Abundance and impact of egg parasitoids on the pine processionary moth (Thaumetopoea pityocampa) in Bulgaria

doi:10.3832/ifor3538-014

Abundance and impact of egg parasitoids on the pine processionary moth (Thaumetopoea pityocampa) in Bulgaria

Plamen Mirchev, Georgi Georgiev , Margarita Georgieva, Ivailo Markoff, Gergana Zaemdzhikova, Maria Matova

iForest - Biogeosciences and Forestry, Volume 14, Issue 5, Pages 456-464 (2021)
doi: https://doi.org/10.3832/ifor3538-014
Published: Oct 02, 2021 - Copyright © 2021 SISEF

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We collected 2297 egg batches of the pine processionary moth (Thaumetopoea pityocampa) during the period 1991-2018 from 44 sites in Bulgaria. The sampling sites were classified into three groups according to T. pityocampa phenological form (early, late and both forms) as well as in two groups of its range (historical and newly colonized areas). Seven primary egg parasitoids were identified: Ooencyrtus pityocampae, Baryscapus servadeii, Pediobius bruchicida, Anastatus bifasciatus, Eupelmus (Macroneura) vesicularis, Eupelmus (Macroneura) vladimiri and Trichogramma sp., and one hyperparasitoid, Baryscapus transversalis. The average impact of egg parasitoids (the percentage of parasitized host eggs) on T. pityocampa in Bulgaria was 13.8%. The two main parasitoids, O. pityocampae and B. servadeii, parasitized about 90% of the host eggs. The remaining parasitoids were of insignificant consequence to the parasitism of the T. pityocampa eggs, but in areas recently colonized by the pest, A. bifasciatus and Trichogramma sp. had a noticeable share (up to 33% of the impact). In old habitats of the host (areas colonized more than 10 years), the impact was almost two times higher than in new ones (15.3% vs. 8.6%). This could be attributed to B. servadeii, which was rare in newly colonized areas of T. pityocampa (impact 0.5%), but strongly dominant in old habitats (impact 7.2%). In contrast, O. pityocampae had a significant impact in new habitats (4.9%), which increased only slightly over time, reaching 6.0% in old habitats. There was no significant difference between the percentage of parasitism of the early and late form of the pine processionary moth (14.8% vs. 15.9%). However, there was a significant difference in the share of separate species in the parasitoid complex: in the early form, B. servadeii definitely dominated (63% of the infested eggs), while in the late form O. pityocampae dominated, although not so strongly (52% of the infested eggs). This difference is most likely due to the phenological characteristics of the parasitoids and the two forms of T. pityocampa. B. transversalis secondarily infested about 5% of the eggs of O. pityocampae and B. servadeii. This percentage was slightly lower for new habitats and habitats of the early form of pine processionary moth (3% and 4%, respectively). The impacts of the main parasitoids O. pityocampae and B. servadeii as well as the total impact of the parasitoid complex as a whole decreased with altitude. Conversely, the impacts of A. bifasciatus and Trichogramma sp. slightly increased with altitude probably due to the reduced competition of the main parasitoids.

Keywords

Thaumetopoea pityocampa, Distribution, Habitats, Expansion, Phenological Forms, Egg Parasitism, Bulgaria

Authors’ address

(1)

0000-0001-5703-2597
0000-0003-3165-1992
0000-0002-8725-557X

Forest Research Institute, Bulgarian Academy of Sciences, Sofia (Bulgaria)

Corresponding author

Georgi Georgiev
ggeorgiev.fri@gmail.com

Citation

Mirchev P, Georgiev G, Georgieva M, Markoff I, Zaemdzhikova G, Matova M (2021). Abundance and impact of egg parasitoids on the pine processionary moth (Thaumetopoea pityocampa) in Bulgaria. iForest 14: 456-464. - doi: 10.3832/ifor3538-014

Academic Editor

Massimo Faccoli

Paper history

Received: May 29, 2020
Accepted: Aug 07, 2021

First online: Oct 02, 2021
Publication Date: Oct 31, 2021
Publication Time: 1.87 months

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List of the papers citing this article based on CrossRef Cited-by.

(1)

Auger-Rozenberg MA, Torres-Leguizamon M, Courtin C, Rossi JP, Kerdelhué C (2015a)
Incongruent evolutionary histories of two parasitoids in the Mediterranean basin: influence of host specialization and ecological characteristics. Journal of Biogeography 42: 1040-1051.
CrossRef | Gscholar

(2)

Auger-Rozenberg MA, Barbaro L, Battisti A, Blache S, Charbonnier Y, Denux O, Garcia J, Goussard F, Imbert C-E, Kerdelhué C, Roques A, Torres-Leguizamon M, Vetillard F (2015b)
Ecological responses of parasitoids, predators and associated insect communities to the climate-driven expansion of pine processionary moth. In: “Processionary Moths and Climate Change: an Update” (Roques A ed). Springer, Dordrecht, Netherlands, pp. 311-358.
Gscholar

(3)

Battisti A, Stastny M, Netherer S, Robinet C, Schopf A, Roques A, Larsson S (2005)
Expansion of geographic range in the pine processionary moth caused by increased winter temperatures. Ecological Applications 15: 2084-2096.
CrossRef | Gscholar

(4)

Bellin S, Schmidt GH, Douma-Petridou E (1990)
Structure, ooparasitoid spectrum and rate of parasitism of egg-batches of Thaumetopoea pityocampa (Den. & Schiff.) (Lep., Thaumetopoeidae) in Greece. Journal of Applied Entomology 110: 113-120.
CrossRef | Gscholar

(5)

Bellin S (1995)
Zur Biologie von Baryscapus transversalis Graham (Hym.: Eulophidae), Hyperparasitoid der Primärparasitoiden von Thaumetopoea pityocampa (Den. and Schiff.) (Lep., Thaumetopoeidae) [On the biology of Baryscapus transversalis Graham (Hym.: Eulophidae), hyperparasitoid of the primary parasitoids of Thaumetopoea pityocampa (Den. and Schiff.) (Lep., Thaumetopoeidae)]. Mitteilungen der Deutschen Gesellschaft für Allgemeine und Angewandte Entomologie 9: 453-457. [in German]
Gscholar

(6)

Bouzar-Essaidi K, Branco M, Battisti A, Garcia A, Rosário Fernandes M, Chabane Y, Bouzemarene M, Benfekih L (2021)
Response of the egg parasitoids of the pine processionary moth to host density and forest cover at the southern edge of the range. Agricultural and Forest Entomology 23 (2): 212-221.
CrossRef | Gscholar

(7)

Boyadzhiev P, Dautbasic M, Mujezinovic O, Mirchev P, Georgiev G, Georgieva M (2015)
Baryscapus transversalis Graham (Hymenoptera: Eulophidae) - a new species for the fauna of Bosnia and Herzegovina. Šumarski List 1-2: 69-71.
Gscholar

(8)

Fusu L (2017)
An integrative taxonomic study of European Eupelmus (Macroneura) (Hymenoptera: Chalcidoidea: Eupelmidae), with a molecular and cytogenetic analysis of Eupelmus (Macroneura) vesicularis: several species hiding under one name for 240 years. Zoological Journal of the Linnean Society 181 (3): 519-603.
CrossRef | Gscholar

(9)

Georgiev G, Rousselet J, Laparie M, Robinet C, Georgieva M, Zaemdzhikova G, Roques A, Bernard A, Poitou L, Buradino M, Kerdelhué C, Rossi J-P, Matova M, Boyadzhiev P, Mirchev P (2021)
Comparative studies of egg parasitoids of the pine processionary moth (Thaumetopoea pityocampa, Den. and Schiff) in historic and expansion areas in France and Bulgaria. Forestry 94 (2): 324-331.
CrossRef | Gscholar

(10)

Graham MWRV (1987)
A reclassification of the European Tetrastichinae (Hymenoptera: Eulophidae), with a revision of certain genera. Bulletin of the British Museum of Natural History (Entomology) 55 (1): 1-392.
Gscholar

(11)

Graham MWRV (1991)
A reclassification of the European Tetrastichinae (Hymenoptera: Eulophidae): revision of the remaining genera. Memoirs of the American Entomological Institute 49: 1-322.
Gscholar

(12)

Hezil S, Chakali G, Battisti A (2018)
Plant phenotype affects oviposition behaviour of pine processionary moth and egg survival at the southern edge of its range. iForest 11: 572-576.
CrossRef | Gscholar

(13)

Hódar JA, Cayuela L, Heras D, Pérez-Luque AJ, Torres-Muros L (2021)
Expansion of elevational range in a forest pest: can parasitoids track their hosts? Ecosphere 12 (4): 1-14.
CrossRef | Gscholar

(14)

Jactel H, Barbaro L, Battisti A, Bosc A, Branco M, Brockerhoff E, Castagneyrol B, Dulaurent A-M, Hódar JA, Jacquet J-S, Mateus E, Paiva M-R, Roques A, Samalens J-C, Santos H, Schlyter F (2015)
Insect - Tree Interactions in Thaumetopoea pityocampa. In: “Processionary Moths and Climate Change: an Update” (Roques A ed). Springer, Dordrecht, Netherlands, pp. 265-310.
CrossRef | Gscholar

(15)

López-Sebastián E, Selfa J, Pujade-Villar J, Juan-Martínez MJ (2003)
Baryscapus transversalis Graham, 1991 (Hymenoptera, Chalci
Online | Gscholar

(16)

Masutti L (1964)
Ricerche sui parassiti oofagi della Thaumetopoea pityocampa (Schiff.) [Research on oophagous parasites of Thaumetopoea pityocampa (Schiff.)]. Annali del Centro di Economia Montana delle Venezie 4: 205-271. [in Italian]
Gscholar

(17)

Mirchev P, Schmidt GH, Tsankov G, Pllana S (2000)
Egg parasitoids of the processionary moth Thaumetopoea pityocampa (Den. and Schiff.) collected in Albania. Bollettino di Zoologia Agraria e di Bachicoltura - Serie II 31 (2): 152-165.
Gscholar

(18)

Mirchev P, Schmidt GH, Tsankov G, Avci M (2004)
Egg parasitoids of Thaumetopoea pityocampa (Den. & Schiff.) (Lep., Thaumetopoeidae) and their impact in SW Turkey. Journal of Applied Entomology 128 (8): 533-542.
CrossRef | Gscholar

(19)

Mirchev P (2005)
Egg parasitoids on pine processionary moth, Thaumetopoea pityocampa (Den. & Schiff.) (Lepidoptera, Thaumetopoeidae) in countries of Balkan Peninsula. D.Sc. Thesis, University of Forestry, Sofia, Bulgaria, pp. 64. [in Bulgarian]
Gscholar

(20)

Mirchev P, Georgiev G, Matova M (2011)
Prerequisites for expansion of pine processionary moth Thaumetopoea pityocampa (Den. and Schiff.) in Bulgaria. Journal of Balkan Ecology 14 (2): 117-130.
Online | Gscholar

(21)

Mirchev P, Georgiev G, Tsankov G (2017)
Long-term studies on egg parasitoids of pine processionary moth (Thaumetopoea pityocampa) in a new locality in Bulgaria. Journal of the Entomological Research Society 19 (3): 15-25.
Online | Gscholar

(22)

Mirchev P, Georgiev G, Georgieva M, Matova M, Zaemdzhikova G (2018)
Enlargement of pine processionary moth (Thaumetopoea pityocampa) range in Bulgaria. Forest Review 48 (1): 4-7.
Gscholar

(23)

Mirchev P, Georgieva M, Zaemdzhikova G, Matova M, Hlebarska S, Filipova E, Georgiev G (2019)
Phenological form diversity of Thaumetopoea pityocampa in Bulgaria. Poplar 203: 65-69.
Online | Gscholar

(24)

Mirchev P, Georgiev G, Zaemdzhikova G, Georgieva M, Matova M (2021)
Impact of egg parasitoids on pine processionary moth Thaumetopoea pityocampa (Denis & Schiffermüller, 1775) (Lepidoptera: Notodontidae) in a new habitat. Acta Zoologica Bulgarica 73 (1): 131-134.
Online | Gscholar

(25)

Nikolskaya MN, Trjapitzin VA (1978)
Trichogrammatidae. In: “Keys to the insects of the European Part of the USSR, Volume III, Hymenoptera, Part II” (Medvedev GS ed). Nauka, Leningrad, Russia, pp. 501-513. [in Russian]
Gscholar

(26)

Rahim N, Chakali G, Battisti A (2016)
Egg mortality in the cedar processionary moth, Thaumetopoea bonjeani (Lepidoptera: Notodontidae) in an outbreak area of Algeria. Biocontrol Science and Technology 26 (6): 849-860.
CrossRef | Gscholar

(27)

Roques A, Rousselet J, Avci M, Avtzis DN, Basso A, Battisti A, Ben Jamaa ML, Bensidi A, Berardi L, Berretima W, Branco M, Chakali G, Cota E, Dautbašić M, Delb H, El Alaoui El Fels MA, El Mercht S, El Mokhefi M, Forster B, Garcia J, Georgiev G, Glavendekić MM, Goussard F, Halbig P, Henke L, Hernandez R, Hódar JA, Ipekdal K, Jurc M, Klimetzek D, Laparie M, Larsson S, Mateus E, Matošević D, Meier F, Mendel Z, Meurisse N, Mihajlović L, Mirchev P, Nasceski S, Nussbaumer C, Paiva MR, Papazova I, Pino J, Podlesnik J, Poirot J, Protasov A, Rahim N, Peña GS, Santos H, Sauvard D, Schopf A, Simonato M, Tsankov G, Wagenhoff E, Yart A, Zamora R, Zamoum M, Robinet C (2015)
Climate warming and past and present distribution of the processionary moths (Thaumetopoea spp.) in Europe, Asia Minor and North Africa. In: “Processionary Moths and Climate Change: an Update” (Roques A ed). Springer, Dordrecht, Netherlands, pp. 81-161.
CrossRef | Gscholar

(28)

Sabev L, Stanev S (1959)
Climatic regions in Bulgaria and their climate. Vol. 5, Publishing House “Science and Art”, Sofia, Bulgaria, pp. 176. [in Bulgarian]
Gscholar

(29)

Schmidt GH, Kitt J (1994)
Identification by meconia of two egg parasitoids of Thaumetopoea wilkinsoni. Phytoparasitica 22 (1): 39-41.
CrossRef | Gscholar

(30)

Schmidt GH, Tsankov G, Mirchev P (1997)
Notes on the egg parasitoids of Thaumetopoea pityocampa (Den. and Schiff.) (Insecta: Lepidoptera: Thaumetopoeidae) collected on the Greek island Hydra. Bollettino di Zoologia Agraria e di Bachicoltura - Serie II 29 (1): 91-99.
Online | Gscholar

(31)

Schmidt GH, Tanzen E, Bellin S (1999)
Structure of egg-batches of Thaumetopoea pityocampa (Den. and Schiff.) (Lep., Thaumetopoeidae), egg parasitoids and rate of egg parasitism on the Iberian Peninsula. Journal of Applied Entomology 123: 449-458.
CrossRef | Gscholar

(32)

Simonato M, Pilati M, Magnoux E, Courtin C, Sauné L, Rousselet J, Battisti A, Auger-Rozenberg M-A, Kerdelhué C (2019)
A population genetic study of the egg parasitoid Baryscapus servadeii reveals large scale automictic parthenogenesis and almost fixed homozygosity. Biological Control 139 (1652): 104097.
CrossRef | Gscholar

(33)

Tanzen E, Schmidt GH (1995)
Identification by meconia of four species egg parasitoids Thaumetopoea pityocampa (Den. and Schiff.) (Insecta Lepidoptera Thaumetopoeidae). Bollettino di Zoologia Agraria e di Bachicoltura - Serie II 27 (1): 61-70.
Gscholar

(34)

Tiberi R (1990)
Egg parasitoids of the pine processionary caterpillar, Thaumetopoea pityocampa (Den and Schiff) (Lep, Thaumetopoeidae) in Italy. Distribution and activity in different areas. Journal of Applied Entomology 110: 14-18.
CrossRef | Gscholar

(35)

Trjapitzin VA (1978a)
Eupelmidae. In: “Keys to the insects of the European Part of the USSR, Volume III, Hymenoptera, Part II” (Medvedev GS ed). Nauka, Leningrad, Russia, pp. 228-235. [in Russian]
Gscholar

(36)

Trjapitzin VA (1978b)
Encyrtidae. In: “Keys to the insects of the European Part of the USSR, Volume III, Hymenoptera, Part II” (Medvedev GS ed). Nauka, Leningrad, Russia, pp. 236-328. [In Russian]
Gscholar

(37)

Trjapitzin VA (1978c)
Eulophidae. In: “Keys to the insects of the European Part of the USSR, Volume III, Hymenoptera, Part II” (Medvedev GS ed). Nauka, Leningrad, Russia, pp. 381-467. [In Russian]
Gscholar

(38)

Trjapitzin VA (1989)
Parasitic Hymenoptera of the fam. Encyrtidae of Palaearctics. Nauka, Leningrad, Russia, pp. 489. [In Russian]
Gscholar

(39)

Tsankov G (1990)
Egg parasitoids of the pine processionary moth, Thaumetopoea pityocampa (Den. and Schiff.) (Lep., Thaumetopoeidae) in Bulgaria: species, importance, biology and behaviour. Journal of Applied Entomology 110: 7-13.
CrossRef | Gscholar

(40)

Tsankov G, Schmidt GH, Mirchev P (1996)
Parasitism of egg-batches of the pine processionary moth Thaumetopoea pityocampa (Den. and Schiff.) (Lep., Thaumetopoeidae) in various regions of Bulgaria. Journal of Applied Entomology 120: 93-105.
CrossRef | Gscholar

(41)

Tsankov G, Douma-Petridou E, Mirchev P, Georgiev G, Koutsaftikis A (1999)
Spectrum of egg parasitoids and rate of parasitism of egg batches of the pine processionary moth Thaumetopoea pityocampa (Den. & Schiff.) in the northern Peleponnes/Greece. Journal of the Entomological Research Society 1 (2): 1-8.
Online | Gscholar

(42)

Zaemdzhikova G, Markoff I, Mirchev P, Georgiev G, Georgieva M, Nachev R, Zaiakova M, Dobreva M (2018)
Zone and rate of pine processionary moth (Thaumetopoea pityocampa) expansion in Bulgaria. Silva Balcanica 19 (3): 13-20.
Online | Gscholar

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