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Da-wei Liu


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Journal of Zhejiang University SCIENCE B 2016 Vol.17 No.2 P.158-168


Potential natural exposure of endangered red-crowned crane (Grus japonensis) to mycotoxins aflatoxin B1, deoxynivalenol, zearalenone, T-2 toxin, and ochratoxin A

Author(s):  Da-wei Liu, Hong-yi Liu, Hai-bin Zhang, Ming-chang Cao, Yong Sun, Wen-da Wu, Chang-hu Lu

Affiliation(s):  Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing 210037, China; more

Corresponding email(s):   wuwenda@njau.edu.cn, luchanghu@njfu.com.cn

Key Words:  Food, Mycotoxin, Red-crowned crane, Yancheng Biosphere Reserve

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Da-wei Liu, Hong-yi Liu, Hai-bin Zhang, Ming-chang Cao, Yong Sun, Wen-da Wu, Chang-hu Lu. Potential natural exposure of endangered red-crowned crane (Grus japonensis) to mycotoxins aflatoxin B1, deoxynivalenol, zearalenone, T-2 toxin, and ochratoxin A[J]. Journal of Zhejiang University Science B, 2016, 17(2): 158-168.

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author="Da-wei Liu, Hong-yi Liu, Hai-bin Zhang, Ming-chang Cao, Yong Sun, Wen-da Wu, Chang-hu Lu",
journal="Journal of Zhejiang University Science B",
publisher="Zhejiang University Press & Springer",

%0 Journal Article
%T Potential natural exposure of endangered red-crowned crane (Grus japonensis) to mycotoxins aflatoxin B1, deoxynivalenol, zearalenone, T-2 toxin, and ochratoxin A
%A Da-wei Liu
%A Hong-yi Liu
%A Hai-bin Zhang
%A Ming-chang Cao
%A Yong Sun
%A Wen-da Wu
%A Chang-hu Lu
%J Journal of Zhejiang University SCIENCE B
%V 17
%N 2
%P 158-168
%@ 1673-1581
%D 2016
%I Zhejiang University Press & Springer
%DOI 10.1631/jzus.B1500211

T1 - Potential natural exposure of endangered red-crowned crane (Grus japonensis) to mycotoxins aflatoxin B1, deoxynivalenol, zearalenone, T-2 toxin, and ochratoxin A
A1 - Da-wei Liu
A1 - Hong-yi Liu
A1 - Hai-bin Zhang
A1 - Ming-chang Cao
A1 - Yong Sun
A1 - Wen-da Wu
A1 - Chang-hu Lu
J0 - Journal of Zhejiang University Science B
VL - 17
IS - 2
SP - 158
EP - 168
%@ 1673-1581
Y1 - 2016
PB - Zhejiang University Press & Springer
ER -
DOI - 10.1631/jzus.B1500211

A survey was conducted to determine whether mycotoxins were present in the foods consumed by red-crowned cranes (Grus japonensis) in the yancheng Biosphere Reserve, China. Collected in the reserve’s core, buffer, and experimental zones during overwintering periods of 2013 to 2015, a total of 113 food samples were analyzed for aflatoxin B1, deoxynivalenol, zearalenone, T-2 toxin, and ochratoxin A using high performance liquid chromatography (HPLC). The contamination incidences vary among different zones and the mycotoxins levels of different food samples also presented disparity. Average mycotoxin concentration from rice grain was greater than that from other food types. Among mycotoxin-positive samples, 59.3% were simultaneously contaminated with more than one toxin. This study demonstrated for the first time that red-crowned cranes were exposed to mycotoxins in the yancheng Biosphere Reserve and suggested that artificial wetlands could not be considered good habitats for the birds in this reserve, especially rice fields.




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[1]Bansal, J., Pantazopoulos, P., Tam, J., et al., 2011. Surveys of rice sold in Canada for aflatoxins, ochratoxin A and fumonisins. Food Addit. Contam. Part A, 28(6):767-774.

[2]Bellio, M.G., Kingsford, R.T., Kotagama, S.W., 2009. Natural versus artificial-wetlands and their waterbirds in Sri Lanka. Biol. Conserv., 142(12):3076-3085.

[3]Binder, E.M., Tan, L.M., Chin, L.J., et al., 2007. Worldwide occurrence of mycotoxins in commodities, feeds and feed ingredients. Anim. Feed Sci. Technol., 137(3-4):265-282.

[4]BirdLife International, 2015. Species factsheet: Grus japonensis. Available from http://www.birdlife.org [Accessed on Mar. 15, 2015]

[5]Bouaziz, C., Bouslimi, A., Kadri, R., et al., 2013. The in vitro effects of zearalenone and T-2 toxins on Vero cells. Exp. Toxicol. Pathol., 65(5):497-501.

[6]Carnaghan, R.B., 1965. Hepatic tumors in ducks fed a low level of toxin groundnut meal. Nature, 208(5006):208.

[7]Chen, F., Ma, Y.L., Xue, C.Y., et al., 2008. The combination of deoxynivalenol and zearalenone at permitted feed concentrations causes serious physiological effects in young pigs. J. Vet. Sci., 9(1):39-44.

[8]Chi, M.S., Robison, T.S., Mirocha, C.J., et al., 1978. Acute toxicity of 12,13-epoxytrichothecenes in one-day-old broiler chicks. Appl. Environ. Microbiol., 35(4):636-640.

[9]Chi, M.S., Mirocha, G.J., Weaver, G.A., et al., 1980. Effect of zearalenone on female white leghorn chickens. Appl. Environ. Microbiol., 39:1026-1030.

[10]Choudhury, H., Carlson, C.W., Semeniuk, G., 1971. A study of ochratoxin toxicity in hens. Poult. Sci., 50(6):1855-1859.

[11]Dias, R.A., Blanco, D.E., Goijman, A.P., et al., 2014. Density, habitat use, and opportunities for conservation of shorebirds in rice fields in southeastern South America. Condor, 116(3):384-393.

[12]D'Mello, J.P.F., Macdonald, A.M.C., Postel, D., et al., 1998. Pesticide use and mycotoxin production in Fusarium and Aspergillus phytopathogens. Eur. J. Plant. Pathol., 104(8):741-751.

[13]Dong, K., Lv, S.C., Healy, T., 2005. Carrying capacity of red-crowned cranes in the national Yancheng rare birds nature reserve, Jiangsu Province, China. Acta Ecol. Sin., 25(10):2608-2615 (in Chinese).

[14]Fan, Y., 2008. Toxic effect of aflatoxin B1 and deoxynivalenol to cyprinus carpio and cultured hepatocytes in vitro. PhD Thesis, Nanjing Agricultural University, Nanjing, China (in Chinese).

[15]Fink-Gremmels, J., 1999. Mycotoxins: their implications for human and animal health. Vet. Quart., 21(4):115-120.

[16]Georgiadou, M., Dimou, A., Yanniotis, S., 2012. Aflatoxin contamination in pistachio nuts: a farm to storage study. Food Control, 26(2):580-586.

[17]Gu, D., Fu, J., Yan, W., et al., 2012. Evaluation of coastal wetlands degradation in Yancheng city and zonal diagnosis. Wetland Sci., 10:1-7 (in Chinese).

[18]Huff, W.E., Doerr, J.A., Hamilton, P.B., et al., 1981. Acute toxicities of vomitoxin (Deoxynivalenol) in broiler chickens. Poult. Sci., 60(7):1412-1414.

[19]Huff, W.E., Kubena, L.F., Harvey, R.B., et al., 1986. Individual and combined effects of aflatoxin and deoxynivalenol (DON, vomitoxin) in broiler chickens. Poul. Sci., 65(7):1291-1298.

[20]Hussein, H.S., Brasel, J.M., 2001. Toxicity, metabolism, and impact of mycotoxins on humans and animals. Toxicology, 167(2):101-134.

[21]IARC (International Agency for Research on Cancer), 1993. Some naturally occurring substances: food items and constituents, heterocyclic aromatic amines and mycotoxins. In: IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, Vol. 56. IARC Lyon, France, p.245-395.

[22]IUCN (International Union for Conservation of Nature), 2014. IUCN Red List of Threatened Species. Version 2014.3. Available from http://www.iucnredlist.org [Accessed on Mar. 15, 2015]

[23]Jouany, J.P., 2007. Methods for preventing, decontaminating and minimizing the toxicity of mycotoxins in feeds. Anim. Feed Sci. Technol., 137(3-4):342-362.

[24]Kamalavenkatesh, P., Vairamuthu, S., Balachandran, C., et al., 2005. Immunopathological effect of the mycotoxins cyclopiazonic acid and T-2 toxin on broiler chicken. Mycopathologia, 159(2):273-279.

[25]Khayoon, W.S., Saad, B., Yan, C.B., et al., 2010. Determination of aflatoxins in animal feeds by HPLC with multifunctional column clean-up. Food Chem., 118(3):882-886.

[26]Kolf-Clauw, M., Ayouni, F., Tardieu, D., et al., 2008. Variations in zearalenone activation in avian food species. Food Chem. Toxicol., 46(5):1467-1473.

[27]Krnjaja, V., Mandić, V., Lević, J., et al., 2015. Influence of N-fertilization on Fusarium head blight and mycotoxin levels in winter wheat. Crop Prot., 67:251-256.

[28]Lawson, B., MacDonald, S., Howard, T., et al., 2006. Exposure of garden birds to aflatoxins in Britain. Sci. Total Environ., 361(1-3):124-131.

[29]Lee, K.E., Kim, K.E., Lee, C., 2010. Occurrence of Fusarium mycotoxin beauvericin in animal feeds in Korea. Anim. Feed Sci. Technol., 157(3-4):190-194.

[30]Lee, S.D., Jabloński, P.G., Higuchi, H., 2007. Wintering foraging of threatened cranes in the Demilitarized Zone of Korea: behavioral evidence for the conservation importance of unplowed rice fields. Biol. Conserv., 138(1-2):286-289.

[31]Li, R., Wang, X., Zhou, T., et al., 2014. Occurrence of four mycotoxins in cereal and oil products in Yangtze Delta region of China and their food safety risks. Food Control, 35(1):117-122.

[32]Li, W.J., Wang, Z.J., Ma, Z.J., et al., 1997. A regression model for the spatial distribution of red-crowned crane in Yancheng Biosphere Reserve, China. Ecol. Model., 103(2-3):115-121.

[33]Li, Z.Q., Wang, Z., Ge, C., 2013. Time budgets of wintering red-crowned cranes: effects of habitat, age and family size. Wetlands, 33(2):227-232.

[34]Lijinsky, W., Butler, W.H., 1966. Purification and toxicity of aflatoxin G1. Exp. Biol. Med., 123(1):151-154.

[35]Liu, C.Y., Jiang, H.X., Zhang, S.Q., et al., 2013. Multi-scale analysis to uncover habitat use of red-crowned cranes: implication for conservation. Curr. Zool., 59(5):604-617.

[36]Lv, S.C., 2007. Quantitative distribution in night of red-crowned crane on the artificial wetland during wintering stage. Chin. J. Wildl., 28(2):11-13 (in Chinese).

[37]Lu, Q.X., Yang, H.Y., Wang, B., et al., 2008. Diagnosis of soilborne fungal disease in wheat. J. Triticeae Crops, 28(3):531-536 (in Chinese).

[38]Ma, Y.Q., Li, X.M., 2002. Research on the Red-Crowned Crane. Shanghai Press for Science Technology and Education, Shanghai, p.100 (in Chinese).

[39]Ma, Z.J., Wang, Z.J., Tang, H.X., 1999. Habitat and selection by Red-crowned Crane Grus japanensis in winter in Yancheng Biosphere Reserve, China. IBIS, 141(1):135-139.

[40]Ma, Z.J., Li, W.J., Wang, Z.J., 2000. Nature Conservation of Red-Crowned Cranes. Qinghua University Press, Beijing, p.41 (in Chinese).

[41]Ma, Z.J, Cai, Y.T., Li, B., et al., 2010. Managing wetland habitats for waterbirds: an international perspective. Wetlands, 30(1):15-27.

[42]Marin, S., Ramos, A.J., Cano-Sancho, G., et al., 2013. Mycotoxins: occurrence, toxicology, and exposure assessment. Food Chem. Toxicol., 60:218-237.

[43]Meissonnier, G.M., Laffitte, J., Raymond, I., et al., 2008. Subclinical doses of T-2 toxin impair acquired immune response and liver cytochrome P450 in pigs. Toxicology, 247(1):46-54.

[44]Minervini, F., Dell'Aquila, M.E., 2008. Zearalenone and reproductive function in farm animals. Int. J. Mol. Sci., 9(12):2570-2584.

[45]Nguyen, M.T., Tozlovanu, M., Tran, T.L., et al., 2007. Occurrence of aflatoxin B1, citrinin and ochratoxin A in rice in five provinces of the central region of Vietnam. Food Chem., 105(1):42-47.

[46]Nielsen, K.F., Mogensen, J.M., Johansen, M., et al., 2009. Review of secondary metabolites and mycotoxins from the Aspergillus niger group. Anal. Bioanal. Chem., 395(5):1225-1242.

[47]Oberheu, D.G., Dabbert, C.B., 2001. Aflatoxin production in supplemental feeders provided for northern bobwhite in Texas and Oklahoma. J. Wildl. Dis., 37(3):475-480.

[48]Olsen, G.H., Carpenter, J.W., Gee, G.F., et al., 1995. Mycotoxin-induced disease in captive whooping cranes (Grus americana) and sandhill cranes (Grus canadensis). J. Zoo Wildl. Med., 26:569-576.

[49]Pain, D.J., Gargi, R., Cunningham, A.A., et al., 2004. Mortality of globally threatened Sarus cranes Grus antigon from monocrotophos poisoning in India. Sci. Total Environ., 326(1-3):55-61.

[50]Parent-Massin, D., 2004. Haematotoxicity of trichothecenes. Toxicol. Lett., 153(1):75-81.

[51]Park, J.W., Choi, S.Y., Hwang, H.J., et al., 2005. Fungal mycoflora and mycotoxins in Korean polished rice destined for humans. Int. J. Food Microbiol., 103(3):305-314.

[52]Peckham, J.C., Doupnik, B.Jr., Jones, O.H.Jr., 1971. Acute toxicity of ochratoxins A and B in chicks. Appl. Microbiol., 21:492-494.

[53]Placinta, C.M., D'Mello, J.P.F., Macdonald, A.M.C., 1999. A review of worldwide contamination of cereal grains and animal feed with Fusarium mycotoxins. Anim. Feed Sci. Technol., 78(1-2):21-37.

[54]Qiu, J., Shi, J., 2014. Genetic relationship, carbendazim sensitivity and mycotoxin production of the Fusarium Graminearum populations from maize, wheat and rice in Eastern China. Toxins, 6(8):2291-2309.

[55]Rodrigues, I., Naehrer, K., 2012. A three-year survey on the worldwide occurrence of mycotoxins in feedstuffs and feed. Toxins, 4(12):663-675.

[56]Santos, L., Marin, S., Sanchis, V., et al., 2009. Screening of mycotoxin multicontamination in medicinal and aromatic herbs sampled in Spain. J. Sci. Food Agric., 89(10):1802-1807.

[57]Schrödter, R., 2004. Influence of harvest and storage conditions on trichothecenes levels in various cereals. Toxicol. Lett., 153(1):47-49.

[58]Scudamore, K.A., Hetmanski, M.T., Nawaz, S., et al., 1997. Determination of mycotoxins in pet foods sold for domestic pets and wild birds using linked-column immunoassay clean-up and HPLC. Food Addit. Contam., 14(2):175-186.

[59]Sklan, D., Shelly, M., Makovsky, B., et al., 2003. The effect of chronic feeding of diacetoxyscirpenol and T-2 toxin on performance, health, small intestinal physiology and antibody production in turkey poults. Br. Poult. Sci., 44(1):46-52.

[60]Smith, J.W., Hamilton, P.B., 1970. Aflatoxicosis in the broiler chicken. Poult Sci., 49(1):207-215.

[61]Speijers, G.J., Speijers, M.H., 2004. Combined toxic effects of mycotoxins. Toxicol. Lett., 153(1):91-98.

[62]Stafford, M.E., McLaughlin, C.S., 1973. Trichodermin, a possible inhibitor of the termination process of protein synthesis. J. Cell. Physiol., 82(1):121-128.

[63]Streit, E., Schatzmayr, G., Tassis, P., et al., 2012. Current situation of mycotoxin contamination and co-occurrence in animal feed-focus on Europe. Toxins, 4(12):788-809.

[64]Sulyok, M., Krska, R., Schuhmacher, R., 2010. Application of an LC-MS/MS based multi-mycotoxin method for the semi-quantitative determination of mycotoxins occurring in different types of food infected by moulds. Food Chem., 19(1):408-416.

[65]Swamy, H.V., Smith, T.K., MacDonald, E.J., 2004. Effects of feeding blends of grains naturally contaminated with Fusarium mycotoxins on brain regional neurochemistry of starter pigs and broiler chickens. J. Anim. Sci., 82(7):2131-2139.

[66]Torres, A.M., Barros, G.G., Palacios, S.A., et al., 2014. Review on pre- and post-harvest management of peanuts to minimize aflatoxin contamination. Food Res. Int., 62:11-19.

[67]Wang, Q.S., 2008. Threats for red-crowned crane. China Crane News, 12(2):7-12.

[68]Wang, Y., Liu, S.L., Zheng, H., et al., 2013. T-2 toxin, zearalenone and fumonisin B1 in feedstuffs from China. Food Addit. Contam. Part B, 6(2):116-122.

[69]Wang, Z., 2012. Landscape patterns in Yancheng coastal lines. PhD Thesis, Chinese Academy of Sciences, Beijing, China (in Chinese).

[70]Wang, Z., Li, Z.Q., Beauchamp, G., et al., 2011. Flock size and human disturbance affect vigilance of endangered red-crowned cranes (Grus japonensis). Biol. Conserv., 144(1):101-105.

[71]Windingstad, R.M., Cole, R.J., Nelson, P.E., et al., 1989. Fusarium mycotoxins from peanuts suspected as a cause of sandhill crane mortality. J. Wildl. Dis., 25(1):38-46.

[72]Xu, X.M., 2003. Effects of environmental conditions on the development of Fusarium ear blight. Eur. J. Plant Pathol., 109(7):683-689.

[73]Yoshizawa, T., Morooka, N., 1974. Studies on the toxic substances in infected cereals (III). Acute toxicities of new trichothecene mycotoxins: deoxynivalenol and its monoacetate. Food Hyg. Soc. Jpn., 15(4):261-269 (in Japanese).

[74]Zain, M.E., 2011. Impact of mycotoxins on humans and animals. J. Saudi Chem. Soc., 15(2):129-144.

[75]Zinedine, A., Soriano, J.M., Moltó, J.C., et al., 2007. Review on the toxicity, occurrence, metabolism, detoxification, regulations and intake of zearalenone: an oestrogenic mycotoxin. Food Chem. Toxicol., 45(1):1-18.

[76]Zuo, P., Wan, S.W., Qin, P., et al., 2004. A comparison of the sustainability of original and constructed wetlands in Yancheng Biophere Reserve, China: implication from energy evaluation. Environ. Sci. Policy, 7(4):329-343.

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