Diversity of insect carried-fungi in chili (Capsicum annuum) crop at Banyumas District, Central Java Province, Indonesia

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AGUS SUROTO
ENDANG MUGIASTUTI
TARJOKO
EKA OKTAVIANI
MUHAMMAD BAHRUDIN

Abstract

Abstract. Suroto A, Mugiastuti E, Tarjoko, Oktaviani E, Bahrudin M. 2023. Diversity of insect carried-fungi in chili (Capsicum annuum) crop at Banyumas District, Central Java Province, Indonesia. Biodiversitas 24: 3394-3406. This study aimed to determine the species of fungal pathogens that have the potency to be carried by various insects in endemic areas of chili (Capsicum annuum L.) disease and locations with high populations of chili insect vectors in the Banyumas District. The insect samples were collected from three chili planting locations in Banyumas District (Karanglewas, Sumbang, and Sokaraja Sub-districts) from March to November 2022. The following methods carried out the research: (i) determining the sampling location, (ii) insect sampling and identification, (iii) isolation and purification of fungal pathogen carried by insects, (iv) pathogenicity test, (v) identification of fungal pathogens based on morphology characters. The exploration of 13 villages in 3 (three) sub-districts of Banyumas District found 60 insects collected from healthy and diseased chili plants. Totally, six genera of fungi were isolated and identified, namely Fusarium, Pythium, Curvularia, Penicillium, Geotrichum, and Phytophthora. This is preliminary research on the interaction between plants, microbes, and insects. Understanding these aspects is essential, not only from an ecological perspective but also for improving the genetic quality of crops as well as for integrated pest management.

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References
Agrios G. N. 2008. Transmission of plant diseases by insects in Encyclopedia of Entomology. ed. Capinera J. L. (Springer Dordrecht, Netherlands), pg 3853–3885. https://doi.org/10.1007/978-1-4020-6359-6
Agrios, G.N. 1997. Plant pathology 4th Ed. London: Academic Press.
Aleknavi?ius, D., Lukša, J., Strazdait?-Žielien?, Ž., Servien?, E. 2022. The bacterial microbiota of edible insects Acheta domesticus and Gryllus assimilis revealed by high content analysis. Foods 11(8):1073. doi: 10.3390/foods11081073
Amteme, K., & Tefa, A. 2018. Identification of Pathogenic Fungi in Several Varieties of Lowland Rice Seeds Based on Storage Models. Jurnal Pertanian Konservasi Lahan Kering 3(1): 4-7. doi: 10.32938/sc.v3i01.150
Arma, R., Sari, D.E., Irsan. 2018. Identification of fruit flies (Bactrocera sp.) on chilli plants. Jurnal Agrominansia 3 (2): 109-119. doi: 10.34003/272007
Asghar, U., Malik, M. F., Anwar, F., Javed, A., & Raza, A. 2015. DNA Extraction from insects by using different techniques: A review. Advances in Entomology 3 (4): 132–138. doi: 10.4236/ae.2015.34016
Asniah, Syair, Wahyuni, T.A.S. 2012. Survey on Rotten Disease Incidence on Staik Base (Phytophthora capsici) of Pepper Plant (Piper ningrum. L) in South Konawe Regency. J Agroteknos. 2(3):151–157
Azhari, A.A., Sayuthi, M., Hasnah, H. 2019. Pathogenicity of Fungi Metarhizium anisopliae (Metsch) in controlling Green Stink bug (Nezara viridula L.) at Different Developmental Stages in Laboratory). Jurnal Ilmiah Mahasiswa Pertanian-AGT 4(2): 178-187. https://doi.org/10.17969/jimfp.v4i2.7424
Baba, K. & Inoue, S. 1936. The list of insects collected in Awashima Is., Nigata. [In Japanese.]. Insect World 40:401-403
Bande, L.O.S, Hadisutrisno, B., Somowiyarjo, S., Sunarminto, B.H. 2014. Distribution Pattern and Intensity of Pepper Foot Rot Disease in Southeast Sulawesi. J Agroteknos. 4(1):58–65.
Banjo, A. D., Lawal, O. A., Adeduji, O.O. 2005. Bacteria and fungi isolated from housefly (Musca domestica L.) larvae. African Journal of Biotechnology 4 (8): 780-784. https://www.ajol.info/index.php/ajb/article/view/15181
Barnett, H. L. 1960. Illustrated genera of imperfect fungi. Minneapolis.
Barnett, H.L., B.B. Hunter. 1998. Illustrated Genera of Imperfect Fungi 4th Edition. APS Press. The American Phytopathological Sociey. St Paul, Minnesota, 218 p.
Batubara, R. 2002. Biologi Serangga Penggerek Kayu. Fakultas Pertanian. Program Ilmu Kehutanan. Universitas Sumatera Utara. USU Digital Library.
Borror, D. J., & R. E. White. 1970. A Field Guide to Insects: America North of Mexico 2nd ed. Edition. Houghton Mifflin Company. USA.
Chandi, R.S. 2021. Integrated management of insect vectors of plant pathogens. Agricultural Reviews R-1982: 1-6. doi: 10.18805/ag.R-1982
Chapman, R.F. 2013. The Insects: Structure and Function 5th edition. Cambridge University Press. Cambridge.
Cicero, J.M., Adair, M.M., Adair Jr., R.C., Hunter, W.B., Avery, P.B., Mizel III, R.F. 2017. Predatory behavior of long-legged flies (Diptera: Dolichopodidae) and their potential negative effects on the parasitoid biological control agent of the Asian citrus psyllid (Hemiptera: Lividae). Florida Entomologist 100 (2): 485-487. https://doi.org/10.1653/024.100.0243
Dicke, M. & Baldwin, I.T. 2010. The evolutionary context for herbivore induced plant volatiles: beyond the ‘cry for help’. Trends in Plant Science 15: 167–175. doi: 10.1016/j.tplants.2009.12.002
Dugan, F.M. 2006. The Identification of Fungi. St Paul Minnesota. The American Phytopathological Society (APS) Press. ISBN: 0890543364
Dwiastuti, M.E., Fajrin, M.N. 2014. Root and crown rot diseases on strawberries (Fragaria x ananassa Dutch.) and their biological agents. Prosiding Seminar Nasional PERHORTI, Malang, Jawa Timur. ISBN 978-979-508-017-6
Efendi, S., Yaherwandi, Y., Nelly, N. 2018. Biology and demography statistics of Coccinella transversalis Thunberg (Coleoptera: Coccinellidae), predator of Aphis gossypii Glover (Homoptera: Aphididae). Jurnal Perlindungan Tanaman Indonesia 22 (1): 91-97. https://doi.org/10.22146/jpti.28409
Eigenbrode, S.D., Bosque-Perez, N.A., Davis, T.S. 2018. Insect-borne plant pathogens and their vectors: ecology, evolution, and complex interactions. Annual Review of Entomology 63: 169-191. https://doi.org/10.1146/annurev-ento-020117-043119
Engel, P., Moran, N.A. 2013. The gut microbiota of insects–diversity in structure and function. FEMS Microbiology Reviews. 37(5):699–735. doi: 10.1111/1574-6976.12025
Erb, M., Reymond, P. 2019. Molecular Interactions Between Plants and Insect Herbivores. Annual Review of Plant Biology, 70(1): 527-557. doi:10.1146/annurev-arplant-050718-095910
Erwin, D.C., Ribeiro, O.K. 1996. Phytophthora Diseases Worldwide. St Paul (USA): The American Phytopathological Society (APS) Press. https://doi.org/10.1046/j.1365-3059.1998.0179a.x
Fahy, P.C., and G.J. Persley 1983. Plant bacterial diseases, a diagnostic guide. In: Media and methods for isolation and diagnostic tests. Fahy, P.C and A. C. Haywad (eds.). Acadamic Press, New York. pp. 369-370.
Fardiaz, S. 1989. Mikrobiologi Pangan. Jurusan Teknologi Pangan dan Gizi. Fakultas Teknologi Pertanian IPB. Bogor.
Felton, G.W., Tumlinson, J.H. 2008. Plant-insect dialogs: complex interactions at the plant-insect interface. Curr Opin Plant Biol 11: 457–463. doi: 10.1016/j.pbi.2008.07.001
Franco, F.P., Moura, D.S., Vivanco, J.M., Silva-Filho, M.C., 2017. Plant–insect–pathogen interactions: a naturally complex ménage à trois. Curr. Opin. Microbiol. 37: 54–60. doi: 10.1016/j.mib.2017.04.007
Funder, S. 1953. Practical mycology: manual for identification of fungi. Broggers Boktr. Torlag, Oslo.
Galimberti, A., Alyokhin, A., Qu, H., Rose, J. 2020. Simulation modelling of potato virus Y spread in relation to initial inoculum and vector activity. Journal of Integrative Agricuture 19 (2): 376-388. doi: 10.1016/S2095-3119(19)62656-0
Gedling, C.R., Smith, C.M., LeMoine, C.M.R., Cassone, B.J. 2018. The Mexican bean beetle (Epilachna varivestis) regurgitome and insights into beetle-borne virus specificity. Plos One 13(1): e0192003. https://doi.org/10.1371/journal.pone.0192003
Ghosh S, Ghanim M. 2021. Factors Determining Transmission of Persistent Viruses by Bemisia tabaci and Emergence of New Virus–Vector Relationships. Viruses. 13(9):1808. https://doi.org/10.3390/v13091808
Guo, Y., Ji, N., Bai, L., Ma, J, Li, Z. 2022. Aphid viruses: a brief view of a long history. Front. Insect Sci 2: 846716. doi: 10.3389/finsc.2022.846716
Gupta, A., Nair, S. 2020. Dynamics of insect-microbiome interaction influence host and microbial symbiont. Frontiers in Microbiology 11:1357. doi: 10.3389/fmicb.2020.01357
Hatcher, P.E., 1995. Three-way interactions between plant pathogenic fungi, herbivorous
insects and their host plants. Biol. Rev. 70, 639–694. https://doi.org/10.1111/j.1469-185X.1995.tb01655.x
Heath, R. N., Wingfield, M. J., Van Wyk, M., & Roux, J. 2009. Insect associates of Ceratocystis albifundus and patterns of association in a native savanna ecosystem in South Africa. Environmental Entomology 38(2): 356–364. https://doi.org/10.1603/022.038.0207
Heck, M. 2018. Insect transmission of plant pathogens: a systems biology perspective. mSystems 3 (2):e00168-17. https://doi.org/10.1128/mSystems.00168-17
Hoesain, M., Prastowo, S., Suharto, Pradana, A.A., Aisyah, I.N., Alfarizy, F.K., Adiwena, M. 2021. Combination of plant growth-promoting bacteria and botanical pesticide increases organic red rice yield and reduces the Leptocorisa acuta population. Biodiversitas Journal of Biological Diversity 22 (4): 1686-1694. doi: 10.13057/biodiv/d22041
Ishigami, K., Jang, S., Itoh, H., Kikuchi, Y. 2021. Insecticide resistance governed by gut symbiosis in a rice pest, Cletus punctiger, under laboratory conditions. Biol. Lett. 18: 20200780. https://doi.org/10.1098/rsbl.2020.0780
Ivayani., Faishol, F., Prasetyo, J., Nurdin, M. 2018. The effectiveness of several isolates of Trichoderma sp. against the occurrence of downy mildew disease caused by Peronosclerospora maydis and growth of corn plants (Zea mays). Jurnal Penelitian Pertanian Terapan. 18(1): 39-45. https://doi.org/10.25181/jppt.v18i1.641
Iwebor, M., Frolov, S., Frolova, I., Shabaldas, O., Chernikova, M. 2020. The role of insects in the spreading of pathogens and development of diseases on
sunflower in the Krasnodar region of the Russian Federation. E3S Web of Conferences 222, 02025. https://doi.org/10.1051/e3sconf/202022202025
Jones, T.-K. L., & Medina, R. F. 2020. Corn stunt disease: An ideal insect-microbial-plant pathosystem for comprehensive studies of vector-borne plant diseases of corn. Plants 9(6): 747. https:// doi.org/10.3390/plants9060747
Khan, M.M., Guo, C-F., Peng, J., Fan, Z-Y., Hafeez, M., Ali, D., Wang, K., Almarzoug, M.H.A., Qiu, B-L. 2022. Screening and validation of reference gene using in RT-qPCR for gene expression studies in Paederus fuscipes, a medically and agriculturally important insect. Journal of King Saud University-Science 34:101654. https://doi.org/10.1016/j.jksus.2021.101654
Khan, M.M., Nawaz, M., Hua, H., Cai, W., Zhao, J. 2018. Lethal and sublethal effects of emamectin benzoate on the rove beetle, Paederus fuscipes, a non-target predator of rice brown planthopper, Nilaparvata lugens. Ecotoxicology and Environmental Safety 165: 19-24. https://doi.org/10.1016/j.ecoenv.2018.08.047
Koudamiloro, A., Togola, A., Djihinto, A.C., Dourokpindou, O.K., Akogbeto, M. 2019. Survey of potential insect vectors of Rice Yellow Mottle Virus in the Southern and Central rice basin of Benin. Journal of Applied Biosciences 133: 13504 - 13515.https://dx.doi.org/10.4314/jab.v133i1.3
Leitao, A.L. 2009. Potential of Penicillium species in the bioremediation field. Int. J. Environ. Res. Public Health. 6 (4): 1393-1417. doi: 10.3390/ijerph6041393
Li, W-H., Mou, D-F., Hsieh, C-K., Weng, S-H., Tsai, W-S., Tsai, C-W. 2021. Vector transmission of Tomato Yellow Leaf Curl Thailand Virus by the Whitefly Bemisia tabaci: circulative or propagative? Insects 12:181. https://doi.org/10.3390/insects12020181
Liu, B., Preisser, E.L., Chu, D., Pan, H., Xie, W., Wang, S., Wu, Q., Zhou, X., Zhang, Y. 2013. Multiple forms of vector manipulation by a plant-infecting virus: Bemisia tabaci and tomato yellow leaf curl virus. J Virol. 87(9):4929-37. doi: 10.1128/JVI.03571-12.
Luo, S.T., Zhang, X., Wang, J.F., Jiao, C.Y., Chen, Y.Y., Shen, Y.B. 2018. Plant ion channels and transporters in herbivory-induced signalling. Funct. Plant Biol. 45: 111–131. doi: 10.1071/FP16318
Maharani, Y., Maryana, N., Rauf, A., Hidayat, P. 2020. Insect parasitoid and ant of associated on aphids (Aphididae) colonies on plants in West Java. Cropsaver 3(2): 59-67. https://doi.org/10.24198/cropsaver.v3i2.30645
Mairawita, Habazar, T., Hasyim, A., Nazir, N., Suswati. 2012. The potential of flower-visiting insects as a vectors blood disease bacterium (Ralstonia solanacearum Phylotype IV) on bananas in West Sumatra. Indonesian Journal of Entomology 9(1): 38-47. doi: 10.5994/jei.9.1.38
Marianah, L. 2020. Insect vector and virus disease intensity on Red Chili Plants. Agrihumanis: Journal of Agriculture and Human Resource Development Studies 1(2): 127-134. doi: https://doi.org/10.46575/agrihumanis.v1i2.70
McDonald, F., Muller, G. 1992. Some Diseases of Hot Pepper in the Carribean Community Countries. Carribbean Agricultural Research and Development Institute. Factsheet: 1-4.
Medrano, E.G., Esquivel, J., Bell, A., Greene, J., Roberts, P., Bacheler, J., Marois, J., Wright, D., Nichols, R., Lopez, J. 2009. Potential for Nezara viridula (Hemiptera: Pentatomidae) to transmit bacterial and fungal pathogens into cotton bolls. Curr Microbiol. 59(4):405-12. doi: 10.1007/s00284-009-9452-5
Mehrwar, V., Uniyal, V.P., 2021. Insect pest diversity of standing crops and traditional pest management in agricultural areas of the Mandakini Valley, Garhwal Himalaya, Uttarakhand, India. International Journal of Horticulture, Agriculture and Food Science 5(4): 1-9. https://dx.doi.org/10.22161/ijhaf.5.4.1
Melsilawati, W., Khotimah, S., Linda, R. 2012. Fungi found in the house flies (Musca domestica L., 1758). Jurnal Protobiont 1 (1): 12-19. http://dx.doi.org/10.26418/protobiont.v1i1.593
Mondal, S., Gray, S.M. 2017. Sequential acquisition of Potato virus Y strains by Myzus persicae favors the transmission of the emerging recombinant strains. Virus Res 241:116-124. doi: 10.1016/j.virusres.2017.06.023
Montong, V., Salaki, C. 2020. Insects as carriers of Ralstonia solanacearum phylotype IV on Kepok Banana Flowers in South Minahasa and Minahasa Districts. International Journal of ChemTech Research 13(1): 199-205. http://dx.doi.org/10.20902/IJCTR.2019.130124
Morris, B. E., Henneberger, R., Huber, H., Moissl-Eichinger, C. 2013. Microbial syntrophy: Interaction for the common good. FEMS Microbiol Rev 37: 384–406. doi: 10.1111/1574-6976.12019
Musser, R.O., Hum-Musser, S.M., Felton, G.W., Gergerich, R.C. 2003. Increased larval growth and preference for virus-infected leaves by the Mexican Bean Beetle, Epilachna varivestis Mulsant, a plant virus vector. Journal of Insect Behavior 16, 247–256 (2003). https://doi.org/10.1023/A:1023919902976
Nakane, T. 1980. The Insect of Japan: Coleoptera. Hoikusha Publishing Cp., LTD. Japan.
Noman, A., Aqeel, M., Qasim, M., Haider, I., & Lou, Y. 2019. Plant-insect-microbe interaction: A love triangle between enemies in ecosystem. Science of The Total Environment, 134181. doi:10.1016/j.scitotenv.2019.1341
Ortis-Urquiza, A., Keyhani, N.O. 2013. Action on the surface: entomopathogenic fungi versus the insect cuticle. Insects 4:357-374. doi:10.3390/insects4030357
Portilla, M., Zhang, M., Glover, J.P., Reddy, G.V.P., Johnson, C. 2022. Lethal concentration and sporulation by contact and direct spray of the entomopathogenic fungus Beauveria bassiana on different stages of Nezara viridula (Heteroptera: Pentatomidae). Journal of Fungi. 8 (11): 1164. https://doi.org/10.3390/jof8111164
Rangkuti, E.E., Wiyono, S., Widodo. 2017. Identification of Colletotrichum spp. originated from papaya plant. Jurnal Fitopatologi Indonesia. 13(5): 175-183. doi: 10.14692/jfi.13.5.175
Ray, S., Gaffor, I., Acevedo, F.E., Helms, A., Chuang, W.P., Tooker, J., Felton, G.W., Luthe, D.S. 2015. Maize plants recognize herbivore-associated cues from caterpillar frass. J Chem Ecol 41: 781–792. doi: 10.1007/s10886-015-0619-1
Roux, J., Heath, R. N., Labuschagne, L., Nkuekam, G. K., Wingfield, M. J. 2007. Occurrence of the wattle wilt pathogen, Ceratocystis albifundus on native South African trees. Forest Pathology, 37(5): 292–302. doi:10.1111/j.1439-0329.2007.00507.x
Sakagami, S. F. 1978. Tetragonula Stingless Bees of the Continental Asia and Sri Lanka (Hymenoptera, Apidae). J. Fac. Sci. Hokkaido Univ.(Zool). 21: 165-247.
Sales, M.S.N, da Costa, G.L., Bittencourt, V.R. E. P. 2002. Isolation of Fungi in Musca domestica Linnaeus. 1758 (Diptera: Muscidae) captured at two natural breeding grounds in the municipality of Serop dica, Rio de Janeiro, Brazil. Mem Inst Oswaldo Cruz 97 (8): 1107-1110. doi: 10.1590/s0074-02762002000800007
Sanjaya, Y., Suhara, Nurjhani, M. 2018. Identification normal external and internal bacteria and fungi in larvae and pupae Papilio polyetes. IOP Conf. Series: Journal of Physics 1013:012172. doi :10.1088/1742-6596/1013/1/012172
Sarker, S., Howlader, A.J., Rain, F.F., Md. Aslam, A.F. 2019. Predatory performance of Coccinella transversalis and its molecular identification. Bangladesh J. Zool. 47(2): 229-241. https://doi.org/10.3329/bjz.v47i2.44334
Sarwar, M. 2020. Insects as transport devices of plant viruses. In Applied Plant Virology: Advances, Detection, and Antiviral Strategies (Ed. L.P Awasthi). Academic Press, Elsevier: London UK. pg 381-402. doi: 10.1016/B978-0-12-818654-1.00027-X
Schmelz, E.A. 2015. Impacts of insect oral secretions on defoliation-induced plant defense. Curr Opin Insect Sci 9: 7–15. doi: 10.1016/j.cois.2015.04.002
Seif, A.A., Nyambo, B. 2013. Fusarium Wilt of Pepper. General Information and Agronomic Aspects. Information on Diseases. http://www.infonet-biovision.org/default/ct/ 119/crops. Diakses tanggal 3 Oktober 2013.
Semangun, H. 2001. Pengantar Ilmu Penyakit Tumbuhan. Gadjah Mada University Press. Yogyakarta.
Shapiro, L., De Moraes, C.M., Stephenson, A.G., Mescher, M.C., 2012. Pathogen effects on
vegetative and floral odours mediate vector attraction and host exposure in a complex pathosystem. Ecol. Lett. 15, 1430–1438. https://doi.org/10.1111/ele.12001
Sikora, E.J. 2004. Fusarium and Verticillium Wilt. Plant Disease Notes. Extension. Alabama A and M Auburn Universities. ANR-861:1-2.
Smith, C.M., Gedling, C.R., Wiebe, K.F., Cassone, B.J. 2017. A Sweet Story: Bean pod mottle virus transmission dynamics by Mexican Bean Beetles (Epilachna varivestis). Genome Biology and Evolution 9 (3): 714–725, https://doi.org/10.1093/gbe/evx033
Sobianti, S., Soesanto, L., & Hadi, S. 2020. Inventory of Seed Transmitted Fungus Pathogens in Five Rice Varieties. Agro Bali: Agricultural Journal. 3(1): 1-15. DOI: 10.37637/ab.v3i1.416
Srivastava, R, Mehta, C.M, Sharma, A.K. 2011. Fusarium pallidoroseum – A new biofertilizer responsible for enhancing plant growth in different crops. International Research Journal of Microbiology 2(6): 192-199.
Stanghellini, M. E., Kim, D. H., Rasmussen, S. L., & Rorabaugh, P. A. 1996. Control of root rot of peppers caused by Phytophthora capsici with a nonionic surfactant. Plant disease, 80 (10): 1113-1116. https://doi.org/10.1094/PD-80-1113
Subiastuti, A.S., Hartono, S., Daryono, B.S. 2019. Detection and identification of Begomovirus infecting Cucurbitaceae and Solanaceae in Yogyakarta, Indonesia. Biodiversitas Journal of Biological Diversity 20 (3): 738-744. doi: 10.13057/biodiv/d200318
Sujadmiko, H. 2015. Effect of soil moisture on infection rate of Phytium sp and Rhizoctonia sp cause of blast disease in oil palm pre-nursery Nurseries (Elaeis Guineensis Jacq). Agrium: Jurnal Ilmu Pertanian 17(2): 95-102. http://dx.doi.org/10.30596%2Fagrium.v17i2.278
Wielkopolan, B., Jakubowska, M., Obrepalska-Steplowska, A. 2021. Beetles as plant pathogen vectors. Frontiers in Plant Science 12:748093. doi: 10.3389/fpls.2021.748093
Wongpia, A., Lomthaisong, K. 2010. Change in the 2DE protein profiles of chilli pepper (Capsicum annuum) leaves in response to Fusarium oxysporum infection. Science Asia 36: 259-270. doi: 10.2306/scienceasia1513-1874.2010.36.259
Yang, D., Zhao, H., Shi, J., Xu, X., Wu, Y., Guo, R., Chen, D., Wang, X., Deng, S., Yang, S., Diao, Q., Hou, C. 2019. Discovery of aphid lethal paralysis virus in Vespa velutina and Apis cerana in China. Insects. 10(6):157. doi: 10.3390/insects10060157
Yun, J-H., Roh, S, W., Whon, T.W., Jung, M-J., Kim, M.S., Park, D-S., Yoon, C., Nam, Y-D., Kim, Y-J., Choi, J-H., Kim, J-Y., Shin, N-R., Kim, S-H., Lee, W-J., Bae, J-W. 2014. Insect gut bacterial diversity determined by environmental habitat, diet, developmental stage, and phylogeny of host. Applied and Environmental Microbiology 80 (17): 5254-5264. doi:10.1128/AEM.01226-14
Yuning, L., Luyangm L., Xueming, C., Xianmei, Y., Jintian, L., Benshui, S. 2022. The bacterial and fungal communities of the larval midgut of Spodoptera frugiperda (Lepidoptera: Noctuidae) varied by feeding on two cruciferous vegetables. Nature Scientific Reports 12: 13063. https://doi.org/10.1038/s41598-022-17278-w
Zhang, Z., Jiao, S., Li, X., Li, M. 2018. Bacterial and fungal gut communities of Agrilus mali at different developmental stages and fed different diets. Nature Scientific Reports 8: 15634. doi: :10.1038/s41598-018-34127-x

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