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Effluent from Citrus Industry: Toxic Parameters of Orange Vinasse

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Abstract

Brazil is one of the greatest producers of orange and its orange juice processing industry produces large volumes of solid and liquid waste daily. As an efficient use of the residues from citrus industry, production of bioethanol is highlighted. However, the generation of bioethanol produces a liquid effluent as a by-product, known as vinasse. The objective of this study was to evaluate the toxicity of an effluent from citrus industries, orange vinasse, when applied to soil using Allium cepa seeds. The evaluation was performed by means of germination, root growth, and genotoxic and mutagenic parameters. The EC50 (effectiveness concentration) and ½ EC50, defined in the germination test, were used for genotoxicity tests. Toxicity was observed in dilutions above 40%, which was responsible for reducing the germination speed index. Genotoxicity was observed only using the EC50 and mutagenicity was not detected. According to the results, orange vinasse showed toxicity similar to the sugar cane vinasse, so caution is suggested in the disposal of this effluent into the environment.

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References

  • Albertini, R. J., Anderson, D., Douglas, G. R., et al. (2000). IPCS guidelines for the monitoring of genotoxic effects of carcinogens in humans. Mutation Research, Reviews in Mutation Research, 463(2), 111–172.

    Article  CAS  Google Scholar 

  • Alloway, B. J. (1995). Heavy metals in soils (2nd ed.). Glasgow: Blackie Academic & Professional.

    Book  Google Scholar 

  • Alves, P. R. L., Natal-da-Luz, T., Sousa, J. P., & Cardoso, E. J. (2015). Ecotoxicological characterization of sugarcane vinasses when applied to tropical soils. The Science of the Total Environment, 526, 222–232.

    Article  CAS  Google Scholar 

  • Araújo-Neto S. E., de Ramos J. D., & Mendonça V. (2002). Desenvolvimento de mudas de maracujazeiro-amarelo em diferentes substratos e recipientes. In: Congresso Brasileiro de Fruticultura. Belém, PA. Brazil (in Portuguese).

  • Awan, A. T., Tsukamoto, J., & Tasic, L. (2013). Orange waste as a biomass for 2G-ethanol production using low cost enzymes and co-culture fermentation. RSC Advances, 3, 25071–25078.

    Article  CAS  Google Scholar 

  • Barros, J. R. M., Barros, A. L. M., & Cypriano, M. P. (2016). O mercado citricultural no Brasil e as suas novas perspectivas. Available on: http://www.citrusbr.com/download/biblioteca/CitrusBR_Livro_Concecitrus_2016.pdf. Accessed on July 23rd, 2019.

  • Becaro, A. A., Siqueira, M. C., Puti, F. C., de Moura, M. R., Correa, D. S., Marconcini, J. M., & Ferreira, M. D. (2017). Cytotoxic and genotoxic effects of silver nanoparticle/carboxymethyl cellulose on Allium cepa. Environmental Monitoring and Assessment, 189(7), 352.

    Article  Google Scholar 

  • Borboa, L., & Torre, C. (1996). The genotoxicity of Zn (II) and Cd (II) in Allium cepa root meristematic cells. The New Phytologist, 134(3), 481–486.

    Article  CAS  Google Scholar 

  • Brusick, D. (1986). Genotoxic effects in cultured mammalian cells produced by low pH treatment conditions and increased ion concentrations. Environmental and Molecular Mutagenesis, 8(6), 879–886.

    Article  CAS  Google Scholar 

  • CETESB - Companhia de Tecnologia de Saneamento Ambiental. (2009). Qualidade das águas interiores no estado de São Paulo. Available on: http://cetesb.sp.gov.br/aguas-interiores/wp-content/uploads/sites/32/2013/11/variaveis.pdf. Accessed 27 June.

  • CETESB - Companhia de Tecnologia de Saneamento Ambiental. (2014). Decisão de Diretoria nº 045/2014/E/C/I. Available from: https://sites.usp.br/sef/wp-content/uploads/sites/52/2015/03/47-CETESB2014_Valores_Orientadores_solo_agua.pdf. Accessed 10 Aug 2018.

  • Chojnacka, K., Chojnacki, A., Górecka, H., & Górecki, H. (2005). Bioavailability of heavy metals from polluted soils to plants. The Science of the Total Environment, 337(1), 175–182.

    Article  CAS  Google Scholar 

  • Christofoletti, C. A., Pedro-Escher, J., Correia, J. E., Marinho, J. F. U., & Fontanetti, C. S. (2013a). Sugarcane vinasse: environmental implications of its use. Waste Management, 33(12), 2752–2761.

    Article  CAS  Google Scholar 

  • Christofoletti, C. A., Pedro-Escher, J., & Fontanetti, C. S. (2013b). Assessment of the genotoxicity of two agricultural residues after processing by diplopods using the Allium cepa assay. Water, Air, & Soil Pollution, 224(4), 1–14.

    Article  CAS  Google Scholar 

  • Christofoletti, C. A., Francisco, A., Pedro-Escher, J., Gastaldi, V. D., & Fontanetti, C. S. (2016). Diplopods as soil bioindicators of toxicity after application of residues from sewage treatment plants and ethanol industry. Microscopy and Microanalysis, 22, 1098–1110.

    Article  CAS  Google Scholar 

  • Citrosuco. (2016a). Relatório de Sustentabilidade Safra 2015–2016. Available on: http://www.citrosuco.com.br/sustentabilidade/relatorio-de-sustentabilidade.html. Acessed on March 4th, 2018.

  • Citrosuco. (2016b). Subprodutos da indústria cítrica. Available on: http://www.citrosuco.com.br/pt/produtos.php#subprodutos. Accessed on February 10th, 2017.

  • Coelho, M. P. M., Moreira-de-Sousa, C., Souza, R. B., Ansoar-Rodríguez, Y., Silva-Zacarin, E. C., & Fontanetti, C. S. (2017). Toxicity evaluation of vinasse and biosolid samples in diplopod midgut: heat shock protein in situ localization. Environemental Science and Pollution Research, 24(27), 22007–22017.

    Article  CAS  Google Scholar 

  • CONAMA – Conselho Nacional de Meio Ambiente. (2011). Resolução n. 430. Available on: http://www2.mma.gov.br/port/conama/legiabre.cfm?codlegi=646. Accessed on July 23th, 2019.

  • Correia, J. E., Christofoletti, C. A., Marcato, A. C. C., Marinho, J. F. U., & Fontanetti, C. S. (2017). Histopathological analysis of tilapia gills (Oreochromis niloticus Linnaeus, 1758) exposed to sugarcane vinasse. Ecotoxicology and Environmental Safety, 135, 319–326.

    Article  CAS  Google Scholar 

  • Das, P., Samantaray, S., & Rout, G. R. (1997). Studies on cadmium toxicity in plants: a review. Environmental Pollution, 98, 29–36.

    Article  CAS  Google Scholar 

  • España-Gamboa, E., Minagos-Cortes, J., Barahona-Perez, L., Dominguez-Maldonado, J., Hernández-Zarate, G., & Alzate-Gaviria, L. (2011). Vinasse: characterization and treatments. Waste Management and Research, 29(12), 1235–1250.

    Article  Google Scholar 

  • Farrell, M., Perkins, W. T., Hobbs, P. J., Griffith, G. W., & Jones, D. L. (2010). Migration of heavy metals in soil as influenced by compost amendments. Environmental Pollution, 158(1), 55–64.

    Article  CAS  Google Scholar 

  • Felisbino, K., Santos-Filho, R., Piancini, L. D., Cestari, M. M., & Leme, D. M. (2018). Mesotrione herbicide does not cause genotoxicity, but modulates the genotoxic effects of atrazine when assessed in mixture using a plant test system (Allium cepa). Pesticide Biochemistry and Physiology, 150, 83–88.

    Article  CAS  Google Scholar 

  • Fenech, M., & Morley, A. A. (1985). Measurement of micronuclei in lymphocytes. Mutation Research/Environmental Mutagenesis and Related Subjects, 147(1–2), 29–36.

    Article  CAS  Google Scholar 

  • Ferreira-Leitao, V., Gottschalk, L. M. F., Ferrara, M. A., Nepomuceno, A. L., Molinari, H. B. C., & Bon, E. P. (2010). Biomass residues in Brazil: availability and potential uses. Waste and Biomass Valorization, 1(1), 65–76.

    Article  CAS  Google Scholar 

  • Francisco, A., Christofoletti, C. A., & Fontanetti, C. S. (2014). Evaluation of allowed parameters for nickel in freshwater bodies using the Allium cepa test. Ciências Biológicas e da Saúde, 35, 49–60.

    Article  Google Scholar 

  • Freire, W. J., & Cortez, L. A. (2000). Vinhaça de cana-de-açúcar. Agropec., 203 (in Portuguese).

  • Garcia, C. F. H., Souza, R. B., De Souza, C. P., Christofoletti, C. A., & Fontanetti, C. S. (2017). Toxicity of two effluents from agricultural activity: comparing the genotoxicity of sugar cane and orange vinasse. Ecotoxicology and Environmental Safety, 142, 216–221.

    Article  CAS  Google Scholar 

  • Gianchini, C. F., & Ferraz, M. V. (2009). Benefícios da utilização de vinhaça em terras de plantio de cana-de-açúcar – Revisão de Literatura. Rev Cient Eletrôn de Agron, 3, 1–15 (in Portuguese).

    Google Scholar 

  • Gjorgieva, D., Kadifkova-Panovska, T., Mitrev, S., Kovacevik, B., Kostadinovska, E., Bačeva, K., & Stafilov, T. (2012). Assessment of the genotoxicity of heavy metals in Phaseolus vulgaris L. as a model plant system by random amplified polymorphic DNA (RAPD) analysis. Journal of Environmental Science and Health, Part A, 47(3), 366–373.

    Article  CAS  Google Scholar 

  • Haq, I., Kumar, S., Raj, A., Lohani, M., & Satyanarayana, G. N. V. (2017). Genotoxicity assessment of pulp and paper mill effluent before and after bacterial degradation using Allium cepa test. Chemosphere, 169, 642–650.

  • ISO- International Organization For Standardization, (2004). Soil quality—determination of the effects of pollutants on soil flora – Part 1 and Part 2.

  • Jansen, L. L., & Cronin, E. H. (1953). Halogeton on trial. Utah Farm & Home Science, 14, 38–39.

    Google Scholar 

  • Justice, O. L., & Reece, M. H. (1954). A review of literature and investigation on the effects of hydrogen-ion concentration on the germination of seeds. Proceedings of the Association of Official Seed Analysts, 44, 144–149.

    Google Scholar 

  • Karaouzas, I., Cotou, E., Albanis, T. A., Kamarianos, A., Skoulikidis, N. T., & Giannakou, U. (2011). Bioassays and biochemical biomarkers for assessing olive mill and citrus processing wastewater toxicity. Environmental Toxicology, 26(6), 669–676.

    Article  CAS  Google Scholar 

  • Kekec, G., Sakcali, M. S., & Uzonur, I. (2010). Assessment of genotoxic effects of boron on wheat (Triticum aestivum L.) and bean (Phaseolus vulgaris L.) by using RAPD analysis. Bulletin of Environmental Contamination and Toxicology, 84(6), 759–764.

    Article  CAS  Google Scholar 

  • Kim, R. Y., Yoon, J. K., Kim, T. S., Yang, J. E., Owens, G., & Kim, K. R. (2015). Bioavailability of heavy metals in soils: definitions and practical implementation—a critical review. Environmental Geochemistry and Health, 37(6), 1041–1061.

    Article  CAS  Google Scholar 

  • Leme, D. M., & Marin-Morales, M. A. (2009). Allium cepa test in environmental monitoring: a review on its application. Mutation Research, 682(1), 71–81.

    Article  CAS  Google Scholar 

  • Marinho, J. F. U., Correia, J. E., de Castro Marcato, A. C., Pedro-Escher, J., & Fontanetti, C. S. (2014). Sugar cane vinasse in water bodies: impact assessed by liver histopathology in tilapia. Ecotoxicology and Environmental Safety, 110, 239–245.

    Article  CAS  Google Scholar 

  • Musgrove, E., Seaman, M., & Hedley, D. (1987). Relationship between cytoplasmic pH and proliferation during exponential growth and cellular quiescence. Experimental Cell Research, 172(1), 65–75.

    Article  CAS  Google Scholar 

  • Navarro, S., Vela, N., & Navarro, G. (2007). An overview on the environmental behaviour of pesticide residues in soils. Spanish Journal of Agricultural Research, 5(3), 357–375.

    Article  Google Scholar 

  • OECD- Organization for Economic Cooperation and Development. (2003). Guideline 208. Terrestrial plant test: 208; Seedling emergence and seedling growth test.

  • Oliveira, J. P. W., Dos Santos, R. N., Pibernat, C. C., & Boeira, J. M. (2012). Genotoxicity and physical chemistry analysis of waters from Sinos River (RS) using Allium cepa and Eichhornia crassipesas bioindicators. Biochemistry and Biotechnology Reports, 1(1), 15–22.

    Article  Google Scholar 

  • Palmieri, M. J., Luber, J., Andrade-Vieira, L. F., & Davide, L. C. (2014). Cytotoxic and phytotoxic effects of the main chemical components of spent pot-liner: a comparative approach. Mutation Research, 763, 30–35.

    Article  CAS  Google Scholar 

  • Pedro-Escher, J., Maziviero, G. T., & Fontanetti, C. S. (2014). Mutagenic action of sugar cane vinasse in the Tradescantia Pallida test system. Journal of Ecosystem and Ecography, 4(2), 145.

    Article  Google Scholar 

  • Pedro-Escher, J., Christofoletti, C. A., Ansoar-Rodríguez, Y., & Fontanetti, C. S. (2016). Sugarcane vinasse, a residue of ethanol industry: toxic, cytotoxic and genotoxic potential using the Allium cepa test. Journal of Environmental Protection, 7(5), 602–612.

    Article  CAS  Google Scholar 

  • Rajiv, S., Jerobin, J., Saranya, V., Nainawat, M., Sharma, A., Makwana, P., & Mukherjee, A. (2016). Comparative cytotoxicity and genotoxicity of cobalt (II, III) oxide, iron (III) oxide, silicon dioxide, and aluminum oxide nanoparticles on human lymphocytes in vitro. Human & Experimental Toxicology, 35(2), 170–183.

    Article  CAS  Google Scholar 

  • Ramalho, J. F. G. P., & Sobrinho, N. M. B. A. (2001). Metais pesados em solos cultivados com cana-de-açúcar pelo uso de resíduos agroindustriais. Rev Florest Amb, 8(1), 120–129 (in Portuguese).

    Google Scholar 

  • Rank, J., & Nielsen, M. H. (1997). Allium cepa anaphase-telophase root tip chromosome aberration assay on N–methyl-N-nitrosourea, maleic hydrazide, sodium azide, and ethyl methanesulfonate. Mutation Research, 390, 121–127.

    Article  CAS  Google Scholar 

  • Rezzadori K., & Benedetti S. (2009). Proposições para valorização de resíduos do processamento do suco de laranja. In: International workshop advances in cleaner production. São Paulo, SP, 1–11 (in Portuguese).

  • Rieuwerts, J. S., Thornton, I., Farago, M. E., & Ashmore, M. R. (1998). Factors influencing metal bioavailability in soils: preliminary investigations for the development of a critical loads approach for metals. Chemical Speciation & Bioavailability, 10(2), 61–75.

    Article  CAS  Google Scholar 

  • Russel, P. J. (2002). Chromosomal mutation. In B. Cummings (Ed.), Genetics (2nd ed., pp. 595–621). San Francisco: Pearson Education Inc.

    Google Scholar 

  • Santos, C. B., Longhi, S. J., Hoppe, J. M., & Moscovich, F. A. (2000). Efeito do volume de tubetes e tipos de substratos na qualidade de mudas de Cryptomeria japonica (L.F.). Cienc Florest, 10(2), 1–15 (in Portuguese).

    Article  Google Scholar 

  • Saverini, M., Catanzaro, I., Sciandrello, G., Avellone, G., Indelicato, S., Marcì, G., & Palmisano, L. (2012). Genotoxicity of citrus wastewater in prokaryotic and eukaryotic cells and efficiency of heterogeneous photocatalysis by TiO2. Journal of Photochemistry and Photobiology B: Biology, 108, 8–15.

    Article  CAS  Google Scholar 

  • Sociedade Nacional de Agricultura. (2014). Available on: http://www.sna.agr.br/etanol-da-laranja-pode-entrar-no-mercado-em-dois-anos/ . Accessed on August 28th, 2018.

  • Souguir, D., Ferjani, E., Ledoigt, G., & Goupil, P. (2008). Exposure of Vicia faba and Pisum sativum to copper-induced genotoxicity. Protoplasma, 233(3–4), 203.

    Article  CAS  Google Scholar 

  • Souza R. B., Moreira-de-Sousa C., Christofoletti C. A., Souza C. P., & Fontanetti C. S. (2017a). Impacto de resíduos (vinhaça e biossólido) lançados no cultivo de cana-de-açúcar em representantes da fauna edáfica. In: Fontanetti C.S., & Correa O.B. (eds) Cana-de-açúcar e seus impactos: uma visão acadêmica. 1st edn. Brazil: Canal 6, pp 197–214 (in Portuguese).

  • Souza, R. B., De Souza, C. P., Bueno, O. C., & Fontanetti, C. S. (2017b). Genotoxicity evaluation of two metallic-insecticides using Allium cepa and Tradescantia pallida: a new alternative against leaf-cutting ants. Chemosphere, 168, 1093–1099.

    Article  Google Scholar 

  • Steinkellner, H., Mun-Sik, K., Helma, C., et al. (1998). Genotoxic effects of heavy metals: comparative investigation with plant bioassays. Environmental and Molecular Mutagenesis, 31(2), 183–191.

    Article  CAS  Google Scholar 

  • Stubbendieck, J. (1974). Effect of pH on germination of three grass species. Journal of Range Management, 27(1), 78–79.

    Article  CAS  Google Scholar 

  • Tavares, V. B., Sivieri, K., Ceron, C. R., et al. (1998). Utilização do resíduo líquido de indústria de processamento de suco de laranja como meio de cultura de Penicillium citrinum: depuração biológica do resíduo e produção de enzima. Quim Nova, 21(6), 722–725 (in Portuguese).

    Article  CAS  Google Scholar 

  • USEPA- United States Environmental Protection Agency. (1996). Ecological effects test guidelines (OPPTS 850.4200): Seed germination/root elongation toxicity test.

  • Valerio, M. E., Garcia, J. F., & Peinado, F. M. (2007). Determination of phytotoxicity of soluble elements in soils, based on a bioassay with lettuce (Lactuca sativa L.). The Science of the Total Environment, 378, 63–66.

    Article  CAS  Google Scholar 

  • Vries W., Groenenberg J.E., Lofts S., Tipping E., & Posch M. (2012). Critical loads of heavy metal for soils. In: Alloway B.J., & Trevors J.T. (eds) Heavy metals in soil. 3rd ed. Springer, pp 211-240.

  • Wilkins, M. R., Widmer, W. W., Grohmann, K., & Cameron, R. G. (2007). Hydrolysis of grapefruit peel waste with cellulase and pectinase enzymes. Bioresource Technology, 98(8), 1596–1601.

    Article  CAS  Google Scholar 

  • Wise, S. S., Schuler, J. H., Katsifis, S. P., & Wise, J. P., Sr. (2003). Barium chromate is cytotoxic and genotoxic to human lung cells. Environmental and Molecular Mutagenesis, 42(4), 274–278.

    Article  CAS  Google Scholar 

  • Yi, M., Yi, H., Li, H., & Wu, L. (2010). Aluminum induces chromosome aberrations, micronuclei, and cell cycle dysfunction in root cells of Vicia faba. Environmental Toxicology, 25(2), 124–129.

    CAS  Google Scholar 

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Acknowledgments

The authors thank Dr. Dejanira de Franceschi de Angelis and Dilza Aparecida Nalin de Oliveira Leite for helping in the preparation of the orange vinasse.

Funding

This study received funding from Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, process n. 2014/17998-7 and 2012/50197-2).

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Garcia, C.F.H., de Souza, R.B., de Souza, C.P. et al. Effluent from Citrus Industry: Toxic Parameters of Orange Vinasse. Water Air Soil Pollut 230, 201 (2019). https://doi.org/10.1007/s11270-019-4260-4

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