle Scholar
  27. Haack RA, Herard F, Sun JH, Turgeon JJ (2010) Managing invasive populations of Asian longhorned beetle and citrus longhorned beetle: a worldwide perspective. Annu Rev Entomol 55:521–546CrossRefGoogle Scholar
  28. İpekdal K, Emin A, Kuzucu AŞ, Karadağ M, Koçluk M, Açıcı Ö, Şah S, Aksu Y, Colombari F (2017) Rearing and releasing Torymus sinensis Kamijo (Hymenoptera: Torymidae), larval parasitoid of the chestnut gall wasp, Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae). Turkish Bull Entomol 7:113–129Google Scholar
  29. Kaartinen R, Stone GN, Hearn J, Lohse K, Roslin T (2010) Revealing secret liaisons: DNA barcoding changes our understanding of food webs. Ecol Entomol 35:623–638CrossRefGoogle Scholar
  30. Kos K, Kriston E, Melika G (2015) Invasive chestnut gall wasp Dryocosmus kuriphilus (Hymenoptera: Cynipidae), its native parasitoid community and association with oak gall wasps in Slovenia. Eur J Entomol 112:698–704CrossRefGoogle Scholar
  31. Matošević D, Melika G (2013) Recruitment of native parasitoids to a new invasive host: first results of Dryocosmus kuriphilus parasitoid assemblage in Croatia. Bull Insectol 66:231–238Google Scholar
  32. Matošević D, Quacchia A, Kriston É, Melika G (2014) Biological control of the invasive Dryocosmus kuriphilus (Hymenoptera: Cynipidae)—an overview and the first trials in Croatia. South East Eur For 5:3–12Google Scholar
  33. Matošević D, Lacković N, Kos K, Kriston E, Melika G, Rot M, Pernek M (2017) Success of classical biocontrol agent Torymus sinensis within its expanding range in Europe. J Appl Entomol 141:758–767CrossRefGoogle Scholar
  34. Montagna M, Gonella E, Pontini M, Ferrari E, Ferracini C, Alma A (2018) Molecular species delimitation of the Asian chestnut gall wasp biocontrol agent released in Italy. Insect Syst Evol. Google Scholar
  35. Moriya S, Inoue K, Mabuchi M (1990) The use of Torymus sinensis to control chestnut gall wasp, Dryocosmus kuriphilus, in Japan. Tech Bull 118:1–12 Food and Fertilizer Technology Center (FFTC) Google Scholar
  36. Moriya S, Shiga M, Adachi I (2003). Classical biological control of the chestnut gall wasp in Japan, In: Van Driesche RG (ed) Proceedings of the 1st international symposium on biological control of arthropods, Hawaii, 14–18 January 2002. USDA Forest Service, Washington, DC, USA, pp 407–415Google Scholar
  37. Murakami Y, Gyoutoku Y (1995) A delayed increase in the population of an imported parasitoid, Torymus (Syntomaspis) sinensis (Hymenoptera: Torymidae) in Kumamoto, southwestern Japan. Appl Entomol Zool 30:215–224CrossRefGoogle Scholar
  38. Palmeri V, Cascone P, Campolo O, Grande SB, Laudani F, Malacrinò A, Guerrieri E (2014) Hymenoptera wasps associated with the Asian gall wasp of chestnut (Dryocosmus kuriphilus) in Calabria, Italy. Phytoparasitica 42:699–702CrossRefGoogle Scholar
  39. Panzavolta T, Bernardo U, Bracalini M, Cascone P, Croci F, Gebiola M, Iodice L, Tiberi R, Guerrieri E (2013) Native parasitoids associated with Dryocosmus kuriphilus in Tuscany, Italy. Bull Insectol 66:195–201Google Scholar
  40. Paparella F, Ferracini C, Portaluri A, Manzo A, Alma A (2016) Biological control of the chestnut gall wasp with T. sinensis: a mathematical model. Ecol Model 338:17–36CrossRefGoogle Scholar
  41. Pérez-Otero R, Crespo D, Mansilla JP (2017) Dryocosmus kuriphilus Yasumatsu, 1951 (Hymenoptera: Cynipidae) in Galicia (NW Spain): pest dispersion, associated parasitoids and first biological control attempts. Arq Entomol 17:439–448Google Scholar
  42. Picciau L, Ferracini C, Alma A (2017) Reproductive traits in Torymus sinensis, biocontrol agent of the Asian chestnut gall wasp: implications for biological control success. Bull Insectol 70:49–55Google Scholar
  43. Quacchia A, Moriya S, Bosio G, Scapin G, Alma A (2008a) Rearing, release and settlement prospect in Italy of Torymus sinensis, the biological control agent of the chestnut gall wasp Dryocosmus kuriphilus. Biocontrol 53:829–839CrossRefGoogle Scholar
  44. Quacchia A, Ferracini C, Bonelli S, Balletto E, Alma A (2008b) Can the Geranium Bronze, Cacyreus marshalli, become a threat for European biodiversity? Biodivers Conserv 17:1429–1437CrossRefGoogle Scholar
  45. Quacchia A, Ferracini C, Nicholls JA, Piazza E, Saladini MA, Tota F, Melika G, Alma A (2013) Chalcid parasitoid community associated with the invading pest Dryocosmus kuriphilus in north-western Italy. Insect Conserv Divers 6:114–123CrossRefGoogle Scholar
  46. Quacchia A, Moriya S, Askew R, Schönrogge K (2014) Torymus sinensis: biology, host range and hybridization. Acta Hortic 1043:105–111CrossRefGoogle Scholar
  47. RefCast-Associação Portuguesa da Castanha (2015) Protocolo BioVespa, Luta Biológica contra a Vespa das Galhas do Castanheiro—Uma estratégia global. VI European Chestnut Meeting, Vila Pouca de Aguiar/Valpaços, Portugal, 9–12 September 2015Google Scholar
  48. Roques A, Rabitsch W, Rasplus J-Y, Lopez-Vamonde C, Nentwig W, Kenis M (2009) Alien terrestrial invertebrates of Europe. In: DAISIE (ed) Handbook of alien species in Europe. Springer, Berlin, pp 63–79CrossRefGoogle Scholar
  49. Shine C, Kettunen M, ten Brink P, Genovesi P, Gollasch S (2009) Technical support to EU strategy on invasive species (IAS)—Recommendations on policy options to control the negative impacts of IAS on biodiversity in Europe and the EU. Final report for the European Commission. Institute for European Environmental Policy (IEEP), Brussels, p 35Google Scholar
  50. Speranza S, Stacchiotti M, Paparatti B (2009) Endemic parasitoids of Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cinipidae) in Central Italy. In: IV International chestnut symposium 844:421–42Google Scholar
  51. Stiling P, Cornelissen T (2005) What makes a successful biocontrol agent? A meta-analysis of biological control agent performance. Biol Control 34:236–246CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Dipartimento di Scienze Agrarie, Forestali e Alimentari (DISAFA)University of TorinoGrugliascoItaly

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