An Outbreak of Aspergillus Species in Response to Environmental Conditions in Serbia
Abstract
The frequency and incidence of A. flavus and A. niger on barley, maize, soybean, sunflower and wheat grain, the abundance of European corn borer (Ostrinia nubilalis) moths and their interaction depending on weather conditions in the 2008-2012 period were studied. Under the agroecological conditions of Serbia, the species A. niger is more frequent than A. flavus, and concerning the crop species, its frequency is highest in kernels of sunflower, than soybean, maize, barley and wheat. A. flavus was extremely dominant on all plant species in 2012 regarding its frequency: 100% on soybean, 95.3% on maize, 65.0% on barley, 57.1% on sunflower and 45.8% on wheat. Furthermore, the incidence of A. flavus was higher in 2012 than in previous years. The uncommonly high frequency and incidence of A. flavus infestation of maize grain in 2012 were caused by extremely stressful agrometeorological conditions, high temperatures and drought over the period from flowering to waxy maturity of maize. The precipitation factor (Pf = precipitation sum / average monthly temperature) showed that 2012 was extremely arid in June (Pf = 0.57), July (Pf = 1.45), August (Pf = 0.15) and September (Pf = 1.42). European corn borer (ECB) was a second factor causing intensive occurrence of A. flavus on maize grain in 2012. The maximum flight of ECB moths was recorded as early as in July (5,149) and, as a result of this, high damage and numerous injuries were detected at harvest. Those injuries were covered by visible olive-green powdery colonies typical of A. flavus. In the chronology of A. flavus occurrence, these are the first data on its very high frequency and incidence under the agroecological conditions of Serbia. As intensive infections with A. flavus were rare in the past 50 years, the level of aflatoxins in maize grain was low.
References
--
Abbas, H.K., Cartwright, R.D., Xie, W., & Shier, T.W. (2006). Aflatoxin and fumonisin contamination of corn (maize, Zea mays) hybrids in Arkansas. Crop Protection, 25(1), 1-9.
Abbas, H.K., Wilkinson, J.R., Zablotowicz, R.M., Accinelli, C., Abel, C.A., Bruns, H.A., & Weaver, M.A. (2009). Ecology of Aspergillus flavus, regulation of aflatoxin production, and management strategies to reduce aflatoxin contamination of corn. Toxin Reviews, 28(2-3), 142-153.
Accinelli, C., Abbas, H.K., Zablotowicz, R.M., & Wilkinson, J.R. (2008). Aspergillus flavus aflatoxin occurrence and expression of aflatoxin biosynthesis genes in soil. Canadian Journal of Microbiology, 54(5), 371-379.
Adamović, M., Bočarov-Stančić, A., Pantić, V., Vukić-Vranješ, M., Jovanović, R., & Panić, M. (2011). Effect of pelleting agent on microbiological and mycotoxicological safety of feed mixtures. Biotechnology in Animal Husbandry, 2(3), 1209-1217. doi:10.2298/BAH1103209A
Bača, F., Gošić-Dondo, S., Kaitović, Ž., & Hadzistevic, D. (2007). European corn borer (Ostrinia nubilalis Hbn) population fluctuation at Zemun Polje between 1986 and 2005. Maydica, 52(3), 325-328.
Bagi, F.F., Bodroža-Solarov, M.I., Balaž, F.F., Mastilović, J.S., Stojšin, V., Budakov, D.B., & Lazić, S.D. (2011). The effect of fungicide treatment on mycotoxin content and yield parameters of wheat. Zbornik Matice srpske za prirodne nauke, 120, 121-128. doi:10.2298/ZMSPN1120121B
Bayman, P., Baker, J.L., & Mahoney, N.E. (2002). Aspergillus on tree nuts: incidence and associations. Mycopathologia / Mycopathologia, 155(3), 161-9. pmid:12617503
Bočarov-Stančić, A.S., Salma, N.M., Pantić, V.R., Adamović, M.J., Miljković, A.D., & Suzić, S.V. (2011). Microbiological and mycotoxicological correctness of protein feed ingredients in Vojvodina. Zbornik Matice srpske za prirodne nauke, 120, 213-220. doi:10.2298/ZMSPN1120213B
Bruns, A.H. (2003). Controlling Aflatoxin and Fumonisin in Maize by Crop Management. Journal of Toxicology, Toxin Reviews, 22(2-3), 153-173.
Burgess, L.W., Summerell, B.A., Bullock, S., Gott, K.P., & Backhouse, D. (1994). Laboratory Manual for Fusarium Research. Sydney: University of Sydney; Sydney: Royal Botanic Gardens - Department of Crop Sciences - Fusarium Research Laboratory.
Chandelier, A., Michelt, J.Z., Tangni, E.K., Baert, K., Moons, E., & Vinkx, C. (2004). Mycotoxins survey in Belgium and toxic Fusarium in belgian wheat. In A. Logrieco & A. Visconti (Eds.), An overview on toxigenic fungi and mycotoxins in Europe. (pp. 11-32). Dordrecht, Boston, London: Kluwer Academic Publishers.
Curtui, V., Seidler, C., Schneider, E., & Usleber, E. (2004). Mycotoxins in food in Germany. In A. Logrieco & A. Visconti (Eds.), An overview on toxigenic fungi and mycotoxins in Europe. (pp. 109-121). Dordrecht, Boston, London: Kluwer Academic Publishers.
Dimić, G., Dimić, E., Kocić-Tanackov, S., & Maletić, Ž. (2006). Mikološka ispitivanja semena tikve golice (Cucurbitapepo L) i jezgra suncokreta (Helianthus annum L) kao komponenata musli proizvoda. Uljarstvo, 37(1-2), 3-6.
Dimić, G.R., Maletić, Ž.M., & Kocić-Tanackov, S.D. (2005). Kserotolerantne mikopopulacije i mikotoksini u komponentama muslija . Zbornik Matice srpske za prirodne nauke, 109, 81-87. Retrieved from http://scindeks.ceon.rs/article.aspx?artid=0352-49 doi:10.2298/ZMSPN0519081D
Donner, M., Atehnkeng, J., Sikora, R.A., Bandyopadhyay, R., & Cotty, P.J. (2009). Distribution of Aspergillus section Flavi in soils of maize fields in three agroecological zones of Nigeria. Soil Biology & Biochemistry, 41(1), 37-44.
Gao, J., Liu, Z., & Yu, J. (2007). Identification of Aspergillus section Flavi in maize in northeastern China. Mycopathologia, 164, 91-95.
Garber, R.K., & Cotty, P.J. (1997). Formation of sclerotia and aflatoxins in developing cotton bolls infected by the S strain of Aspergillus flavus and potential for biocontrol with an atoxigenic strain. Phytopathology, 87(9), 940-945.
Gursoy, N., & Bicici, M. (2004). A review on current situation of toxigenic fungi and mycotoxins formation in Turkey. In A. Logrieco & A. Visconti (Eds.), An overview on toxigenic fungi and mycotoxins in Europe. (pp. 237-246). Dordrecht, Boston, London: Kluwer Academic Publishers.
Hajihasani, M., Hajihassani, A., & Khaghani, S. (2012). Incidence and distribution of seed-borne fungi associated with wheat in Markazi Province, Iran. African Journal of Biotechnology, 11(23), 6290-6295.
Hill, R.A., Blankenship, P.D., Cole, R.J., & Sanders, T.H. (1983). Effects of soil moisture and temperature on preharvest invasion of peanuts by the Aspergillus flavus group and subsequent aflatoxin development. Applied and environmental microbiology, 45(2), 628-33. pmid:6402980
Horn, B.W. (2003). Ecology and population biology of aflatoxigenic fungi in soil. Journal of Toxicology Toxin Reviews, 22(2-3), 351-379.
Ioannou-Kakouri, E., Aleteari, M., Christou, E., Ralli, A., Koliou, A., & Christofidou, M. (2004). Occurrence and control of mycotoxins in foodstuffs in Cyprus. In A. Logrieco & A. Visconti (Eds.), An overview on toxigenic fungi and mycotoxins in Europe. (pp. 11-32). Dordrecht, Boston, London: Kluwer Academic Publishers.
Ittu, M., Trif, A., & Belc, N. (2004). Toxigenic fungi and mycotoxins in Romania: challenges and approaches. In A. Logrieco & A. Visconti (Eds.), An overview of toxigenic fungi and mycotoxins in Europe. (pp. 185-194). Dordrecht, Boston, London: Kluwer Academic Publishers.
Jakić-Dimić, D., Nešić, K., & Petrović, M. (2009). Contamination of cereals with aflatoxins, metabolites of fungi Aspergillus flavus. Biotechnology in Animal Husbandry, 25(5-6), 1203-1208. Retrieved from http://scindeks.ceon.rs/article.aspx?artid=1450-91
Jaime-Garcia, R., & Cotty, P.J. (2006). Spatial distribution of Aspergillus flavus and its toxigenic strains on commercial cottonseed from south Texas and its relationship to aflatoxin contamination. Plant Pathology, 55, 358-366.
Jaime-Garcia, R., & Cotty, P.J. (2010). Crop rotation and soil temperature influence the community structure of Aspergillus flavus in soil. Soil Biology and Biochemistry, 42, 1842-1847.
Jaime-Garcia, R., & Cotty, P.J. (2004). Aspergillus flavus in soils and corncobs in South Texas: Implications for management of aflatoxins in corn-cotton rotations. Plant Disease, 88, 1366-1371.
Jaime-García, R., Tucson, A.Z., & Cotty, P.J. (2006). Crop rotation influences aflatoxin producing potential of Aspergillus communities in South Texas. In: Beltwide Cotton Conferences, San Antonio, Texas.
Jones, R.K., Duncan, H.E., & Hamilton, P.B. (1981). Planting date, harvest date, and irrigation effects on infection and aflatoxin production by Aspergillus flavus in field corn. Phytopathology, 71(8), 810-16.
Klich, M.A. (2007). Environmental and developmental factors influencing aflatoxin production by Aspergillus flavus and Aspergillus parasiticus. Mycoscience, 48(2), 71-80.
Kordić, B., Panin, M.K., Kandić, S., Lončarević, A., & Muntañola-Cvetković, M. (1986). Results of a three year microbiological and mycotoxicological examination of feeds in SR of Serbia. In ANU BiH, Special Publications, Department of Medical Sciences. (pp. 17-28).
Krnjaja, V.S., Lević, J.T., Stanković, S.Ž., Petrović, T.S., & Lukić, M.D. (2013). Molds and mycotoxins in freshly harvested maize. Zbornik Matice srpske za prirodne nauke, 124, 111-119. doi:10.2298/ZMSPN1324111K
Krnjaja, V., Lević, J., Tomić, Z., Stojanović, L., Trenkovski, S., Nešić, Z., & Marinkov, G. (2007). Prisustvo potencijalno toksigenih gljiva u hrani za životinje sa posebnim osvrtom na vrste rodova Aspergillus i Fusarium. Biotechnology in Animal Husbandry, 23(1-2), 95-103. Retrieved from http://scindeks.ceon.rs/article.aspx?artid=1450-91 doi:10.2298/BAH0702095K
Lević, J. (1987). Inheritance of maize leaf resistance to Kabatiella zeae Narita et Hiratsuka and screening for source of resistance (Summary in English). Arhiv za poljoprivredne nauke, 48(170), 173-203.
Lević, J., Ivanović, D., Stanković, H.M., Penčić, V., & Stojkov, S. (1991). Zastupljenost i frekvencija mikopopulacija na hibridnom semenu kukuruza u periodu 1987 1990. In: IX-ti naučni simpozijum iz semenarstva na temu: Ekonomski problemi i efekti semenerstva u Jugoslaviji. Skupština i IX simpozijum semenarstva Jugoslavije, Kopaonik. 51-52.
Lević, J., Ivanović, D., & Stanković, S. (2003). Paraziti kukuruza, sirka i prosa koji se prenose semenom. Biljni lekar, 31(6), 570-577.
Lević, J., Penčić, V., Ivanović, D., & Bočarov-Stančić, A.S. (1993). Maize ear and associated fungi in field and crib environment. Arhiv bioloških nauka, 45(1-2), 37-44.
Lević, J.T., Stanković, S.Ž., Bočarov-Stančić, A.S., Škrinjar, M.M., & Mašić, Z. (2004). The overview of toxigenic fungi and mycotoxins in Serbia and Montenegro. In A. Logrieco & A. Visconti (Eds.), An overview of toxigenic fungi and mycotoxins in Europe. (pp. 201-218). Dordrecht, Boston, London: Kluwer Academic Publishers.
Lević, J., Stanković, S., Krnjaja, V., Bočarov-Stančić, A., & Ivanović, D. (2012). Pojava i učestalost patogena semena žita i industrijskih biljaka u Srbiji . Pesticidi i fitomedicina, 27(1), 33-40. Retrieved from http://scindeks.ceon.rs/article.aspx?artid=1820-39 doi:10.2298/PIF1201033L
Levitin, M. (2004). Toxigenic fungi and mycotoxins in cereals grain and food in Russia. In A. Logrieco & A. Visconti (Eds.), An Overview on toxigenic fungi and mycotoxins in Europe. (pp. 195-199). Kluwer Academic Publishers.
Lillehoj, E.B., Fennell, D.I., & Kwolek, W.F. (1976). Aspergilus flavus and aflatoxin in Iowa corn before harvest. Science, 193(4252), 495-6. pmid:821144
Lončarević, A., Antonijević, M., Penčić, V., Smiljaković, H., & Dujin, T. (1970). Procentualna zastupljenost različitih vrsta gljivica u koncentrovanim smesama za ishranu svinja. In: ZB. 2. Skup svinjogojaca. Novi Sad: Poljoprivredni fakultet.1-4.
Marín, S., Ramos, A.J., Cano-Sancho, G., & Sanchis, V. (2012). Reduction of mycotoxins and toxigenic fungi in the Mediterranean basin maize chain. Phytopathologia Mediterranea, 51(1), 93-118.
Mateo, R., Medina, Á., Gimeno-Adelantado, J.V., & Jiménez, M. (2004). An overview on the status of toxigenic fungi and maycotoxins in Spain. In A. Logrieco & A. Visconti (Eds.), An overview of toxigenic fungi and mycotoxins in Europe. (pp. 219-235). Dordrecht, Boston, London: Kluwer Academic Publishers.
Matsh, S.F., & Payne, G.A. (1984). Preharvest infection of corn silk and kernels by Aspergilllus flavus. Phytopathology, 74, 1284-1289.
McMillian, W.W., Wilson, D.M., & Widstrom, N.W. (1985). Aflatoxin contamination of preharvest corn in Georgia: A six-year study of insect damage and visible Aspergillus flavus. Journal of Environmental Quality, 114(2), 200-202.
Moretti, A., Logrieco, A., Visconti, A., & Bottalico, A. (2004). An overwiew of mycotoxins and toxigenic fungi in Italy. In A. Logrieco & A. Visconti (Eds.), An overview on toxigenic fungi and mycotoxins in Europe. (pp. 141-160). Dordrecht, Boston, London: Kluwer Academic Publishers.
Muthomi, J.W., Mureithi, B.K., Chemining, G.N., Gathumbi, J.K., & Mutit, E.W. (2012). Aspergillus species and Aflatoxin B1 in soil, maize grain and flour samples from semi-arid and humid regions of Kenya. International Journal of Agriculture Science, 2(1), 22-34.
Nelson, M.R., Bigelow, D.M., Orum, T.V., Howell, D.R., & Cotty, P.J. (1996). Magnitude and strain composition of Aspergillus flavus soil surface populations in Yuma County commercial fields. Retrieved from http://hdl.handle.net/10150/210925
Nirenberg, H. (1976). Untersuchungen ber die morphologische biologische Differenzierung in der Fusarium-Sektion Liseola. Mittelungen aus der Biologischen Bundesanstalt für Land - und Forstwirtschaft Berlin. In Mittelungen aus der Biologischen Bundesanstalt für Land - und Forstwirtschaft. Berlin-Dahlam.
Ostry, V., Skarkova, J., Malir, F., & Sycorova, S. (2004). Advences on the occurrence of toxigenic fungi and y mycotoxins in the Czech Republik. In A. Logrieco & A. Visconti (Eds.), An overview on toxigenic fungi and mycotoxins in Europe. (pp. 67-81). Dordrecht, Boston, London: Kluwer Academic Publishers.
Öhlinger, R., Adler, A., Kräutler, O., & Lew, H. (2004). Occurence of toxigenic fungi and related mycotoxins in cereals, feeds and foods in Austria. In A. Logrieco & A. Visconti (Eds.), An overview on toxigenic fungi and mycotoxins in Europe. (pp. 1-10). Dordrecht, Boston, London: Kluwer Academic Publishers.
Panić, M., & Marić, A. (1964). Prilog proučavanju parazita klipa kukuruza u Vojvodini. Zaštita bilja, 77, 67-80.
Peito, A., & Venâncio, A. (2004). An overview of mycotoxins and toxigenic fungi in Portugal. In A. Logrieco & A. Visconti (Eds.), An overview on toxigenic fungi and mycotoxins in Europe. (pp. 173-184). Dordrecht, Boston, London: Kluwer Academic Publishers.
Pepeljnjak, S., & Šegvić, M. (2004). An overview of mycotoxins and toxigenic fungi in Croatia. In A. Logrieco & A. Visconti (Eds.), An overview on toxigenic fungi and mycotoxins in Europe. (pp. 11-32). Dordrecht, Boston, London: Kluwer Academic Publishers.
Perkowski, J., Chełkowski, J., & Goliński, P. (2004). Occurrence of mycotoxins in cereals, plants, foods and feeds in Poland. In A. Logrieco & A. Visconti (Eds.), An overview on toxigenic fungi and mycotoxins in Europe. (pp. 161-172). Dordrecht, Boston, London: Kluwer Academic Publishers.
Polovinski-Horvatović, M.S., Jurić, V.B., & Glamočić, D. (2009). The Frequency of occurrence of Aflatoxin M1 in milk on the territory of Vojvodina. Zbornik Matice srpske za prirodne nauke, 116, 75-80. doi:10.2298/ZMSPN0916075P
Probst, C., Njapau, H., & Cotty, P.J. (2007). Outbreak of an acute aflatoxicosis in Kenya in 2004: identification of the causal agent. Applied and environmental microbiology, 73(8), 2762-4. pmid:17308181
Razzaghi-Abyaneh, M., Shams-Ghahfarokhi, M., Allameh, A., Kazeroon-Shiri, A., Ranjbar-Bahadori, S., Mirzahoseini, H., & Mohammad-Bagher, R. (2006). A survey on distribution of Aspergillus section Flavi in corn field soils in Iran: Population patterns based on aflatoxins, cyclopiazonic acid and sclerotia production. Mycopathologia, 161, 183-192.
Scudamore, K.A. (2004). Occurrence of mycotoxins in UK food commodities. In A. Logrieco & A. Visconti (Eds.), An overview on toxigenic fungi and mycotoxins in Europe. (pp. 247-252). Dordrecht, Boston, London: Kluwer Academic Publishers.
Stack, J., & Carlson, M. (2003). NF571 Aspergillus flavus and Aflatoxins in Corn. In Historical Materials from University of Nebraska-Lincoln Extension. Paper. University of Nebraska, Lincoln Extension. Retrieved from http://digitalcommons.unl.edu/extensionhist/43
Strosnider, H., Azziz-Baumgartner, E., Banziger, M., Bhat, R.V., Breiman, R., Brune, M., . . . Jolly, C. (2006). Workgroup report: public health strategies for reducing aflatoxin exposure in developing countries. Environmental health perspectives , 114(12), 1898-903. pmid:17185282
Škrinjar, M., Bandu, M., Dimić, E., Bošnjak-Bjelobaba, K., & Romanić, R. (2007). Infekcija semena suncokreta žetve 2006. aflatoksigenim gljivama. Uljarstvo, 38(1-2), 41-47. Retrieved from http://scindeks.ceon.rs/article.aspx?artid=0351-95
Škrinjar, M., Jakić-Dimić, D., Šošo, V., Blagojev, N., Vesković-Moračanin, S., & Gerić, T. (2011). Rezultati mikoloških i mikotoksikoloških ispitivanja hraniva na bazi kukuruza namenjenih za ishranu krava muzara. Veterinarski glasnik, 65(5-6), 333-348. doi:10.2298/VETGL110633
Škrinjar, M., Vujičić, I., Stubblefield, R., Jurić, V., Stojanović, E., & Mašić, Z. (1989). The presence of aflatoxin B1 in forage in Vojvodina. In ANU B&H, Special Publications, LXXXIX, Department of Medical Sciences, 14, Sarajevo. (pp. 119-129).
Šutić, M., Svilar, N., Ivanović, D., Tosman, N., & Oljačić, E. (1989). Moulds and mycotoxins in cattle feed. In ANU B&H, Special Publications. (pp. 109-118). Sarajevo: Department of Medical Sciences.
Varga, J., Tóth, B., Mesterházy, Á., Téren, J., & Fazekas, B. (2004). Mycotoxigenic fungi and mycotoxins in foods and feeds in Hungary. In A. Logrieco & A. Visconti (Eds.), An overview on toxigenic fungi and mycotoxins in Europe. (pp. 123-139). Dordrecht, Boston, London: Kluwer Academic Publishers.
Yin, Y., Yan, L., Jiang, J., & Ma, Z. (2008). Biological control of aflatoxin contamination of crops. Journal of Zhejiang University. Science. B, 9(10), 787-92. pmid:18837105
Windham, G.L., Williams, W.P., & Davis, F.M. (1999). Effects of the Southwestern Corn Borer on Aspergillus flavus Kernel Infection and Aflatoxin Accumulation in Maize Hybrids. Plant Disease, 83(6), 535-40. doi:10.1094/PDIS.1999.83.6.535
Singh, K., Frisvad, J.C., & Thrane, U. (1991). An Illustrated Manual on Identification of Some Seed-Borne Aspergilli, Fusaria, Penicillia and Their Mycotoins. Denmark: Danish Government Institute of Seed Pathology for Developing Countries.
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