Leptoglossus occidentalis Heidemann, 1910 (Hemiptera: Coreidae) in Türkiye: Its distribution, life cycle, and fungal associations

Abstract

In this study, the distribution, life cycle and associations with fungi of the alien invasive species Leptoglossus occidentalis Heidemann, 1910 (Hemiptera: Coreidae) in Türkiye were investigated. During the study, conducted between 2019 and 2021, the pest was found to have spread across 35 provinces in Türkiye. The biological data obtained in the study were divided into ecologically similar sub-regions (Ankara-Çankırı-Kırşehir, Artvin, Isparta-Burdur, Izmir-Aydın-Manisa-Muğla-Antalya) in order to reveal the life cycle of the species. Additionally, host plant and insect samples were examined for the presence of Diplodia sapinea (Fr.) Fuckel (pine shoot blight agent) and entomopathogenic fungi species through morphological and molecular identification methods. Consequently, it was found that Leptoglossus occidentalis has two generations in Türkiye. The timing of the first flight was in early May-mid June and the second generation was from mid-July to late August. Although Diplodia sapinea was detected in some of the sampled host plant tissues, it could not be isolated from Leptoglossus occidentalis individuals. Accordingly, it did not find any evidence that Leptoglossus occidentalis vectors Diplodia sapinea although the insect and the fungus cooccurs in sampling areas. Although it was detected 25 fungal species isolated from Leptoglossus occidentalis adults, none of them were entomopathogenic fungal species. It has been revealed that the pest has spread almost all over Türkiye and has become an important risk factor affecting seed yield and quality in coniferous species.

Keywords

• Western conifer seed bug
• alien invasive species
• biology
• Diplodia sapinea

Türkiye’de Leptoglossus occidentalis Heidemann, 1910 (Hemiptera: Coreidae): Yayılışı, biyolojisi ve funguslarla ilişkisi

Abstract

Bu çalışmada yabancı istilacı bir tür olan Leptoglossus occidentalis Heidemann, 1910 (Hemiptera: Coreidae)’in Türkiye’deki yayılışı, biyolojisi ve funguslarla ilişkisi araştırılmıştır. 2019-2021 yılları arasında yürütülen bu çalışma boyunca 35 ilde zararlının yayılışı tespit edilmiştir. Çalışmada elde edilen biyolojik veriler, yoğun olarak örnekleme yapılan yerlerde ve ekolojik olarak benzer alt bölgelere (Ankara-Çankırı-Kırşehir, Artvin, Isparta-Burdur, İzmir-Aydın-Manisa-Muğla-Antalya) ayrılarak türün biyolojisi ortaya konulmuştur. Ayrıca, konukçu bitki ve böcek örnekleri Diplodia sapinea (Fr.) Fuckel (çam sürgün yanıklığı etmeni) ve entomopatojenik fungus türlerinin varlığı açısından morfolojik ve moleküler tanımlama yöntemleriyle incelenmiştir. Sonuç olarak Türkiye’de türün iki generasyona sahip olduğu belirlenmiştir. Birinci uçma zamanı mayıs başı-haziran ortası, ikinci generasyonun ise temmuz ortasından ağustos sonuna kadar olduğu tespit edilmiştir. Örneklenen bitki dokularının bazılarında D. sapinea tespit edilmiş olmakla birlikte, Leptoglossus occidentalis’ten izole edilememiştir. Buna göre, örnekleme alanlarında böcek ve fungus birlikte bulunmasına rağmen Leptoglossus occidentalis’in Diplodia sapinea’nın vektörü olduğuna dair herhangi bir kanıt bulunmamıştır. Leptoglossus occidentalis’ten izole edilen 25 mantar türü tespit edilmesine rağmen, tamamının entomopatojen fungus olmadığı belirlenmiştir. Zararlının Türkiye’nin hemen hemen tamamına yayıldığı ve ibreli türlerde tohum verimi ve kalitesi üzerinde önemli bir risk etmeni haline geldiği ortaya konulmuştur.

Keywords

• Çam kozalak emici böceği
• yabancı istilacı tür
• yaşam döngüsü
• Diplodia sapinea
• Türkiye

References

1. Arslangündoğdu, Z., Hızal, E., 2010. The western conifer seed bug, Leptoglossus occidentalis (Heidemann, 1910), recorded in Turkey (Heteroptera: Coreidae). Zoology in the Middle East, 50(1): 138-139.
2. Awan, H. U. M., Pettenella, D. 2017. Pine nuts: a review of recent sanitary conditions and market development. Forests, 8(10): 367.
3. Barta, M., 2009. New facts about distribution and host spectrum of the invasive Nearctic conifer pest, Leptoglossus occidentalis (Heteroptera: Coreidae) in south-western Slovakia. Folia Faunistica Slovaca, 14(23): 139-142.
4. Barta M., 2016. Biology and temperature requirements of the invasive seed bug Leptoglossus occidentalis (Heteroptera: Coreidae) in Europe. Journal of Pest Science, 89: 31-44.
5. Bates, S.L., Borden, J.H., 2005. Life table for Leptoglossus occidentalis (Heteroptera: Coreidae) and prediction of damage in lodgepole pine seed orchards. Agricultural and Forest Entomology, 7: 145-151.
6. Ben Jamâa, M., Mejri, M., Naves, P., Sousa, E., 2013. Detection of Leptoglossus occidentalis Heidemann, 1910 (Heteroptera: Coreidae) in Tunisia. African Entomology, 21(1): 165-167.
7. Bernardinelli, I., Rovato, M., Zandigiacomo, P., 2006. Life history and laboratory rearing of Leptoglossus occidentalis. In: Forster B, Knizek M, Grodzki W, (eds) Methodology of forest insect and disease survey in central Europe. IUFRO 7.03.10, Proceedings of the Workshop, 11–14 September 2006, Gmunden, Austria.
8. Cibrián-Tovar, D., Ebel, B.H., Yates, H.O., Méndez-Montiel, J.T., 1986. Cone and seed insects of the Mexican conifers. General Technical Report, Southeastern Forest Experiment Service, USDA Forest Service, No. SE-40, viii + 110 pp.

9. Çerçi, B., Koçak, Ö., 2016. Contribution to the knowledge of Heteroptera (Hemiptera) fauna of Turkey. Journal of Insect Biodiversity, 4(15): 1-18.
10. Çerçi, B., Karataş, A., Karataş, A., 2021. Insecta non gratae: New distribution records of eight alien bug (Hemiptera) species in Turkey with contributions of citizen science. Zootaxa, 5057(1): 1-28.
11. Dursun G., 2016. Balıkesir kent ormanı ve BAUN Çağış yerleşkesindeki Heteroptera (Hemiptera) faunasının kışlak tuzaklarla belirlenmesi üzerinde araştırmalar. Yüksek Lisans Tezi, Balıkesir Üniversitesi, Fen Bilimleri Enstitüsü, Balıkesir.
12. Farinha A.O., Branco M., Pereira M.F.C., Auger-Rozenberg M.A., Mauricio A., Yart A., Guerreiro V., Sousa E.M.R., Roques A., 2018. Micro X-ray computed tomography suggests cooperative feding among adult invasive bugs Leptoglossus occidentalis on mature seeds of stone pine Pinus pinea. Agricultural and Forest Entomology, 20: 18-27.
13. Faúndez E.I., Rocca J.R., 2017. La chinche de las coníferas occidental, Leptoglossus occidentalis Heidemann (Heteroptera: Coreidae) en Chile; rápida expansión, posibles impactos y desafíos. Revista Chilena de Entomología, 42.
14. Feducci, M., Pepori, A., Benassai, D., Cambi, M., Capretti, P., 2009. Cone damages by Diplodia pinea and seed boring insects on Pinus pinea L. (italian stone pine) in central Italy. Suleyman Demirel University, Faculty of Forestry Journal Special Issue: 41-47
15. Fent M., Kment P., 2011. First record of the invasive western conifer seed bug Leptoglossus occidentalis (Heteroptera: Coreidae) in Turkey. North-Western Journal of Zoology, 7 (1): 72-80.
16. Heidemann O., 1910. New species of Leptoglossus from North America. Proceedings of the Entomological Society of Washington, 12: 191-197.
17. Hızal, E. 2012. Two invasive alien insect species, Leptoglossus occidentalis (Heteroptera: Coreidae) and Cydalima perspectalis (Lepidoptera: Crambidae), and their distribution and host plants in Istanbul Province, Turkey. Florida Entomologist, 95(2): 344-349.
18. Hızal, E., İnan, M., 2012. Leptoglossus occidentalis (Heidemann, 1910) is an invasive insect species, Journal of the Bartin Faculty of Forestry, 14: 56-61.
19. İpekdal, K. 2022. Estimating the potential threat of increasing temperature to the forests of Turkey: a focus on two invasive alien insect pests. iForest-Biogeosciences and Forestry, 15(6), 444-450.
20. İpekdal, K., Oğuzoğlu, Ş., Oskay, F., Aksu, Y., Doğmuş Lehtijärvi, H. T., Lehtijärvi A. T., Can T., Aday Kaya, A. G., Özçankaya, M., Avcı, M. 2019. Western Conifer Seed Bug Leptoglossus occidentalis Heidemann (1910) (Hemiptera: Coreidae) Current Situation in the World and Turkey. General Directorate of Forestry, Ankara, Turkey.
21. Ishikawa, T., Kikuhara, Y., 2009. Leptoglossus occidentalis Heidemann (Hemiptera: Coreidae), a presumable recent invader to Japan. Japanese Journal of Entomology, 12(3): 115-116.
22. Kalkan, M., Arık, G., Çiçekçi, G., Yılmaz, M., Parlak, S. 2021. Çam kozalak emici böceği (Leptoglossus occidentalis Heidemann)’nin karaçam ve sarıçam tohumlarının doluluk ve çimlenmesine etkisi. Ağaç ve Orman, 2(1): 29-34.
23. Kılcı, M., Akbin, G., Sayman, M., Özçankaya, M.İ. 2013. Kozak Yöresi Fıstık Çamlarında Gübrelemenin Kozalak Verimine Etkisi. Ege Ormancılık Araştırma Enstitüsü. Teknik Bülten No: 52.
24. Koerber, T.W., 1963. Leptoglossus occidentalis (Hemiptera, Coreidae), a newly discovered pest of coniferous seed. Annals of the Entomological Society of America, 56(2): 229-234.
25. Liebhold, A. M., Brockerhoff, E. G., Kalisz, S., Nuñez, M. A., Wardle, D. A., Wingfield, M. J. 2017. Biological invasions in forest ecosystems. Biological Invasions, 19: 3437-3458.
26. Luchi, N., Capretti, P., Surico, G., Orlando, C., Pazzagli, M., Pinzani, P., 2005. A Real-Time quantitative PCR assay for the detection of Sphaeropsis sapinea from ınoculated Pinus nigra shoots. Journal of Phytopathology, 153(1): 37–42.
27. Luchi, N., Mancini, V., Feducci, M., Santini, A., Capretti, P., 2012. Leptoglossus occidentalis and Diplodia pinea: a new insect-fungus association in Mediterranean forests. Forest Pathology, 42: 246-251.
28. Maltese, M., Caleca, V., Carapezza, A., 2009. Primi reperti in Sicilia su diffusione e biologia di Leptoglossus occidentalis Heidemann (Hetroptera: Coreidae), cimice americana dei semi delle conifere. In Congresso Nazionale di Selvicoltura, 3: 1413-1418.
29. Mas, H., Naya, M., Pe´rez-Laorga, E., Aguado, A., Marco, M., Aragoneses, J., Rodrigo, E., 2013. Estudio del ciclo biolo´gico de Leptoglossus occidentalis Heidemann, 1910 (Hemiptera, Coreidae) en la Comunitat Valenciana. 6th Spanish Forest Congress, 10–14 June 2013, pp:13.
30. Mitchell, P.L., 2000. Leaf-footed bugs (Coreidae). In: Schaeffer CW, Panizzi AR (eds) Heteroptera of economic importance. CRC Press, Boca Raton, 337-403.
31. OGM. 2023. Ormancılık İstatistikleri. https://www.ogm. gov.tr/tr/e-kutuphane/resmi-istatistikler (Ziyaret Tarihi: 14.05.2024)
32. Oğuzoğlu Ş., Avcı M., 2020. Biological observations on Leptoglossus occidentalis Heidemann, 1910 (Hemiptera: Coreidae) in Turkey and contributions to its parasitoids and distribution. Turkish Journal of Forestry Research, 7: 9-21.
33. Özek, T., Avcı, M., 2017. Isparta Orman Bölge Müdürlüğü göknar, çam ve sedir ormanlarında tespit edilen kozalak zararlıları. Turkish Journal of Forestry, 18(3): 178-186.
34. Özden, S., Okan, T., Buğday, S. E., & Köse, C. (2022). Perspectives of farmers on the decline in Pinus pinea nut yield and the sustainability of the production: a case study in Kozak Basin in western Turkey. Agriculture, 12(7): 1070.
35. Özgen İ., Dioli P., Çelik V., 2017. New and interesting record of western conifer seed bug: Leptoglossus occidentalis (Heidemann, 1910) (Heteroptera: Coreidae) in Eastern Turkey. Journal of Entomology and Zoology Studies, 5(5): 830-833.
36. Parlak, S., 2017. An invasive species: Leptoglossus occidentalis (Heidemann) how does it affect forestry activities? Kastamonu University Journal of Forestry Faculty, 17(3): 531-542.
37. Petrakis, P. V., 2011. First record of Leptoglossus occidentalis (Heteroptera: Coreidae) in Greece. Entomologia Hellenica, 20(2): 83-93.
38. Putshkov, P. V., Gubin, A. I., Popov, G. V., Kalesnik, V. I., Syzhko, V. V., 2012. The North American intruder Leptoglossus occidentalis Heidemann (Heteroptera: Coreidae) settled down in Ukraine. Українська ентомофауністика, 3(3): 1-3.
39. Richardson, D. M., Rejmánek, M., 2011. Trees and shrubs as invasive alien species–a global review. Diversity and distributions, 17(5), 788-809.
40. Sousa, E., Pimpão, M., Valdiviesso, T., Naves, P., Branco, M. 2017. Cone pests of stone pine in the Mediterranean Basin. Mediterranean pine nuts from forests and plantations. Options Méditerranéennes Série A. Séminaires Méditerranéens, 122: 91-107.
41. Stanosz, G.R., Swar, W.J., Smith, D.R., 1999. RAPD marker and isozyme characterization of Sphaeropsis sapinea isolates from diverse coniferous hosts and locations. Mycological Research, 103: 1193-1202.
42. Stanosz, G. R., Blodgett, J. T., Smith, D. R., Kruger, E. L., 2001. Water stress and Sphaeropsis sapinea as a latent pathogen of red pine seedlings. New Phytologist, 149(3), 531–538.
43. Sümer, S., 2000. Shoot blight disease caused by Sphaeropsis sapinea in pine stands at the south-eastern region, Turkey. (OGM inceleme raporu)
44. Tamburini, M., Maresi, G., Salvadori, C., Battisti, A., Zottele, F., Pedrazzoli, F., 2012. Adaptation of the invasive western conifer seed bug Leptoglossus occidentalis to Trentino, an alpine region (Italy). Bulletin of Insectology, 65: 161-170.
45. Ünligil, H., Ertaş, A., 1993. İstanbul yakınlarındaki çam ağaçlarında Sphaeropsis sapinea (Fr.) Dyko & Sutton mantar hastalığı. İstanbul Üniversitesi Orman Fakültesi Dergisi, 43: 131-138.
46. Villa, M., Tescari, G., Taylor, S. J., 2001. Nuovi dati sulla presenza in Italia di Leptoglossus occidentalis. Bollettino della Società Entomologica Italiana, 133(2): 103-112.
47. White, T., Bruns, T., Lee, S., Taylor, J., 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis, M.A., Gelfand, D.H., Sninsky, JJ, White TJ, eds. PCR Protocols: A Guide to Methods and Applications. New York, USA: Academic Press Inc., ss. 315-322.
48. Yıldırım, E., Yazıcı, G., Moulet, P., 2013. Contribution to the knowledge of the Gerridae, Coreoidea, Piesmatidae, Saldidae, Corixoidea, Nepoidea and Notonectidae (Hemiptera, Heteroptera) fauna of Turkey. Linzer Biologische Beiträge, 45(1): 995-1010.