Eur. J. Entomol. 118: 279-287, 2021 | DOI: 10.14411/eje.2021.028

Effect of the instar of the pear psyllid Cacopsylla pyri (Hemiptera: Psyllidae) on the behaviour and fitness of the parasitoid Trechnites insidiosus (Hymenoptera: Encyrtidae)Original article

Guillaume Jean LE GOFF ORCID..., Jeremy BERTHE ORCID..., Kévin TOUGERON ORCID..., Benoit DOCHY ORCID..., Olivier LEBBE ORCID..., François RENOZ ORCID..., Thierry HANCE ORCID...
Earth and Life Institute, Ecology and Biodiversity, UC Louvain, Croix du sud 4-5 bte L7.07.04, 1348 Louvain-la-Neuve, Belgium; e-mails: guillaume.legoff@uclouvain.be, berthe.jeremy@outlook.be, kevin.tougeron@uclouvain.be, benoit.dochy@uclouvain.be, olivier.lebbe@uclouvain.be, francois.renoz@uclouvain.be, thierry.hance@uclouvain.be

Improved methods of integrated pest management of the pear psyllid Cacopsylla pyri (L.), the primary pest of pear in Europe and North America, are needed. Trechnites insidiosus (Crawford) is the most abundant parasitoid of C. pyri in pear orchards, where it is present early in the psyllid infestation period. However, little is known about its general biology, interaction with its host and potential as a control agent. The objective of this laboratory study was to evaluate the behaviour of a specialist parasitoid when presented with different larval instars of C. pyri, and assess the quality of the next generation of parasitoids. T. insidiosus was able to insert its ovipositor into all host instars. However, the fourth instar of the host appeared to be the most suitable in terms of behavioural acceptance, time spent walking, antennal activity and progeny development (mummy formation, development time and tibial length). In addition, we report a low frequency of host-feeding behaviour by this parasitoid. From a biological control perspective, we suggest that favouring T. insidiosus, either through mass releases or conservation of naturally present populations, when the first generation of psyllids reach the fourth instar, would maximize the chance of controlling psyllid populations in pear orchards.

Keywords: Psyllidae, Cacopsylla pyri, Encyrtidae, Trechnites insidiosus, parasitoid, behaviour, host instar, locomotor activity, host acceptance, host suitability, offspring quality, pear orchards, biological control

Received: May 19, 2021; Revised: August 20, 2021; Accepted: August 20, 2021; Published online: September 23, 2021  Show citation

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LE GOFF, G.J., BERTHE, J., TOUGERON, K., DOCHY, B., LEBBE, O., RENOZ, F., & HANCE, T. (2021). Effect of the instar of the pear psyllid Cacopsylla pyri (Hemiptera: Psyllidae) on the behaviour and fitness of the parasitoid Trechnites insidiosus (Hymenoptera: Encyrtidae). EJE, 118, Article 279-287. https://doi.org/10.14411/eje.2021.028
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    References

    1. Albittar L., Ismail M., Bragard C. & Hance T. 2016: Host plants and aphid hosts influence the selection behaviour of three aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae). - Eur. J. Entomol. 113: 516-522. Go to original source...
    2. Armand E., Lyoussoufi A., d'Arcier F.F. & Rieux R. 1990: Inter-relations entre les populations du psylle du poirier Psylla pyri (L.) (Hom., Psyllidae) et le complexe de ses parasitoïdes dans un verger traité du sud-est de la France. - J. Appl. Entomol. 110: 242-252. Go to original source...
    3. Armand E., Lyoussouf A. & Rieux R. 1991: Evolution du complexe parasitaire des psylles du poirier Psylla pyri et Psylla pyrisuga (Homoptera: Psyllidae). - Entomophaga 36: 287-294. Go to original source...
    4. Augustin J., Boivin G., Brodeur J. & Bourgeois G. 2020: Effect of temperature on the walking behaviour of an egg parasitoid: disentangling kinetic response from integrated response. - Ecol. Entomol. 45: 741-750. Go to original source...
    5. Aung K.S.D., Takasu K., Ueno T. & Takagi M. 2012: Effect of host-feeding on reproduction in Ooencyrtus nezarae (Ishii) (Hymenoptera: Encyrtidae), an egg parasitoid of the bean bug Riptortus clavatus. - J. Fac. Agric. Kyushu Univ. 57: 115-120. Go to original source...
    6. Avilla J., Artigues M., Marti S. & Sarasua M.J. 1992: Parasitoides de Cacopsylla pyri (L.) (= Psylla pyri (L.)) presentes en una plantación comercial de peral en Lleida no sometida a tratamientos insecticidas. - Bol. San. Veg. Plagas 18: 133-138.
    7. Bartlett B.R., Clausen C.P., DeBach P., Goeden R.D., Legner E.F., McMurtry J.A., Oatman E.R., Bay E.C. & Rosen D. 1978: Introduced Parasites and Predators of Arthropod Pests and Weeds: A World Review. Agriculture Handbook No. 480, UDSA, Washington D.C., 551 pp.
    8. Bernal J.S., Waggoner M. & Gonzalez D. 1997: Reproduction of Aphelinus albidopus (Hymenoptera: Aphelinidae) on russian wheat aphid (Hemiptera: Aphididae) hosts. - Eur. J. Entomol. 94: 83-96.
    9. Berthe J. 2018: Evaluation de la capacité de parasitisme de Trechnites insidiosus pour le contrôle biologique du psylle du poirier Cacopsylla pyri. MSc Thesis, Université catholique de Louvain, Louvain la Neuve, 89 pp.
    10. Booth S.R. 1992: The Potential of Endemic Natural Enemies to Suppress Pear Psylla, Cacopsylla pyricola Förster, in the Hood River Valley, Oregon. PhD Thesis, Oregon State University, Corvallis, OR, 155 pp.
    11. Buès R., Boudinhon L. & Toubon J.-F. 2003: Resistance of pear psylla (Cacopsylla pyri L.; Hom., Psyllidae) to deltamethrin and synergism with piperonyl butoxide. - J. Appl. Entomol. 127: 305-312. Go to original source...
    12. Bufaur M., Harizanova V. & Stoeva A. 2010: Parasitoids of the pear sucker Cacopsylla pyri L. (Psyllidae) in Bulgaria - Morphology and biology. In: Traditions and Challenges of Agricultural Education, Science and Business. Scientific Works of the Agricultural University of Plovdiv, Vol. 55, Book 2, pp. 71-76.
    13. Burts E.C. 1983: Effectiveness of a soft-pesticide program on pear pests. - J. Econ. Entomol. 76: 936-941. Go to original source...
    14. Chang J. 1977: Studies on the Susceptibility of Pear Trees to Pear Psylla, Psylla pyricola Foerster (Homoptera: Psyllidae). MSc Thesis, University of Ottawa, Ottawa, 140 pp.
    15. Charnov E.L. 1976: Optimal foraging, the marginal value theorem. - Theor. Popul. Biol. 9: 129-136. Go to original source...
    16. Charnov E.L. & Skinner S.W. 1985: Complementary approaches to the understanding of parasitoid oviposition decisions. - Environ. Entomol. 14: 383-391. Go to original source...
    17. Civolani S. 2012: The past and present of pear protection against the pear psylla, Cacopsylla pyri L. In Perveen F. (ed.): Insecticides - Pest Engineering. InTech, London, Rijeka, pp. 385-408. Go to original source...
    18. Civolani S., Peretto R., Caroli L., Pasqualini E., Chicca M. & Leis M. 2007: Preliminary resistance screening on abamectin in pear psylla (Hemiptera: Psyllidae) in Northern Italy. - J Econ. Entomol. 100: 1637-1641. Go to original source...
    19. Colinet H., Salin C., Boivin G. & Hance T. 2005: Host age and fitness-related traits in a koinobiont aphid parasitoid. - Ecol. Entomol. 30: 473-479. Go to original source...
    20. Emami M.S., Shishehbor P. & Karimzadeh J. 2014: The influences of plant resistance on predation rate of Anthocoris nemoralis (Fabricius) on Cacopsylla pyricola (Förster). - Arch. Phytopathol. Plant Prot. 47: 2043-2050. Go to original source...
    21. Erler F. 2004: Natural enemies of the pear psylla Cacopsylla pyri in treatedvs untreated pear orchards in Antalya, Turkey. - Phytoparasitica 32: 295-304. Go to original source...
    22. FAOSTAT 2021: Global Fruit Production in 2019, by Selected Variety. URL: https://www.statista.com/statistics/264001/worldwide-production-of-fruit-by-variety
    23. Gajski D. & Pekár S. 2021: Assessment of the biocontrol potential of natural enemies against psyllid populations in a pear tree orchard during spring. - Pest Manag. Sci. 77: 2358-2366. Go to original source...
    24. Ge Y., Liu P., Zhang L., Snyder W.E., Smith O.M. & Shi W. 2020: A sticky situation: honeydew of the pear psylla disrupts feeding by its predator Orius sauteri. - Pest Manag. Sci. 76: 75-84. Go to original source...
    25. Godfray H.C.J. 1994: Parasitoids: Behavioral and Evolutionary Ecology. Princeton University Press, 483 pp. Go to original source...
    26. Guerrieri E. & Noyes J.S. 2009: A review of the European species of the genus Trechnites Thomson (Hymenoptera: Chalcidoidea: Encyrtidae), parasitoids of plant lice (Hemiptera: Psylloidea) with description of a new species. - Syst. Entomol. 34: 252-259. Go to original source...
    27. Guttierrez A.P. 1966: The Bionomics of Two Encyrtid Parasites of Psylla pyricola Forster in Northern California. MSc Thesis, University of California, Berkeley, 76 pp.
    28. Hamilton W.D. 1967: Extraordinary sex ratios. A sex-ratio theory for sex linkage and inbreeding has new implications in cytogenetics and entomology. - Science 156: 477-488. Go to original source...
    29. Heimpel G.E. & Collier T.R. 1996: The evolution of host-feeding behaviour in insect parasitoids. - Biol. Rev. 71: 373-400. Go to original source...
    30. Herard F. 1985: Analysis of parasite and predator populations observed in pear orchards infested by Psylla pyri (L.) (Hom.: Psyllidae) in France. - Agronomie 5: 773-778. Go to original source...
    31. Horton D.R. 1999: Monitoring of pear psylla for pest management decisions and research. - Integr. Pest Manag. Rev. 4: 1-20. Go to original source...
    32. Jaworska K., Olszak R.W. & Zajac R.Z. 1996: Parasitization rate on the larvae of pear (Cacopsylla pyri) in orchards with differing intensity of chemical control. - Acta Horticult. 422: 334-335. Go to original source...
    33. Jerinic-Prodanovic D., Protic L. & Mihajlovic L. 2010: Predators and parasitoids of Cacopsylla pyri (L.) (Hemiptera: Psyllidae) in Serbia. - Pesticidi Fitomed. 25: 29-42. Go to original source...
    34. Jervis M.A. & Kidd N.A.C. 1986: Host-feeding strategies in Hymenopteran parasitoids. - Biol. Rev. 61: 395-434. Go to original source...
    35. Jia Y.-J. & Liu T.-X. 2018: Dynamic host-feeding and oviposition behavior of an aphid parasitoid Aphelinus asychis. - BioControl 63: 533-542. Go to original source...
    36. Lacey L., Arthurs S., Horton D. & Miliczky G. 2005: Spinosad and Granulovirus Effects on Codling Moth. Final Projekt Report. USDA-ARS, Yakima Agricultural Research Laboratory, Wapato, WA, 9 pp.
    37. Lamichhane J.R., Messéan A. & Ricci P. 2019: Research and innovation priorities as defined by the Ecophyto plan to address current crop protection transformation challenges in France. - Adv. Agron. 154: 81-152. Go to original source...
    38. Le Goff G.J., Lebbe O., Lohaus G., Richels A., Jacquet N., Byttebier V. & Hance T. 2019: What are the nutritional needs of the pear psylla Cacopsylla pyri? - Arthr.-Plant Interact. 13: 431-439. Go to original source...
    39. Mackauer M., Michaud J.P. & Völkl W. 1996: Host choice by Aphidiid parasitoids (Hymenoptera: Aphidiidae): Host recognition, host quality, and host value. - Can. Entomol. 128: 959-980. Go to original source...
    40. Mansfield S. & Mills N.J. 2002: Host egg characteristics, physiological host range, and parasitism following inundative releases of Trichogramma platneri (Hymenoptera: Trichogrammatidae) in walnut orchards. - Environ. Entomol. 31: 723-731. Go to original source...
    41. McMullen R.D. 1966: New Records of chalcidoid parasites and hyperparasites of Psylla pyricola Förster in British Columbia. - Can. Entomol. 98: 236-239. Go to original source...
    42. Mehrnejad M.R. & Copland M.J.W. 2006: Behavioral responses of the parasitoid Psyllaephagus pistaciae (Hymenoptera: Encyrtidae) to host plant volatiles and honeydew. - Entomol. Sci. 9: 31-37. Go to original source...
    43. Miliczky E.R. & Horton D.R. 2005: Densities of beneficial arthropods within pear and apple orchards affected by distance from adjacent native habitat and association of natural enemies with extra-orchard host plants. - Biol. Contr. 33: 249-259. Go to original source...
    44. Muratori F.B., Damiens D., Hance T. & Boivin G. 2008: Bad housekeeping: why do aphids leave their exuviae inside the colony? - BMC Evol. Biol. 8: 338, 7 pp. Go to original source...
    45. Oudeh B., Kassis W. & Abu-Tara R. 2013: Seasonal activity of the predator, Anthocoris nemoralis (F.) and the parasitoid, Trechnites psyllae (R.) against the pear psylla Cacopsylla pyricola (F.) (Hemiptera: Psyllidae). - Egypt. J. Biol. Contr. 23: 17-23.
    46. Pan M.-Z., Wang L., Zhang C.-Y., Zhang L.-X. & Liu T.-X. 2017: The influence of feeding and host deprivation on egg load and reproduction of an aphid parasitoid, Aphidius gifuensis (Hymenoptera: Braconidae). - Appl. Entomol. Zool. 52: 255-263. Go to original source...
    47. Retan A. & Peterson V. 1982: Pear psylla. - Insect Answers 1982: EB0906, 2 pp.
    48. Sanchez J.A., López-Gallego E. & La-Spina M. 2020: The impact of ant mutualistic and antagonistic interactions on the population dynamics of sap-sucking hemipterans in pear orchards. - Pest Manag. Sci. 76: 1422-1434. Go to original source...
    49. Sanchez J.A. & Ortin-Angulo M.C. 2012: Abundance and population dynamics of Cacopsylla pyri (Hemiptera: Psyllidae) and its potential natural enemies in pear orchards in southern Spain. - Crop Prot. 32: 24-29. Go to original source...
    50. Seemüller E. & Schneider B. 2004: 'Candidatus Phytoplasma mali', 'Candidatus Phytoplasma pyri' and 'Candidatus Phytoplasma prunorum', the causal agents of apple proliferation, pear decline and European stone fruit yellows, respectively. - Inte. J. Syst. Evol. Microbiol. 54: 1217-1226. Go to original source...
    51. Sigsgaard L., Esbjerg P. & Philipsen H. 2006a: Controlling pear psyllids by mass releasing Anthocoris nemoralis and A. nemorum (Heteroptera: Anthocoridae). - J. Fruit Ornam. Plant Res. 14 (Suppl. 3): 89-98.
    52. Sigsgaard L., Esbjerg P. & Philipsen H. 2006b: Experimental releases of Anthocoris nemoralis F. and Anthocoris nemorum (L.) (Heteroptera: Anthocoridae) against the pear psyllid Cacopsylla pyri L. (Homoptera: Psyllidae) in pear. - Biol. Contr. 39: 87-95. Go to original source...
    53. Tianna DuPont S. & Strohm C.J. 2020: Integrated pest management programmes increase natural enemies of pear psylla in Central Washington pear orchards. - J. Appl. Entomol. 144: 109-122. Go to original source...
    54. Tianna DuPont S., Strohm C., Nottingham L. & Rendon D. 2021: Evaluation of an integrated pest management program for central Washington pear orchards. - Biol. Contr. 152: 104390, 13 pp. Go to original source...
    55. Tougeron K., Iltis C., Renoz F., Albittar L., Hance T., Demeter S. & Le Goff G.J. 2021: Ecology and biology of the parasitoid Trechnites insidiosus and its potential for biological control of pear psyllids. - Pest Manag Sci ps.6517 (in press). Go to original source...
    56. Unruh T.R., Westigard P.H. & Hagen K.S. 1994: Pear psylla. In Nechols J.R. (ed.): Biological Control in the Western United States. DNR Publ. 3361, University of California, Oakland, pp. 95-100.
    57. Van Alphen J.J.M. & Visser M.E. 1990: Superparasitism as an adaptive strategy for insect parasitoids. - Annu. Rev. Entomol. 35: 59-79. Go to original source...
    58. Van Den Assem J., Gijswijt M.J. & Nübel B.K. 1982: Characteristics of courtship and mating behaviour used as classificatory criteria in Eulophidae: Tetrastichinae (Hymenoptera), with special reference to the genus Tetrastichus. - Tijdscr. Entomol. 125: 205-219.
    59. Villagra C.A., Ramirez C.C. & Niemeyer H.M. 2002: Antipredator responses of aphids to parasitoids change as a function of aphid physiological state. - Anim. Behav. 64: 677-683. Go to original source...
    60. Walker A.M. & Hoy M.A. 2003: Responses of Lipolexis oregmae (Hymenoptera: Aphidiidae) to different instars of Toxoptera citricida (Homoptera: Aphididae). - J. Econ. Entomol. 96: 1685-1692. Go to original source...
    61. Zhukovskaya M., Yanagawa A. & Forschler B.T. 2013: Grooming behavior as a mechanism of insect disease defense. - Insects 4: 609-630. Go to original source...

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