Advertisement

Journal of Pest Science

, Volume 92, Issue 1, pp 361–369 | Cite as

Tracking seasonal emergence dynamics of an invasive gall wasp and its associated parasitoids with an open-source, microcontroller-based device

  • Gabriele RondoniEmail author
  • Carlo Ricci
  • Eric Conti
Original Paper
  • 80 Downloads

Abstract

The invasive Asian chestnut gall wasp, Dryocosmus kuriphilus (Hymenoptera: Cynipidae), is one of the most economically important pests of chestnut forest systems. Control is either based on the use of pesticides or the release of the parasitoid Torymus sinensis (Torymidae) for classical biological control of the pest. Both approaches require frequent monitoring of wasp emergence patterns, usually by recording adult emergence from samples of galls stored in dark boxes. Here, we have improved this monitoring method by developing and evaluating a microcontroller-based device. Cages in which galls were placed were modified by insertion of a turntable, which automatically separates wasps emerging at different times. We used this device to monitor the seasonal emergence of D. kuriphilus, its coevolved parasitoid T. sinensis and newly associated native parasitoids from fresh or overwintered chestnut galls formed in 2013 and 2014. In summer, native parasitoids (3.6 and 5.8% of 2-year parasitism) associated with current-year chestnut galls started emerging before the gall wasp and only partially overlapped with D. kuriphilus emergence. After overwintering, in the spring of the following year, T. sinensis (4.3 and 5.5% of 2-year parasitism from overwintered galls) emerged earlier than indigenous parasitoids (1.6 and 4.8%) and indicated potential for D. kuriphilus control. Overall, 14 species of native parasitoids belonging to five families were recorded from fresh and overwintered galls. We provide the schematic and the programming codes for this new device and propose that this automatic device be used to better track the flight periods of D. kuriphilus and its parasitoids.

Keywords

Dryocosmus kuriphilus Cynipidae Torymus sinensis Biological control Integrated pest management Parasitoid efficacy 

Notes

Acknowledgements

Authors would like to thank Davide Pettorossi, Marida Corradetti, Quirino Santini, Daniela Fortini and Luciana Bartoli for assistance and technical support.

Funding

Personal funding to GR was provided by ‘Cassa di Risparmio di Perugia’ Foundation and by PSR UMBRIA 2014–2020, mis. 19.2, ‘PAL GAL Media Valle del Tevere’. Work was supported by PSR UMBRIA 2007-2013, mis. 1.2.4 project ‘CoBiot.’

Compliance with ethical standards

Conflict of interest

The authors have declared that no conflict of interest exists.

Human and animal rights

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

Supplementary material

10340_2018_1037_MOESM1_ESM.docx (112 kb)
Supplementary material 1 (DOCX 111 kb)

References

  1. Abe Y, Ide T, Wachi N (2011) Discovery of a new gall-inducing species in the inquiline tribe Synergini (Hymenoptera: Cynipidae): inconsistent implications from biology and morphology. Ann Entomol Soc Am 104:115–120CrossRefGoogle Scholar
  2. Aebi A, Schönrogge K, Melika G, Alma A, Bosio G, Quacchia A et al (2006) Parasitoid recruitment to the globally invasive chestnut gall wasp Dryocosmus kuriphilus. In: Ozaki K, Yukawa J, Ohgushi T, Price PW (eds) Ecology and evolution of galling arthropods and their associates. Springer, Tokyo, pp 103–121CrossRefGoogle Scholar
  3. Aebi A, Schonrogge K, Melika G, Quacchia A, Alma A, Stone GN (2007) Native and introduced parasitoids attacking the invasive chestnut gall wasp Dryocosmus kuriphilus. IOBC WPRS Bull 37:166–171Google Scholar
  4. Aebi A, Schoenenberger N, Bigler F (2011) Evaluating the use of Torymus sinensis against the chestnut gall wasp Dryocosmus kuriphilus in the Canton Ticino, Switzerland. Agroscope Reckenholz-Tänikon, ZürichGoogle Scholar
  5. 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
  6. Bernardo U, Iodice L, Sasso R, Tutore VA, Cascone P, Guerrieri E (2013) Biology and monitoring of Dryocosmus kuriphilus on Castanea sativa in Southern Italy. Agric For Entomol 15:65–76CrossRefGoogle Scholar
  7. Böckmann E, Hommes M, Meyhöfer R (2015) Yellow traps reloaded: What is the benefit for decision making in practice? J Pest Sci 88:439–449CrossRefGoogle Scholar
  8. Bonal R, Vargas-Osuna E, Mena JD, Aparicio JM, Santoro M, Martín A (2018) Looking for variable molecular markers in the chestnut gall wasp Dryocosmus kuriphilus: first comparison across genes. Sci Rep 8:5631CrossRefGoogle Scholar
  9. Bosio G, Gerbaudo C, Piazza E (2009) Dryocosmus kuriphilus Yasumatsu: an outline seven years after the first report in Piedmont (Italy). Acta Hortic 866:341–348Google Scholar
  10. Boukili VKS, Hoopes MF, Briggs CJ (2007) Effect of microenvironment on development of a gall midge. Environ Entomol 36:441–450CrossRefGoogle Scholar
  11. Brussino G, Bosio G, Baudino M, Giordano R, Ramello F, Melika G (2002) A dangerous exotic insect threatening European chestnut. Inf Agrar 58:59–61 (Italian) Google Scholar
  12. Buchholz S (2009) Design of a time-sorting pitfall trap for surface-active arthropods. Entomol Exp Appl 133:100–103CrossRefGoogle Scholar
  13. Colombari F, Battisti A (2016) Native and introduced parasitoids in the biocontrol of Dryocosmus kuriphilus in Veneto (Italy). EPPO Bull 46:275–285CrossRefGoogle Scholar
  14. Comont RF, Purse BV, Phillips W, Kunin WE, Hanson M, Lewis OT et al (2014) Escape from parasitism by the invasive alien ladybird, Harmonia axyridis. Insect Conserv Divers 7:334–342CrossRefGoogle Scholar
  15. 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
  16. Cooper WR, Rieske LK (2010) Gall structure affects ecological associations of Dryocosmus kuriphilus (Hymenoptera: Cynipidae). Environ Entomol 39:787–797CrossRefGoogle Scholar
  17. Corbett A, Rosenheim JA (1996) Quantifying movement of a minute parasitoid, Anagrus epos (Hymenoptera: Mymaridae), using fluorescent dust marking and recapture. Biol Control 6:35–44CrossRefGoogle Scholar
  18. Csóka G, Stone G, Melika G (2017) Non-native gall-inducing insects on forest trees: a global review. Biol Invasions 19:3161–3181CrossRefGoogle Scholar
  19. EFSA Panel on Plant Health (2010) Risk assessment of the oriental chestnut gall wasp, Dryocosmus kuriphilus for the EU territory and identification and evaluation of risk management options. EFSA J 8:1–114Google Scholar
  20. EPPO (2017) PQR—EPPO database on quarantine pests. http://eppo.int. Accessed 28 Dec 2017
  21. Ferracini C, Ingegno BL, Navone P, Ferrari E, Mosti M, Tavella L, Alma A (2012) Adaptation of indigenous larval parasitoids to Tuta absoluta (Lepidoptera: Gelechiidae) in Italy. J Econ Entomol 105:1311–1319CrossRefGoogle Scholar
  22. 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
  23. Ferracini C, Gonella E, Ferrari E, Saladini MA, Picciau L, Tota F et al (2015b) Novel insight in the life cycle of Torymus sinensis, biocontrol agent of the chestnut gall wasp. Biocontrol 60:169–177CrossRefGoogle Scholar
  24. Ferracini C, Ferrari E, Pontini M, Nova LKH, 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
  25. Francati S, Alma A, Ferracini C, Pollini A, Dindo ML (2015) Indigenous parasitoids associated with Dryocosmus kuriphilus in a chestnut production area of Emilia Romagna (Italy). Bull Insectol 68:127–134Google Scholar
  26. Gibbs M, Schonrogge K, Alma A, Melika G, Quacchia A, Stone GN, Aebi A (2011) Torymus sinensis: A viable management option for the biological control of Dryocosmus kuriphilus in Europe? Biocontrol 56:527–538CrossRefGoogle Scholar
  27. Girardoz S, Kenis M, Quicke DL (2006) Recruitment of native parasitoids by an exotic leaf miner, Cameraria ohridella: host-parasitoid synchronization and influence of the environment. Agric For Entomol 8:49–56CrossRefGoogle Scholar
  28. Graziosi I, Rieske LK (2014) Potential fecundity of a highly invasive gall maker, Dryocosmus kuriphilus (Hymenoptera: Cynipidae). Environ Entomol 43:1053–1058CrossRefGoogle Scholar
  29. Graziosi I, Santi F (2008) Chestnut gall wasp (Dryocosmus kuriphilus): spreading in Italy and new records in Bologna province. Bull Insectol 61:343–348Google Scholar
  30. Hill AP, Prince P, Covarrubias EP, Doncaster CP, Snaddon JL, Rogers A (2018) AudioMoth: evaluation of a smart open acoustic device for monitoring biodiversity and the environment. Methods Ecol Evol 9:1199–1211CrossRefGoogle Scholar
  31. Kato K, Hijii N (1997) Effects of gall formation by Dryocosmus kuriphilus Yasumatsu (Hym., Cynipidae) on the growth of chestnut trees. J Appl Entomol 121:9–15CrossRefGoogle Scholar
  32. Kato K, Hijii N (1999) Mortality factors of the chestnut gall-wasp, Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae) after gall formation. Entomol Sci 2:483–491Google Scholar
  33. Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170CrossRefGoogle Scholar
  34. 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
  35. Maltoni A, Mariotti B, Tani A (2012) Case study of a new method for the classification and analysis of Dryocosmus kuriphilus Yasumatsu damage to young chestnut sprouts. iForest 5:50–59CrossRefGoogle Scholar
  36. Martorana L, Foti MC, Rondoni G, Conti E, Colazza S, Peri E (2017) An invasive insect herbivore disrupts plant volatile-mediated tritrophic signalling. J Pest Sci 90:1079–1085CrossRefGoogle Scholar
  37. Millar J, Paine T, Campbell C, Hanks L (2002) Methods for rearing Syngaster lepidus and Jarra phoracantha (Hymenoptera: Braconidae), larval parasitoids of the phloem-colonizing longhorned beetles Phoracantha semipunctata and P. recurva (Coleoptera: Cerambycidae). Bull Entomol Res 92:141–146CrossRefGoogle Scholar
  38. Moriya S, Masakazu S, Ishizue A (2002) Classical biological control of the chestnut gall wasp in Japan. In: 1st international symposium on biological control of arthropods, Waikiki, Japan, pp 407–415Google Scholar
  39. Murakami Y, Tokuhisa E (1985) Behavioural sequences of oviposition and host-feeding of Torymus (Syntomaspis) beneficus Yasumatsu et Kamijo (Hymenoptera: Torymidae), a native parasitoid of Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae). Appl Entomol Zool 20:43–49CrossRefGoogle Scholar
  40. Paine TD, Joyce AL, Millar JG, Hanks LM (2004) Effect of variation in host size on sex ratio, size, and survival of Syngaster lepidus, a parasitoid of Eucalyptus longhorned beetles (Phoracantha spp.): II. Biol Control 30:374–381CrossRefGoogle Scholar
  41. Panzavolta T, Bracalini M, Croci F, Campani C, Bartoletti T, Miniati G et al (2011) Asian chestnut gall wasp in Tuscany: gall characteristics, egg distribution and chestnut cultivar susceptibility. Agric For Entomol 14:139–145CrossRefGoogle Scholar
  42. Panzavolta T, Bernardo U, Bracalini M, Cascone P, Croci F, Gebiola M et al (2013) Native parasitoids associated with Dryocosmus kuriphilus in Tuscany, Italy. Bull Insectol 66:195–201Google Scholar
  43. 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
  44. Quacchia A, Moriya S, Bosio G, Scapin I, Alma A (2008) 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
  45. Quacchia A, Ferracini C, Nicholls JA, Piazza E, Saladini MA, Tota F et al (2012) Chalcid parasitoid community associated with the invading pest Dryocosmus kuriphilus in north-western Italy. Insect Conserv Divers 6:114–123CrossRefGoogle Scholar
  46. R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  47. Reale L, Tedeschini E, Rondoni G, Ricci C, Bin F, Frenguelli G, Ferranti F (2016) Histological investigation on gall development induced by a worldwide invasive pest, Dryocosmus kuriphilus, on Castanea sativa. Plant Biosyst 150:35–42CrossRefGoogle Scholar
  48. Rieske LK (2007) Success of an exotic gallmaker, Dryocosmus kuriphilus, on chestnut in the USA: a historical account. IOBC WPRS Bull 37:172–174Google Scholar
  49. Rohde B, Paris T, Heatherington E, Hall D, Mankin R (2013) Responses of Diaphorina citri (Hemiptera: Psyllidae) to conspecific vibrational signals and synthetic mimics. Ann Entomol Soc Am 106:392–399CrossRefGoogle Scholar
  50. Romani R, Rondoni G, Gragnoli L, Pergolari P, Santinelli C, Rossi Stacconi MV, Ricci C (2010) Bio-ethological and morphological investigations on Dryocosmus kuriphilus Yasumatsu. Atti Accad Naz Italiana Entomol Rend 58:97–104 (in Italian, English abstract) Google Scholar
  51. Rondoni G, Bertoldi V, Malek R, Foti MC, Peri E, Maistrello L et al (2017) Native egg parasitoids recorded from the invasive Halyomorpha halys successfully exploit volatiles emitted by the plant–herbivore complex. J Pest Sci 80:1087–1095CrossRefGoogle Scholar
  52. Rondoni G, Bertoldi V, Malek R, Djelouah K, Moretti C, Buonaurio R, Conti E (2018) Vicia faba plants respond to oviposition by invasive Halyomorpha halys activating direct defences against offspring. J Pest Sci 91:671–679CrossRefGoogle Scholar
  53. Santi F, Maini S (2011) New association between Dryocosmus kuriphilus and Torymus flavipes in chestnut trees in the Bologna area (Italy): first results. Bull Insectol 64:275–278Google Scholar
  54. Stone GN, Schönrogge K (2003) The adaptive significance of insect gall morphology. Trends Ecol Evol 18:512–522CrossRefGoogle Scholar
  55. Stone GN, Schönrogge K, Atkinson RJ, Bellido D, Pujade-Villar J (2002) The population biology of oak gall wasps (Hymenoptera: Cynipidae). Annu Rev Entomol 47:633–668CrossRefGoogle Scholar
  56. Tosi L, Beccari G, Rondoni G, Covarelli L, Ricci C (2015) Natural occurrence of Fusarium proliferatum on chestnut in Italy and its potential entomopathogenicity against the Asian chestnut gall wasp Dryocosmus kuriphilus. J Pest Sci 88:369–381CrossRefGoogle Scholar
  57. Ugolini F, Massetti L, Pedrazzoli F, Tognetti R, Vecchione A, Zulini L, Maresi G (2014) Ecophysiological responses and vulnerability to other pathologies in European chestnut coppices, heavily infested by the Asian chestnut gall wasp. For Ecol Manag 314:38–49CrossRefGoogle Scholar
  58. Warmund MR (2013) Dryocosmus kuriphilus-induced chestnut galls and their inhabitants. HortScience 48:969–974CrossRefGoogle Scholar
  59. Wheat D (2012) Arduino internals. Apress, New YorkGoogle Scholar
  60. Wickert AD (2014) The ALog: inexpensive, open-source, automated data collection in the field. Bull Ecol Soc Am 95:166–176CrossRefGoogle Scholar
  61. Yasumatsu K (1951) A new Dryocosmus injurious to chestnut trees in Japan (Hym., Cynipidae). Mushi 22:89–93Google Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Department of Agricultural, Food and Environmental SciencesUniversity of PerugiaPerugiaItaly

Personalised recommendations