Hostname: page-component-7b9c58cd5d-f9bf7 Total loading time: 0 Render date: 2025-03-15T21:20:57.622Z Has data issue: false hasContentIssue false

Chalcidoid parasitoids of overwintered pupae of Hyphantria cunea (Lepidoptera: Arctiidae) in hazelnut plantations of Turkey's central Black Sea region

Published online by Cambridge University Press:  03 January 2012

G.T. Sullivan*
Affiliation:
Suleyman Demirel University, Faculty of Agriculture, Department of Plant Protection, 32260 Isparta, Turkey; Ondokuz Mayis University, OYDEM, 55139 Samsun, Turkey
I. Karaca
Affiliation:
Suleyman Demirel University, Faculty of Agriculture, Department of Plant Protection, 32260 Isparta, Turkey
S.K. Ozman-Sullivan
Affiliation:
Ondokuz Mayis University, Faculty of Agriculture, Department of Plant Protection, 55139 Samsun, Turkey
Z.Q. Yang
Affiliation:
Research Institute of Forest Ecology, Environment and Protection, Chinese Academy of Forestry, Haidian District, Beijing 100091, China
*
1Corresponding author (e-mail: gsullivan@omu.edu.tr).
Rights & Permissions [Opens in a new window]

Abstract

Overwintered pupae of fall webworm, Hyphantria cunea (Drury), were collected from 38 hazelnut (Corylus avellana L. (Betulaceae)) plantations in Samsun province, Turkey, in 2008 and 2009. Four chalcidoid (Hymenoptera: Chalcidoidea) species were reared: Chouioia cunea Yang (Eulophidae), Conomorium amplum (Walker), Dibrachys boarmiae (Walker), and Psychophagus omnivorus (Walker) (Pteromalidae). Overall parasitism was 11.97% and 4.84% for 2008 and 2009, respectively; species richness on sites ranged from one to three species. Psychophagus omnivorus parasitised 6.7% of all pupae and comprised 79% of chalcidoid rearings. Chouioia cunea had the highest clutch average (117) and female:male ratio (44.5:1). Records of Chouioia cunea and Conomorium amplum are new for Turkey and, except for P. omnivorus, all parasitoids are new records for H. cunea in Turkey.

Résumé

Nous avons prélevé des nymphes de la chenille à tente estivale, Hyphantria cunea (Drury), qui ont passé l'hiver, dans 38 plantations d'aveliniers (Corylus avellana L. (Betulaceae)) dans la province de Samsun, Turquie, en 2008 et 2009. Nous avons obtenu par élevage quatre espèces de chalcidoïdes (Hymenoptera : Chacidoidea) Chouioia cunea Yang (Eulophidae), ainsi que Conomorium amplum (Walker), Dibrachys boarmiae (Walker) et Psychophagus omnivorus (Walker) (Pteromalidae). Le parasitisme global était de 11,97 % en 2008 et de 4,84 % en 2009; la richesse spécifique variait d'une à trois espèces sur les sites. Psychophagus omnivorus parasitait 6,7 % de toutes les nymphes et représentait 79 % des chacidoïdes obtenus par élevage. Chouioia cunea possédait la ponte moyenne la plus importante (117) et le rapport femelles : mâles le plus élevé (44,5:1). C'est la première fois que Chouioia cunea et Conomorium amplum sont signalés en Turquie; c'est aussi la première fois que toutes les espèces, à l'exception de P. omnivorus, sont récoltées sur H. cunea en Turquie.

[Traduit par la Rédaction]

Type
Biodiversity & Evolution
Copyright
Copyright © Entomological Society of Canada 2011

Fall webworm, Hyphantria cunea (Drury) (Lepidoptera: Arctiidae), is a polyphagous defoliating pest native to Canada, Mexico, and the United States of America, and has been reported from Europe (at least 15 countries), Eurasia (Russia and Turkey), and Asia (Azerbaijan, Georgia, Iran, China, Korea, and Japan). At least eight families, 20 genera, and 40 species of chalcidoids (Hymenoptera: Chalcidoidea) parasitise H. cunea (Warren and Tadic Reference Warren and Tadic1967; Szalay–Marzso Reference Szalay-Marzso1972; Sharov and Izhevskiy Reference Sharov and Izhevskiy1987; Tuncer Reference Tuncer1992; Boriani Reference Boriani1994; Nurieva Reference Nurieva2002; Rezaei et al. Reference Rezaei, Moharramipour and Talebi2003; Japoshvili et al. Reference Japoshvili, Nikolaishvili, Dzneladze and Goguadze2006; Yang et al. Reference Yang, Wang, Wei, Qu and Qiao2008) (Table 1). Noyes (Reference Noyes2001) reported 55 species of chalcidoids from H. cunea (including considerable overlap with species records in Table 1). Several studies have reported specifically on parasitoids of overwintered pupae (Deseo et al. Reference Deseo, Montermini and Cortellini1986; Tuncer and Ecevit Reference Tuncer and Ecevit1996; Rezaei et al. Reference Rezaei, Moharramipour and Talebi2003).

Table 1. Chalcidoids recorded from Hyphantria cunea in North America, Europe, and Asia.

* Hyperparasitoids.

Hyphantria cunea is an important pest of hazelnut plantations in Turkey, the world's leading producer and exporter of hazelnuts (Bozoglu Reference Bozoglu2009), Corylus avellana L. (Betulaceae). A severe outbreak occurred in the central Black Sea region in 1984–1985, especially in hazelnut plantations in Samsun province, Turkey. A subsequent outbreak from 2007 to 2010 prompted our study. Hyphantria cunea has the potential to invade several hundred thousand hectares of unaffected hazelnut plantations between the eastern limit of its present distribution in Turkey and affected areas in western Georgia. The objective of this study was to record chalcidoid parasitoids from overwintered pupae of H. cunea from the Samsun region to provide important baseline data for future studies and potential biological control of this pest in the region.

During late March and early April of 2008 and 2009, pupae were collected from 13 (2008) and 27 (2009) sites in the Carsamba (41°11′56″N, 36°43′30″E), Terme (41°12′32″N, 36°58′20″E), and Salipazari (41°04′51″N, 36°49′35″E) areas of Samsun province. To standardise collection efforts across sites, four person hours of search effort were dedicated to each site. Apparently healthy pupae were separated from those that had obvious signs of disease, damage, or exit holes. No healthy pupae were found at 11 of the 13 sites used in 2008; those sites were abandoned in 2009. The remaining 2 sites and 25 new sites were used in 2009. Pupae were collected from living and dead trees as well as from wood piles and fence posts that were mostly located on the plantation boundaries. In the laboratory, each pupa was placed in a separate plastic vial (5.0 cm × 2.5 cm) with a wad of moistened tissue paper to maintain humidity. Vials were sealed with finely woven mesh and stored in a dark, slightly ventilated laboratory cupboard at ambient temperatures that ranged from 13 to 21°C. Laboratory conditions were designed to approximate the natural environment of pupae during the April–June parasitoid emergence period. Emerged parasitoids were briefly refrigerated before counting and subsequent storage in 80% ethanol prior to identification. Levels of parasitism, clutch size, and sex ratio were recorded.

We collected 4297 overwintered H. cunea pupae in 2008 and 2009. Number of pupae per site ranged from 2 to 561. Four chalcidoid species (identified by ZQY) were reared from the pupae: Chouioia cunea Yang (Eulophidae), Conomorium amplum (Walker), Dibrachys boarmiae (Walker), and Psychophagus omnivorus (Walker) (Pteromalidae) (Table 2). Except for P. omnivorus, they are new records for H. cunea in Turkey, and Conomorium amplum and Chouioia cunea are new records for Turkey.

Table 2. Average parasitism (%), average clutch size, and average sex ratio of chalcidoids reared from overwintered pupae of Hyphantria cunea from the Samsun region of Turkey in 2008 and 2009.

* Three specimens from two pupae.

In 2008 and 2009, chalcidoids were reared from 11 of 13 sites (84.6%) and 22 of 27 sites (81.5%), respectively. Species richness at sites ranged from one to three species in both years. Chalcidoid parasitism and total parasitism were 11.97% and 13.77%, respectively, in 2008 and 4.84% and 11.29%, respectively, in 2009.

Psychophagus omnivorus and Conomorium amplum were responsible for 78.9% and 2.8% of total chalcidoid parasitism, respectively. Average clutch sizes ranged from 117 (Chouioia cunea) to 1.5 (Conomorium amplum) and average female:male ratios ranged from 44.5:1 (Chouioia cunea) to 1:2 (Conomorium amplum). The female:male ratio was almost equal (0.92:1) in P. omnivorous, the most common species (Table 2).

Chouioia cunea, a parasitoid of H. cunea in China (Yang Reference Yang1989), has been reported from Italy and Japan (Boriani Reference Boriani1994), Iran (Rezaei et al. Reference Rezaei, Moharramipour and Talebi2003), and Georgia (Japoshvili et al. Reference Japoshvili, Nikolaishvili, Dzneladze and Goguadze2006). For this species, Yang et al. (Reference Yang, Wang, Wei, Qu and Qiao2008) reported parasitism of H. cunea ranging from 5.1% to 12.8%, a female:male ratio of 45–96:1, and an average clutch size of 124. The respective numbers recorded in our study for this parasitoid were 1.9%, 44.5:1, and 117. Chouioia cunea has been mass reared and successfully used in China for the control of H. cunea (Yang et al. Reference Yang, Wei and Wang2006).

Conomorium amplum was reared from only two pupae (0.047%) in our study and was apparently very rare. This parasitoid has been reported from H. cunea in Italy (Boriani Reference Boriani1994) and China (Xiao and Huang Reference Xiao and Huang2000). Dibrachys boarmiae was reported as a hyperparasitoid in Italy (Boriani Reference Boriani1994) and, in our study, was found at low levels (1.2%), probably also as a hyperparasitoid.

Of the parasitoid species we recorded, only P. omnivorus has been reported previously from the study area (Tuncer Reference Tuncer1992; Tuncer and Ecevit Reference Tuncer and Ecevit1996). Tuncer (Reference Tuncer1992) recorded 6.3% and 8% parasitism of overwintered pupae of H. cunea in 1990 and 1991, respectively. Those levels are similar to the 6.7% parasitism that we recorded for that species. Tuncer and Ecevit (Reference Tuncer and Ecevit1996) reported clutch sizes for P. omnivorus ranging from 16 to 47, compared with the average clutch size of 60 recorded in our study. Psychophagus omnivorus has also been reported from Russia (Sharov and Izhevskiy Reference Sharov and Izhevskiy1987), Azerbaijan (Nurieva Reference Nurieva2002), and Iran (Rezaei et al. Reference Rezaei, Moharramipour and Talebi2003), and was considered the most important chalcidoid associated with H. cunea in middle and east European countries (Szalay–Marzso Reference Szalay-Marzso1972).

In the current study, the reasonable percentage of parasitism and high average clutch size recorded for P. omnivorus suggest that it may be a suitable candidate for a regional biological control program for H. cunea. The demonstrated success of Chouioia cunea in China strongly suggests that it also deserves further investigation. Overall, this study contributes to the international body of knowledge of the chalcidoid parasitoids of H. cunea and strengthens the case for biological control of this widely distributed pest.

The authors thank Suleyman Demirel University (Isparta, Turkey) for funding and the Department of Plant Protection, Faculty of Agriculture, at Ondokuz Mayis University (Samsun, Turkey) for research facilities.

References

Boriani, M. 1994. New records of parasitoids from Hyphantria cunea (Drury 1773) (Lepidoptera, Arctiidae) in Italy. Entomofauna, 15: 425432.Google Scholar
Bozoglu, M. 2009. Effects of Turkey's accession to the European Union on hazelnut markets. Acta Horticulturae, 845: 763768.CrossRefGoogle Scholar
Deseo, K.V.Montermini, A.Cortellini, W. 1986. The first outbreak of the fall webworm (Hyphantria cunea Drury; Lepid., Arctiidae) in North Italy: preliminary observations on the development, diapause and derivation. Journal of Applied Entomology, 101: 201206. doi:10.1111/j.1439-0418.1986.tb00850.xCrossRefGoogle Scholar
Japoshvili, G.Nikolaishvili, A.Dzneladze, N.Goguadze, L. 2006. The fall webworm (Hyphantria cunea) in western Georgia. Proceedings of the Georgian Academy of Science, Biological Series B., 4: 122126.Google Scholar
Noyes, J.S. 2001. Interactive catalogue of world Chalcidoidea 2001 [online]. Available from: http://www.taxapad.com/taxapadmain.php [accessed 14 October 2010].Google Scholar
Nurieva, I. 2002. Bioecological abilities of parasitoids parasitising Hyphantria cunea Drury (Lepidoptera: Arctiidae) in Azerbaijan. Turkiye 5. Biyolojik Mucadele Kongresi, 4–7 Eylul 2002, Erzurum, Turkiye.Google Scholar
Rezaei, V.Moharramipour, S.Talebi, A.A. 2003. The first report of Psychophagus omnivorus (Walker) and Chouioia cunea (Yang) parasitoid wasps of American white webworm Hyphantria cunea Drury (Lep.: Arctiidae) from Iran. Applied Entomology and Phytopathology, 70: 137138.Google Scholar
Sharov, A.A.Izhevskiy, S.S. 1987. The parasitoid complex of the American white butterfly Hyphantria cunea (Drury) (Lepidoptera, Arctiidae) in the south of the European part of the USSR. Entomologicheskoye Obozreniye, 66: 290298 [Entomological Review, 67: 48–56]Google Scholar
Szalay-Marzso, L. 1972. Biology and control of the fall webworm (Hyphantria cunea Drury) in the middle and east European countries. European and Mediterranean Plant Protection Organisation / Organisation Européenne et Méditerranéenne pour la Protection des Plantes Bulletin, 3: 2335.Google Scholar
Tuncer, C. 1992. Amerikan beyaz kelebegi (Hyphantria cunea Drury, Lepidoptera: Arctiidae) 'nin Samsun ve cevresindeki biyolojisi ve ozellikle konukcu bitkilerin degisik acilardan etkileri uzerinde arastirmalar. Doktora Tezi, Ankara Universitesi, Fen Bilimleri Enstitusu, Ankara.Google Scholar
Tuncer, C.Ecevit, O. 1996. Amerikan beyaz kelebeginin Samsun ili findik uretim alanlarindaki kisa biyolojisi ve dogal dusmanlari. In Findik ve Diger Sert Kabuklu Meyveler Sempozyumu, Ondokuz Mayis Universitesi, Ziraat Fakultesi, Samsun, Turkey. pp. 134145.Google Scholar
Warren, L.O.Tadic, M. 1967. The fall webworm, Hyphantria cunea, its distribution and natural enemies: A world list (Lepidoptera: Arctiidae). Journal of the Kansas Entomological Society, 40: 194202.Google Scholar
Xiao, H.Huang, D.W. 2000. Taxonomic study on genus Conomorium Masi (Hymenoptera: Pteromalidae) from China. Acta Zootaxonomica Sinica, 25: 191194.Google Scholar
Yang, Z.Q. 1989. A new genus and species of Eulophidae (Hymenoptera: Chalcidoidea) parasitizing Hyphantria cunea (Drury) (Lepidoptera: Arctiidae) in China. Entomotaxonomia, 11: 117130.Google Scholar
Yang, Z.Q.Wei, J.R.Wang, X.Y. 2006. Mass rearing and augmentative releases of the native parasitoid Chouioia cunea (Hymenoptera: Eulophidae) for biological control of the introduced fall webworm Hyphantria cunea in China. Biocontrol, 51: 401418. doi:10.1007/s10526-006-9010-zCrossRefGoogle Scholar
Yang, Z.Q.Wang, X.Y.Wei, J.R.Qu, H.R.Qiao, X.R. 2008. Survey of the native insect natural enemies of Hyphantria cunea (Drury) (Lepidoptera: Arctiidae) in China. Bulletin of Entomological Research, 98: 293302. doi:10.1017/S0007485308005609.CrossRefGoogle ScholarPubMed
Figure 0

Table 1. Chalcidoids recorded from Hyphantria cunea in North America, Europe, and Asia.

Figure 1

Table 2. Average parasitism (%), average clutch size, and average sex ratio of chalcidoids reared from overwintered pupae of Hyphantria cunea from the Samsun region of Turkey in 2008 and 2009.