SURVEY OF THE GUT PATHOGENIC MICROFLORA ASSOCIATED WITH CATERPILLARS OF THE BOX TREE MOTH CYDALIMA PERSPECTALIS WALKER, 1859 (LEPIDOPTERA: CRAMBIDAE)
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Jan 23, 2019
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Abstract
The invasive box tree moth Cydalima perspectalis is an important and dangerous pest on Buxus spp. In this study, its destructive potential was evaluated in five areas of Bulgaria through the assessment of the defoliation levels caused by the caterpillars on the box trees. The microorganism species composition and diversity in the gut of caterpillars were investigated. In a total of 206 caterpillars, 5 bacterial (Acinetobacter schindleri, Enterococcus casseliflavus, Klebsiella mobilis, Paenibacillus anaericanus, and Paenibacillus popilliae) and 5 fungal species (Metarhizium sp., Beauveria sp., Verticillium sp., Alternaria sp. and Mucor sp.), were recovered. The most prevalent pathogen (52.4%) was the bacterium P. popilliae. Two entomopathogenic fungi, Metarhizium sp. and Beauveria sp., were observed in high and quite similar prevalences of 29.6% and 28.6%, respectively. The presence of these three pathogens (P. popilliae, Metarhizium sp. and Beauveria sp.) in relatively high levels in the gut of caterpillars indicates the possible role of gut pathogenic microorganisms as agents affecting caterpillar survival in natural populations of the pests. Further research is needed to assess the effect of the identified bacteria and fungi on C. perspectalis life stages.
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Harizanova, V., Naydenov, M., Stoeva, A., Valcheva, I., Draganova, D., Borisov, Y., & Mohamedova, M. (2019). SURVEY OF THE GUT PATHOGENIC MICROFLORA ASSOCIATED WITH CATERPILLARS OF THE BOX TREE MOTH CYDALIMA PERSPECTALIS WALKER, 1859 (LEPIDOPTERA: CRAMBIDAE). Acta Entomologica Serbica, 23(2), 15-25. https://doi.org/10.5281/zenodo.2547665
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References
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Arnaudov, V., & Raikov, S. (2017). Box tree moth – Cydalima perspectalis (Walker, 1859) (Lepidoptera: Crambidae), a new invasive pest for the bulgarian fauna. “XXII Savetovanje o biotehnologiji”. Zbornikradova, 1, 453-456.
Barnettand, H. L., & Hunter, B. B. (1987). Illustrated genera of imperfect fungi. New York. MacMillan Publishing Company. 147 pp.
Belokobylskij, S. A., & Gninenko, Y. I. (2016). A solitary endoparasitoid (Hymenoptera: Braconidae: Microgastrinae) of the severe Buxus pest Cydalima perspectalis (Lepidoptera: Crambidae) in the North Caucasus of Russia. Zoosystematica rossica, 25(2), 248-254.
Beshkov, S., Abadjiev, S., & Dimitrov, D. (2015). Cydalima perspectalis (Walker, 1859) (Lepidoptera: Pyraloidea: Crambidae: Spilomelinae) – new invasive pest moth in Bulgaria. The entomologist’s record and Journal of Variation, 127, 18-22.
Billen, W. (2007). Diaphania perspectalis (Lepidoptera: Pyralidae) – a new moth in Europe. Mitteilungender Entomologischen Gesellschaft Basel, 57, 135-137.
Burjanadze, M., Nakaidze, E., Arjevanidze, M., & Abramishvili, T. (2013). Effect of local strains of Beauveria bassiana (Bb024) and Metarhizium anisopliae (M7/2) against the fall webworm, Hyphantria cunea (Lepidoptera: Arctiidae) in Georgia. Proceedings of the Meeting Biological Control - its unique role in organic and integrated production. Zagreb (Croatia), pp. 97-101.
Butt, T. M., Jackson, C., & Magan, N. (2001). Introduction-fungal control agents: progress, problems and potential. In Butt, T. M., Jackson, C., & Magan, N. (Eds.), “Fungi as biocontrolagent” (pp. 1-8). UK: CABI International.
Chen, B., The, B.-S., Sun, C., Lu, X., Boland, W., & Shao, Y. (2016). Biodiversity and activity of the gut microbiota across the life history of the insect herbivore Spodoptera littoralis. Scientific Reports, 6, 29505.
Draganova, S., Takov, D., Pilarska, D., Doychev, D., Mirchev, P., & Georgiev, G. (2013). Fungal pathogens on some Lepidopteran forest pests in Bulgaria. Acta Zoologica Bulgarica, 65(2), 179-186.
Early, R., Bradley, B. A., Dukes, J. S., Lawler, J. J., Olden, J. D., Blumenthal, D. M., Gonzalez, P., Grosholz, E. D., Ibanez, I., Miller, L. P., Cascade, S. J. B., & Andrew, T. J. (2016). Global threats from invasive alien species in the twenty-first century and national response capacities. Nature communication. Retrieved from: https://www.nature.com/articles/ncomms12485.
EPPO, 2014. EPPO Reporting Service, No. 2014/015. Paris, France: European and Mediterranean Plant Protection Organization.
Fora, C. G., Sasu, L., Poşta, D., & Berar, C. (2016). Chemical possibilities of Cydalima perspectalis Walk. (Lepidoptera: Crambidae) control. Journal of Horticulture, Forestry and Biotechnology, 20(3), 31-34.
Goettel, M. S., Poprawski, T. J., Vandenberg, J. D., Li, Z., & Roberts, D. W. (1990). Safety to nontarget invertebrates of fungal biocontrol agents. In Laird, M., Lacey, L. A., & Davidson, E. W. (Eds.), “Safety of Microbial Insecticides” (pp. 347-375). Boca Raton, Florida, CRC Press.
Göttig, S. & Herz, A. (2016). Are egg parasitoids of the genus Trichogramma (Hymenoptera: Trichogrammatidae) promising biological control agents for regulating the invasive box tree pyralid, Cydalima perspectalis (Lepidoptera: Crambidae)? Biocontrol Science and Technology, 26(11), 1471-1488.
Göttig, S., Korn, S., & Herz, A. (2017). Repellent and toxic properties of plant oils and extracts on Cydalima perspectalis Walker (Lepidoptera: Crambidae). Archives of Phytopathology and Plant Protection, 50(13-14), 658-673.
Hızal, E. (2012). Two invasive alien insect species, Leptoglossus occidentalis (Heteroptera: Coreidae) and Cydalima perspectalis (Lepidoptera: Crambidae), and their distribution and hostplants in Istanbul province, Turkey. Florida Entomologist, 95(2), 344-349.
Hoover, J. (2000). Insect advice from extension: Gypsy Moth (Limantria dispar L.). Penn state Colleage of Agriculture Science. Retrieved from: http://ento.psu.edu/extension/factsheets/pdf/gypsymoth.pdf
Humber, R. A. (2005). Entomopathogenic FungalI dentification. Retrieved from: https://www.ars.usda.gov/ARSUserFiles/80620520/apswkshoprev.pdf
Indiragandhi, O., Anandham, R., Madhaiyan, M., Poonguzhali, S., Kim, G. H., Saravanan, V. S., & Sa, T. (2007). Cultivable bacteria associated with larval gut of prothiofos-resistant, prothiofos0susceptible and field-caught populations of diamondback moth, Plutella xylostella and their potential for, antagonism towards entomopathogenic fungi and host insect nutrition. Journal of Applied Microbiology, 103, 2664-2675.
Karthikaraj, K., Prasannakumar, K., & Isaiarasu, L. (2013). Use of plant extracts for the control of flacherie disease in silkworm, Bombyx mori L. (Lepidoptera: Bombicidae). International Journal of Microbiology Research, 4, 158-161.
Klein, M. G. (1992). Use of Bacillus popilliae in Japanese beetle control. In Jackson, T. A., & Glare, T. R. (Eds.), “Use of Pathogens in Scarab Pest Management” (pp. 179-189). Hampshire, UK, Intercept Limited.
Korycinska, A., & Eyre, D. (2011). Box tree caterpillar Cydalima perspectalis – plant pest factsheet. The Food and Environment Research Agency (Fera). Retrieved from: https://planthealthportal.defra.gov.uk/assets/factsheets/boxTreeCaterpillar2011.pdf
Lacey, L. A., Grzywacz, D., Shapiro-Ilan, D. I., Frutos, R., Brownbridge, M., & Goettel, M. S. (2015). Insect pathogens as biological control agents: Back to the future. Journal of Invertebrate Pathology, 132, 1-41.
Leuthardt, F. L. G. (2013). Cydalima perspectalis (box tree moth). Invasive Species Compendium. Retrieved from: https://www.cabi.org/isc/datasheet/118433.
Osborn, F., Berlioz, L., Vitelli-Flores, J, Monsalve, W., Dorta, B., & Lemoine, V. R. (2002). Pathogenic effects of bacteria isolated from larvae of Hylesia metabus Crammer (Lepidoptera: Saturniidae). Journal of Invertebrate Pathology, 80, 7-12.
Mirchev, P., & Tsankov, G. (2000). Factors influencing changes in the distribution and economic importance of the pine processionary moth (Thaumetopoea pityocampa Den. et Schiff.) in Bulgaria. Forest Science, 2(3), 15-24.
Panajotov, P., Zashev, B., Grigorova, R., & Tsankov, G. (1960). Entomopathogenic fungi on caterpillars of Lymantria dispar L. in Bulgaria. Bulletin de l‘Institut central desforests, 6, 205-208.
Penchevа, A., & Yovkova, M. (2016). New data on alien insect pests of ornamental plants in Bulgaria. Forestry Ideas, 22, 17-33.
Pilarska, D., Georgiev, G., McManus, M., Mirchev, P., Pilarski, P., & Linde, A. (2007). Entomophaga maimaiga – an effective introduced pathogen of the gypsy moth (Lymantria dispar L.) in Bulgaria. Proceeding of the International Conference „Alien Arthropods in South East Europe – crossroad of three continents”. University of Forestry, Sofia, Bulgaria, pp. 37- 43.
Priya, G. N., Ojha, A., Kajla, M. K., Raj, A., & Rajagopal, R. (2012). Host plant induced variation in gut bacteria of Helicoverpa armigera. PLoS ONE, 7(1), e30768.
Pu, Z. L., & Li, Z. Z. (1996). Insect Mycology. Hefei, Anhui,China: Science Technology Press, 375 p.
Rajendran, L., Samiyappan, R., Raguchander, T., & Saravanakumar, D. (2007). Endophytic bacteria mediate plant resistance against cotton bollworm. Journal of Plant Interaction, 2(1), 1-10.
Raineri, V., Bonechi, F., Caracciolo, D., Cresta, P., & Mariotti, M. (2017). Cydalima perspectalis (Walker, 1859) (Lepidoptera, Crambidae) and the threats for the nature 2000 habitat 5110 in Liguria (NW-Italy). Bollettino dei Musei e Degli Istituti Biologici dell’Universita di Genova, 79, 215-236.
Rippere, K. E., Tran, M. T., Yousten, A. A., Hilu, K. H., & Klein, M. G. (1998). Bacillus popilliae and Bacillus lentimorbus, bacteria causing milky disease in Japanese beetles and related scarab larvae. International Journal of Systematic Bacteriology, 48, 395-402.
Sakai, A. K., Allendorf, F. W., Holt, J. S., Lodge, D. M., Molofsky, J., With, K. A., Baughman, S., Cabin, J. R., Cohen, J. E., Ellstrand, N. C., McCauley, D. E., O’Neil, P., Parker, I. M., Thompson, J. N., & Weller, S. G. (2001). The population biology of invasive species. Annual review of Ecology and Systematics, 32, 305-332.
Samson, R. A., Evans, H. C., & Latgé, J. P. (1988). Atlas of entomopathogenic fungi. New York, Springer-Verlag, 187pp.
Santi, F., Radeghieri, P., Inga-Sigurta, G., & Maini, S. (2015). Sex pheromone traps for detection of the invasive box tree moth in Italy. Bulletin of Insectology, 68(1), 158-160.
Sapna Bai, N., Sasidharan, T. O., Remadevi, O. K., Rajan, P. D., & Balachander, M. (2010). Virulence of Metarhizium isolates against the polyphagous defoliator pest, Spilarctia obliqua (Lepidoptera: Arctiidae). Journal of Tropical Forest Science, 22(1), 74-80.
Sharon, G., Segal, D., Ringo, J. M., Hefetz, A., & Rosenberg, I. Z. (2010). Commensal bacteria play a role in mating preference of Drosophila melanogaster. PNAS, 107(46), 20051-20056.
Subhashini, D. V. (2015). Role of gut bacteria associated with the chlorpyrifos resistant tobacco leaf eating caterpillar Spodoptera litura on the efficacy of entomopathogenic fungi Beauveria bassiana and Paecilomyces sp. Journal of Biological Control, 29(2), 98-102.
Takov, D. I., Doychev, D. D., Linde, A., Draganova, S. A., & Pilarska, D. K. (2012). Pathogens of bark beetles (Curculionidae: Scolytinae) and other beetles in Bulgaria. Biologia, 67(5), 966-972.
Zhang, J., Shen, Z., Tang, X., Xu, L., & Zhu, F. (2013). Isolation and identification of a pathogen, Providencia rettgeri, in Bombyx mori. Global Journal of Bacteriology, Cytology and Nematology, 1(1), 49-55.
Arnaudov, V., & Raikov, S. (2017). Box tree moth – Cydalima perspectalis (Walker, 1859) (Lepidoptera: Crambidae), a new invasive pest for the bulgarian fauna. “XXII Savetovanje o biotehnologiji”. Zbornikradova, 1, 453-456.
Barnettand, H. L., & Hunter, B. B. (1987). Illustrated genera of imperfect fungi. New York. MacMillan Publishing Company. 147 pp.
Belokobylskij, S. A., & Gninenko, Y. I. (2016). A solitary endoparasitoid (Hymenoptera: Braconidae: Microgastrinae) of the severe Buxus pest Cydalima perspectalis (Lepidoptera: Crambidae) in the North Caucasus of Russia. Zoosystematica rossica, 25(2), 248-254.
Beshkov, S., Abadjiev, S., & Dimitrov, D. (2015). Cydalima perspectalis (Walker, 1859) (Lepidoptera: Pyraloidea: Crambidae: Spilomelinae) – new invasive pest moth in Bulgaria. The entomologist’s record and Journal of Variation, 127, 18-22.
Billen, W. (2007). Diaphania perspectalis (Lepidoptera: Pyralidae) – a new moth in Europe. Mitteilungender Entomologischen Gesellschaft Basel, 57, 135-137.
Burjanadze, M., Nakaidze, E., Arjevanidze, M., & Abramishvili, T. (2013). Effect of local strains of Beauveria bassiana (Bb024) and Metarhizium anisopliae (M7/2) against the fall webworm, Hyphantria cunea (Lepidoptera: Arctiidae) in Georgia. Proceedings of the Meeting Biological Control - its unique role in organic and integrated production. Zagreb (Croatia), pp. 97-101.
Butt, T. M., Jackson, C., & Magan, N. (2001). Introduction-fungal control agents: progress, problems and potential. In Butt, T. M., Jackson, C., & Magan, N. (Eds.), “Fungi as biocontrolagent” (pp. 1-8). UK: CABI International.
Chen, B., The, B.-S., Sun, C., Lu, X., Boland, W., & Shao, Y. (2016). Biodiversity and activity of the gut microbiota across the life history of the insect herbivore Spodoptera littoralis. Scientific Reports, 6, 29505.
Draganova, S., Takov, D., Pilarska, D., Doychev, D., Mirchev, P., & Georgiev, G. (2013). Fungal pathogens on some Lepidopteran forest pests in Bulgaria. Acta Zoologica Bulgarica, 65(2), 179-186.
Early, R., Bradley, B. A., Dukes, J. S., Lawler, J. J., Olden, J. D., Blumenthal, D. M., Gonzalez, P., Grosholz, E. D., Ibanez, I., Miller, L. P., Cascade, S. J. B., & Andrew, T. J. (2016). Global threats from invasive alien species in the twenty-first century and national response capacities. Nature communication. Retrieved from: https://www.nature.com/articles/ncomms12485.
EPPO, 2014. EPPO Reporting Service, No. 2014/015. Paris, France: European and Mediterranean Plant Protection Organization.
Fora, C. G., Sasu, L., Poşta, D., & Berar, C. (2016). Chemical possibilities of Cydalima perspectalis Walk. (Lepidoptera: Crambidae) control. Journal of Horticulture, Forestry and Biotechnology, 20(3), 31-34.
Goettel, M. S., Poprawski, T. J., Vandenberg, J. D., Li, Z., & Roberts, D. W. (1990). Safety to nontarget invertebrates of fungal biocontrol agents. In Laird, M., Lacey, L. A., & Davidson, E. W. (Eds.), “Safety of Microbial Insecticides” (pp. 347-375). Boca Raton, Florida, CRC Press.
Göttig, S. & Herz, A. (2016). Are egg parasitoids of the genus Trichogramma (Hymenoptera: Trichogrammatidae) promising biological control agents for regulating the invasive box tree pyralid, Cydalima perspectalis (Lepidoptera: Crambidae)? Biocontrol Science and Technology, 26(11), 1471-1488.
Göttig, S., Korn, S., & Herz, A. (2017). Repellent and toxic properties of plant oils and extracts on Cydalima perspectalis Walker (Lepidoptera: Crambidae). Archives of Phytopathology and Plant Protection, 50(13-14), 658-673.
Hızal, E. (2012). Two invasive alien insect species, Leptoglossus occidentalis (Heteroptera: Coreidae) and Cydalima perspectalis (Lepidoptera: Crambidae), and their distribution and hostplants in Istanbul province, Turkey. Florida Entomologist, 95(2), 344-349.
Hoover, J. (2000). Insect advice from extension: Gypsy Moth (Limantria dispar L.). Penn state Colleage of Agriculture Science. Retrieved from: http://ento.psu.edu/extension/factsheets/pdf/gypsymoth.pdf
Humber, R. A. (2005). Entomopathogenic FungalI dentification. Retrieved from: https://www.ars.usda.gov/ARSUserFiles/80620520/apswkshoprev.pdf
Indiragandhi, O., Anandham, R., Madhaiyan, M., Poonguzhali, S., Kim, G. H., Saravanan, V. S., & Sa, T. (2007). Cultivable bacteria associated with larval gut of prothiofos-resistant, prothiofos0susceptible and field-caught populations of diamondback moth, Plutella xylostella and their potential for, antagonism towards entomopathogenic fungi and host insect nutrition. Journal of Applied Microbiology, 103, 2664-2675.
Karthikaraj, K., Prasannakumar, K., & Isaiarasu, L. (2013). Use of plant extracts for the control of flacherie disease in silkworm, Bombyx mori L. (Lepidoptera: Bombicidae). International Journal of Microbiology Research, 4, 158-161.
Klein, M. G. (1992). Use of Bacillus popilliae in Japanese beetle control. In Jackson, T. A., & Glare, T. R. (Eds.), “Use of Pathogens in Scarab Pest Management” (pp. 179-189). Hampshire, UK, Intercept Limited.
Korycinska, A., & Eyre, D. (2011). Box tree caterpillar Cydalima perspectalis – plant pest factsheet. The Food and Environment Research Agency (Fera). Retrieved from: https://planthealthportal.defra.gov.uk/assets/factsheets/boxTreeCaterpillar2011.pdf
Lacey, L. A., Grzywacz, D., Shapiro-Ilan, D. I., Frutos, R., Brownbridge, M., & Goettel, M. S. (2015). Insect pathogens as biological control agents: Back to the future. Journal of Invertebrate Pathology, 132, 1-41.
Leuthardt, F. L. G. (2013). Cydalima perspectalis (box tree moth). Invasive Species Compendium. Retrieved from: https://www.cabi.org/isc/datasheet/118433.
Osborn, F., Berlioz, L., Vitelli-Flores, J, Monsalve, W., Dorta, B., & Lemoine, V. R. (2002). Pathogenic effects of bacteria isolated from larvae of Hylesia metabus Crammer (Lepidoptera: Saturniidae). Journal of Invertebrate Pathology, 80, 7-12.
Mirchev, P., & Tsankov, G. (2000). Factors influencing changes in the distribution and economic importance of the pine processionary moth (Thaumetopoea pityocampa Den. et Schiff.) in Bulgaria. Forest Science, 2(3), 15-24.
Panajotov, P., Zashev, B., Grigorova, R., & Tsankov, G. (1960). Entomopathogenic fungi on caterpillars of Lymantria dispar L. in Bulgaria. Bulletin de l‘Institut central desforests, 6, 205-208.
Penchevа, A., & Yovkova, M. (2016). New data on alien insect pests of ornamental plants in Bulgaria. Forestry Ideas, 22, 17-33.
Pilarska, D., Georgiev, G., McManus, M., Mirchev, P., Pilarski, P., & Linde, A. (2007). Entomophaga maimaiga – an effective introduced pathogen of the gypsy moth (Lymantria dispar L.) in Bulgaria. Proceeding of the International Conference „Alien Arthropods in South East Europe – crossroad of three continents”. University of Forestry, Sofia, Bulgaria, pp. 37- 43.
Priya, G. N., Ojha, A., Kajla, M. K., Raj, A., & Rajagopal, R. (2012). Host plant induced variation in gut bacteria of Helicoverpa armigera. PLoS ONE, 7(1), e30768.
Pu, Z. L., & Li, Z. Z. (1996). Insect Mycology. Hefei, Anhui,China: Science Technology Press, 375 p.
Rajendran, L., Samiyappan, R., Raguchander, T., & Saravanakumar, D. (2007). Endophytic bacteria mediate plant resistance against cotton bollworm. Journal of Plant Interaction, 2(1), 1-10.
Raineri, V., Bonechi, F., Caracciolo, D., Cresta, P., & Mariotti, M. (2017). Cydalima perspectalis (Walker, 1859) (Lepidoptera, Crambidae) and the threats for the nature 2000 habitat 5110 in Liguria (NW-Italy). Bollettino dei Musei e Degli Istituti Biologici dell’Universita di Genova, 79, 215-236.
Rippere, K. E., Tran, M. T., Yousten, A. A., Hilu, K. H., & Klein, M. G. (1998). Bacillus popilliae and Bacillus lentimorbus, bacteria causing milky disease in Japanese beetles and related scarab larvae. International Journal of Systematic Bacteriology, 48, 395-402.
Sakai, A. K., Allendorf, F. W., Holt, J. S., Lodge, D. M., Molofsky, J., With, K. A., Baughman, S., Cabin, J. R., Cohen, J. E., Ellstrand, N. C., McCauley, D. E., O’Neil, P., Parker, I. M., Thompson, J. N., & Weller, S. G. (2001). The population biology of invasive species. Annual review of Ecology and Systematics, 32, 305-332.
Samson, R. A., Evans, H. C., & Latgé, J. P. (1988). Atlas of entomopathogenic fungi. New York, Springer-Verlag, 187pp.
Santi, F., Radeghieri, P., Inga-Sigurta, G., & Maini, S. (2015). Sex pheromone traps for detection of the invasive box tree moth in Italy. Bulletin of Insectology, 68(1), 158-160.
Sapna Bai, N., Sasidharan, T. O., Remadevi, O. K., Rajan, P. D., & Balachander, M. (2010). Virulence of Metarhizium isolates against the polyphagous defoliator pest, Spilarctia obliqua (Lepidoptera: Arctiidae). Journal of Tropical Forest Science, 22(1), 74-80.
Sharon, G., Segal, D., Ringo, J. M., Hefetz, A., & Rosenberg, I. Z. (2010). Commensal bacteria play a role in mating preference of Drosophila melanogaster. PNAS, 107(46), 20051-20056.
Subhashini, D. V. (2015). Role of gut bacteria associated with the chlorpyrifos resistant tobacco leaf eating caterpillar Spodoptera litura on the efficacy of entomopathogenic fungi Beauveria bassiana and Paecilomyces sp. Journal of Biological Control, 29(2), 98-102.
Takov, D. I., Doychev, D. D., Linde, A., Draganova, S. A., & Pilarska, D. K. (2012). Pathogens of bark beetles (Curculionidae: Scolytinae) and other beetles in Bulgaria. Biologia, 67(5), 966-972.
Zhang, J., Shen, Z., Tang, X., Xu, L., & Zhu, F. (2013). Isolation and identification of a pathogen, Providencia rettgeri, in Bombyx mori. Global Journal of Bacteriology, Cytology and Nematology, 1(1), 49-55.