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Diplopods as Soil Bioindicators of Toxicity After Application of Residues From Sewage Treatment Plants and Ethanol Industry

Published online by Cambridge University Press:  27 October 2016

Cintya A. Christofoletti ,
Annelise Francisco ,
Janaína Pedro-Escher ,
Vinícius D. Gastaldi  and
Carmem S. Fontanetti
Cintya A. Christofoletti
Affiliation:
UNESP (São Paulo State University), Institute of Biosciences, Department of Biology, Av. 24-A, n°1515, 13506-900, Rio Claro, São Paulo, Brazil Hermínio Ometto University Center (UNIARARAS), Laboratory of Structural Biology, Av. Dr. Maximiliano Baruto, n° 500, 13607-339, Araras, São Paulo, Brazil
Annelise Francisco
Affiliation:
UNESP (São Paulo State University), Institute of Biosciences, Department of Biology, Av. 24-A, n°1515, 13506-900, Rio Claro, São Paulo, Brazil
Janaína Pedro-Escher
Affiliation:
UNESP (São Paulo State University), Institute of Biosciences, Department of Biology, Av. 24-A, n°1515, 13506-900, Rio Claro, São Paulo, Brazil
Vinícius D. Gastaldi
Affiliation:
UNESP (São Paulo State University), Institute of Biosciences, Department of Biology, Av. 24-A, n°1515, 13506-900, Rio Claro, São Paulo, Brazil
Carmem S. Fontanetti*
Affiliation:
UNESP (São Paulo State University), Institute of Biosciences, Department of Biology, Av. 24-A, n°1515, 13506-900, Rio Claro, São Paulo, Brazil
*
*Corresponding author. fontanet@rc.unesp.br
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Abstract

Residues like sewage sludge and vinasse have been reused as agricultural fertilizers, but they also present a potential to contaminate soils. Diplopods have been considered excellent bioindicators of soil contamination. In the present study, Rhinocricus padbergi were used to assess toxicity in samples of sewage sludge, biosolids, and sugarcane vinasse. The behavioral analysis, mortality rate, and histological, histochemical, and ultrastructural analyses of the midgut of diplopods were the parameters evaluated. Behaviorally, some diplopods avoided burying themselves after 30 days in soil with biosolid or vinasse. Besides, certain residue combinations were able to cause death of all individuals between 60 and 90 days of exposure. The main tissue responses were significant brush border thickening, induction of epithelial renovation, clustering of hemocytes, accumulation of cytoplasmic granules in hepatic cells, hepatic cells with heteropycnotic nuclei, and cytoplasmic degradation. Alterations were observed at various levels among treatments with different samples and exposure times. Ultrastructural analysis revealed elongation of microvilli coated with a layer of an amorphous substance, resulting in a thicker brush border as observed in the histological analysis. After 30 days of exposure, animals showed an accumulation of spherocrystals in hepatic cells and high absorption of substances, based on the elongation of microvilli. Results obtained in the chemical analysis and the behaviors observed in diplopods suggest that animals processed the residues. Therefore, caution should be exercised in the disposal of these residues in agriculture.

Keywords

soil toxicityhistopathologymillipedes
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 22 , Issue 5 , October 2016 , pp. 1098 - 1110
Copyright
© Microscopy Society of America 2016 

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References

Artuso, N., Kenedy, T.F., Connery, J., Grant, J. & Schmidt, O. (2011). Effects of biosolids at varying rates on earthworms (Eisenia fetida) and springtails (Folsomia candida). Appl Env Soil Sci 2011, 1–11.Google Scholar
Bernet, D., Schimidt, H., Meier, W., Burkhardt-Holm, P. & Wahli, T. (1999). Histopatology in fish: proposal for a protocol to assess aquatic pollution. J Fish Dis 22, 25–34.Google Scholar
Bertelli, C. (2007). Efeitos da disposição de lodos de curtume no solo e na planta’, 135p. Tese de Doutorado. Universidade Estadual Paulista, Rio Claro, São Paulo. Availabe at http://www.athena.biblioteca.unesp.br/exlibris/bd/brc/33004137036P9/2007/bertellic_dr_rcla.pdf (retrieved November 20, 2011).Google Scholar
Bettiol, W., Carvalho, P.C.T. & Franco, B.J.D.C. (1983). Utilização do lodo de esgoto como fertilizante. O solo 75, 44–54.Google Scholar
Bettiol, W. & Ghini, R. (2011). Impacts of sewage sludge in tropical soil: A case study in Brazil. Appl Env Soil Sci 2011, 1–12.CrossRefGoogle Scholar
Bozzatto, V. & Fontanetti, C.S. (2012). Sewage sludge toxicity in edaphic organism: Analysis of midgut responses in the diplopod Rhinocricus padbergi . Microsc Res Techniq 75, 869–875.CrossRefGoogle ScholarPubMed
Brito, F.L., Rolim, M.M. & Pedrosa, E.M.R. (2007). Concentração de cátions presente no lixiviado de solos tratados com vinhaça. Eng Agric 27, 773–781.Google Scholar
Camargo-Mathias, M.I., Fantazzini, E.R. & Fontanetti, C.S. (2004). Ultrastructural features of the midgut of Rhinocricus padbergi (Diplopoda: Spirobolida). Braz J Morphol Sci 21, 65–71.Google Scholar
Camilotti, F., Marques, M.O., Andrioli, I., Silva, A.R., Junior, L.C.T. & Nobile, F.O. (2007). Acúmulo de metais pesados em cana-de-açúcar mediante a aplicação de lodo de esgoto e vinhaça. Eng Agric 27, 284–293.Google Scholar
Cesar, R.G., Egler, S.G., Polivanov, H., Castilhos, Z.C., Rodrigues, A.P.C. & Araújo, P.A. (2008). Biodisponibilidade de mercúrio, zinco e cobre em distintas frações granulométricas de solo contaminado utilizando oligoquetas da espécie Eisenia andrei . Anu Inst Geocienc 31, 33–41.Google Scholar
Christofoletti, C.A., Francisco, A. & Fontanetti, C.S. (2012). Biosolid soil application: Toxicity tests under laboratory conditions. Appl Env Soil Sci 2012, 1–9.Google Scholar
Christofoletti, C.A., Pedro-Escher, J. & Fontanetti, C.S. (2013). Assessment of the genotoxicity of two agricultural residues after processing by diplopods using the Allium cepa assay. Water Air Soil Pollut 224, 1523–1537.Google Scholar
Cortet, J., Vauflery, A.G., Poinsot-Balaguer, N., Gomot, L., Texier, C. & Cluzeau, D. (1999). The use of invertebrate soil fauna in monitoring pollutant effects. Eur J Soil Biol 35, 115–134.CrossRefGoogle Scholar
Dittbrenner, N., Schmitt, H., Capowiez, Y. & Triebskorn, R. (2011). Sensitivity of Eisenia fetida in comparison to Aporrectodea caliginosa and Lumbricus terrestris after imidacloprid exposure. Body mass change and histopathology. J Soil Sediment 11, 1000–1010.Google Scholar
Eom, I.M., Rast, C., Veber, A.M. & Vasseur, P. (2007). Ecotoxicity of a polycyclic aromatic hydrocarbon (PAH)-contaminated soil. Ecotoxicol Environ Saf 67, 190–205.Google Scholar
Fantazzini, E.R., Fontanetti, C.S. & Camargo-Mathias, M.I. (2002). Midgut of the millipede, ‘Rhinocricus padbergi’ Verhoeff, 1938 (Diplopoda: Spirobolida): Histology and histochemistry. Arthropoda Sel 11, 135–142.Google Scholar
Fontanetti, C.S., Christofoletti, C.A., Pinheiro, T.G., Souza, T.S. & Pedro-Escher, J. (2010). Miscroscopy as a tool in toxicological evaluations. In Microscopy: Science, Technology, Applications and Education, Méndez-Vilas, A. & Diaz, J. (Eds.), pp. 1001–1007. Badajoz: Formatex Research Center.Google Scholar
Fontanetti, C.S., Nogarol, L.R., Souza, R.B., Perez, D.G. & Maziviero, G.T. (2011). Bioindicators and biomarkers in the assessment of soil toxicity. In Soil Contamination, Pascucci, S. (Ed.), pp. 143–159. Rijeka: InTech Europe.Google Scholar
Fontanetti, C.S., Tiritan, B. & Camargo-Mathias, M.I. (2006). Mineralized bodies in the fat body of Rhinocricus padbergi (Diplopoda) Brazilian. J Morphol Sci 23, 487–493.Google Scholar
Godoy, J.A.P. & Fontanetti, C.S. (2010). Diplopods as bioindicators of soils: Analysis of midgut of individuals maintained in substract containing sewage sludge. Water Air Soil Pollut 210, 389–398.Google Scholar
Gonçalves, G.K., Sousa, R.O., Vahl, L.C. & Bortolon, L. (2008). Solubilização de fosfatos naturais Pato de Minas e Arad em dois solos alagados. Rev. Bras. Ciênc. Solo 32, 2157–2164.Google Scholar
Granato, E.F. & Silva, C.L. (2002). Geração de energia elétrica a partir do resíduo vinhaça. In Procedings of the 4th Encontro de Energia no Meio Rural, 2002, Campinas (SP) [online]. Available at http://www.proceedings.scielo.br/scielo.php?script=sci_arttext&pid=MSC0000000022002000200006 &lng=en&nrm=iso (retrieved March 18, 2010).Google Scholar
Hopkin, S.P. & Read, H.J. (1992). The Biology of Millipedes, 1st ed. New York: Oxford University Press. 233pp.Google Scholar
Junqueira, L.C. & Junqueira, L.M.M.S. (1983). Técnicas Básicas de Citologia e Histologia. São Paulo: Livraria Editora Santos. 123pp.Google Scholar
Köhler, H.R. (2002). Localization of metals in cells of saprophagous soil arthropods (Isopoda, Diplopoda, Collembola). Microsc Res Techniq 56, 393–401.CrossRefGoogle ScholarPubMed
Köhler, H.R. & Triebskorn, R. (1998). Assessment of the cytotoxic impact of heavy metals on soil invertebrates using a protocol integrating qualitative and quantitative components. Biomarkers 3, 109–127.Google Scholar
Lambais, M.R. & Carmo, J.B. (2008). Impactos da aplicação de biossólidos na microbiota de solos tropicais. Rev Bras Ciênc Solo 32, 1129–1138.Google Scholar
Lanno, R., Wells, J., Conder, J., Bradham, K. & Basta, N. (2003). Bioavailability of chemicals in soil for earthworms. Ecotoxicol Environ Saf 57, 39–47.CrossRefGoogle Scholar
Løkke, H. & Van Gestel, C.A.M. (1998). Handbook of Soil Invertebrate Toxicity Tests. Chichester: John Wiley and Sons Ltd.Google Scholar
Martins, A.L.C., Bataglia, O.C. & Camargo, O.A. (2003). Copper, nickel and zinc phytoavailability in an oxisol amended with sewage sludge and liming. Sci Agric 60, 747–754.Google Scholar
Magalhães, M.O.L., Sobrinho, N.M.B.A., Zonta, E., Lima, L.S. & de Paiva, F.S.D. (2011). Mobilidade de bário em solo tratado com sulfato de bário sob condição de oxidação e redução. Quim Nova 34, 1544–1549.Google Scholar
McBride, M.B. (1995). Toxic metal accumulation from agricultural use of sludge: Are USEPA regulations protective? J Environ Qual 25, 5–18.Google Scholar
Merlini, V.V., Nogarol, L.R., Marin-Morales, M.A. & Fontanetti, C.S. (2012). Toxicity of trifluralin herbicide in a representative of the edaphic fauna: Histopathology of the midgut of Rhinocricus pdbergi (Diplopoda). Microsc Res Techniq 75, 1361–1369.Google Scholar
Meyers, T.R. & Hendricks, J.D. (1985). Histopathology. In Fundamental of Aquatic Toxicology: Methods and Applications, Rand, G.M. & Petrocelli, S.R. (Eds.), pp. 283–331. New York: Hemisphere Publishing.Google Scholar
Nakamura, K. & Taira, J. (2005). Distribution of elements in the millipede Oxidus gracilis C. L. Koch (Polydesmida: Paradoxosomatidae) and to relation of environmental habitats. Biometals 18, 651–658.Google Scholar
Nakamura, K., Taira, J. & Higa, Y. (2005). Internal elements of the millipede, Chamberlinius hualienensis Wang (Polydesmida: Paradoxosomatidae). Appl Entomol Zool 40, 283–288.Google Scholar
Natal da Luz, T., Ribeiro, R. & Sousa, J.P. (2004). Avoidance tests with collembola and earthworms as early screening tools for site-specific assessment of polluted soils. Environ Toxicol Chem. 23, 2188–2193.Google Scholar
Nogarol, L.R. & Fontanetti, C.S. (2010). Acute and subchronic exposure of diplopods to substrate containing sewage mud: Tissular responses of the midgut. Micron 41, 239–246.Google Scholar
Nogarol, L.R. & Fontanetti, C.S. (2011). Ultrastructural alterations in the midgut of diplopods after subchronic exposure to substrate containing sewage mud. Water Air Soil Pollut 218, 539–547.CrossRefGoogle Scholar
Oliveira, E.L., Andrade, L.A.B., Faria, M.A., Evangelista, A.W.P. & Morais, A.R. (2009). Uso de vinhaça de alambique e nitrogênio em cana-de-açúcar irrigada e não irrigada. Pesqui Agropecu Bras 44, 1398–1403.Google Scholar
Pearse, A.G.E. (1985). Histochemistry: Theoretical and Apllied, vol. 2, fourth edition. London: J & A Churchill.Google Scholar
Perez, D.G. & Fontanetti, C.S. (2011 a). Assessment of the toxic potential of sewage sludge in the midgut of the diplopod Rhinocricus padbergi . Water Air Soil Pollut 128, 437–444.CrossRefGoogle Scholar
Perez, D.G. & Fontanetti, C.S. (2011 b). Hemocital responses to environmental stress in invertebrates: A review. Environ Monit Assess 177, 437–447.Google Scholar
Petersen, H. & Luxton, M.A. (1982). Comparative analysis of soil fauna populations and their role in decomposition processes. Oikos 39, 291–357.Google Scholar
Phillips, A.D., Giròn, J., Hicks, S., Dougan, G. & Frankel, G. (2000). Intimin from enteropathogenic Escherichia coli mediates remodelling of the eukaryotic cell surface. Microbiology 146, 1333–1344.Google Scholar
Schubart, O. (1942). Os Myriapodes e suas relações com a agricultura. Pap Avulsos Zool 2, 205–234.Google Scholar
Silva, M.A.S., Griebeler, N.P. & Borges, L.C. (2007). Uso de vinhaça e impactos nas propriedades do solo e lençol freático. Rev Bras Eng Agric Ambient 11, 108–114.Google Scholar
Sochová, I., Hofman, J. & Holoubek, I. (2006). Using nematodes in soil ecotoxicology. Environ Int 32, 374–383.Google Scholar
Souza, T.S. & Fontanetti, C.S. (2011). Morphologial biomarkers in the Rhinocricus padbergi midgut exposed to contamined soil. Ecotoxicol Environ Saf 74, 10–18.Google Scholar
Souza, T.S., Christofoletti, C.A., Bozzatto, V. & Fontanetti, C.S. (2014). The use of diplopods in soil ecotoxicology—a review. Ecotoxicol Environ Saf 103, 68–73.Google Scholar
Stevenson, F.J. (1982). Humus Chemistry: Genesis, Composition, Reaction. New York: John Wiley. 496 pp.Google Scholar
Suthar, S. (2010). Pilot-scale vermireactors for sewage sludge stabilization and metal remediation process: Comparison with small-scale vermireactors. Ecol Eng 36, 703–712.Google Scholar
Triebskorn, R., Henderson, I.F. & Martin, A.P. (1999). Detection of iron in tissues from slugs (Deroceras reticulatum Müller) after ingestion of iron chelates by means of energy-filtering transmission electron microscopy (EFTEM). Pest Manag Sci 55, 55–61.Google Scholar
Triebskorn, R., Köhler, H.R., Zanh, T., Vogt, G., Ludwing, M., Rumpf, S., Kratzmann, M., Alberti, G. & Storch, V. (1991). Invertebrate cells as targets for hazardous substances. Zeitschfirt fuer Angewandte Zoologie 78, 277–287.Google Scholar
Vanzo, J.E., Macedo, L.S. & Tsutiya, M.T. (2010). ETE Franca: uma estação que além de tratar os esgotos, produz insumos agrícolas. In XXVII Congresso Interamericano de Engenharia Sanitária e Ambiental, pp. 1–14. Available at http://www.cepis.org.pe/bvsaidis/aresidua/i-084.pdf (retrieved March 18, 2010).Google Scholar
Walker, J. (1976). Host defense mechanisms in the gastrointestinal tract. Pediatrics 57, 901–916.Google Scholar
Zakeri, Z. & Lockshin, R.A. (2002). Cell death during development. J Immunol Methods 265, 3–20.Google Scholar
Zweifach, B.W., Grant, L. & Mccluskey, R.T. (1974). The Inflammatory Process. New York: Academic Press. 419pp.Google Scholar