Cited by 41Environmental Toxicology and EcotoxicologyHeavy metals in environmentHeavy Metal Exposure and Toxicity

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Long-term exposure of the isopod Porcellionides pruinosus to nickel: Costs in the energy budget and detoxification enzymes

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Abstract

Terrestrial isopods from the species Porcellionides pruinosus were exposed to the maximum allowed nickel concentration in the Canadian framework guideline (50 mg Ni/kg soil) and to 5× this concentration (250 mg Ni/kg soil). The exposure lasted for 28 days and was followed by a recovery period of 14 days where organisms were changed to clean soil. Organisms were sampled after 24 h, 48 h, 96 h, 7 days, 14 days, 21 days, and 28 days of exposure, and at days 35 and 42 during the recovery period. For each sampling time the acetylcholinesterase (AChE), glutathione-S-transferases (GST), catalase (CAT), lactate dehydrogenase (LDH) activities were determined as well as lipid peroxidation rate (LPO) along with lipids, carbohydrates, proteins content, energy available (Ea), energy consumption (Ec) and cellular energy allocation (CEA). The integrated biomarker response (IBR) was calculated for each sampling time as well as for each one of the above parameters. In addition, mortality was also recorded throughout the assay. The results obtained showed that nickel induced oxidative stress, evidenced by results on GST, GPx, CAT or LPO, but also on changes in the energy reserves content of these organisms. In addition, this study showed that these organisms possess a specific strategy to handle nickel toxicity. In this case, biomarkers were associated with costs in the energy budget, and the increase of energy reserves has a compensation for that cost.

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Research works printed but not linked: 66

  1. Alikhan, 1990, Copper and nickel uptake and accumulation, and their effects on redox and electrical potentials of hepatopancreatic cells of Oniscus asellus Linnaeus (Porcellionidae, Isopoda), Can. J. Zool., 68, 651, 10.1139/z90-094 · DOI
  2. Armstrong, 1987, Enzyme-catalyzed detoxication reactions – mechanisms and stereochemistry, Crit. Rev. Biochem. Mol. Biol., 22, 39, 10.3109/10409238709082547 · DOI
  3. Bayley, 1997, Woodlouse locomotor behavior in the assessment of clean and contaminated field sites, Environ. Toxicol. Chem., 16, 2309, 10.1002/etc.5620161116 · DOI
  4. Beliaeff, 2002, Integrated biomarker response: a useful tool for ecological risk assessment, Environ. Toxicol. Chem., 21, 1316, 10.1002/etc.5620210629 · DOI
  5. Bird, 1984, Comparative studies on different methods of malonaldehyde determination, Methods Enzymol., 105, 299, 10.1016/S0076-6879(84)05038-2 · DOI
  6. Bradford, 1976, Arapid and sensitive method for the quantification of microgram quantities of protein, utilising the principle of protein-dye landing, Anal. Biochem., 72, 248, 10.1016/0003-2697(76)90527-3 · DOI · Paper page
  7. Broerse, 2010, Mixture effects of nickel and chlorpyrifos on Folsomia candida (Collembola) explained from development of toxicity in time, Chemosphere, 79, 953, 10.1016/j.chemosphere.2010.02.032 · DOI
  8. Cadenas, 2000, Mitochondrial free radical generation, oxidative stress, and aging, Free Radical Biol. Med., 29, 222, 10.1016/S0891-5849(00)00317-8 · DOI · Paper page
  9. Calabrese, 2001, Hormesis: a generalizable and unifying hypothesis, Crit. Rev. Toxicol., 31, 353, 10.1080/20014091111730 · DOI
  10. Calabrese, 2005, The occurrence of hormetic dose responses in the toxicological literature, the hormesis database: an overview, Toxicol. Appl. Pharmacol., 202, 289, 10.1016/j.taap.2004.06.023 · DOI
  11. Calhôa, 2012, Effects on survival and reproduction of Porcellio dilatatus exposed to different Cd species, Ecotoxicology, 21, 48, 10.1007/s10646-011-0762-6 · DOI · Paper page
  12. CBP, 2010. A Review of the Current Canadian Legislative Framework for Wastewater Biosolids. <http://www.cwwa.ca/cbp-pcb/home/home_e.asp>.
  13. Chen, 2002, nickel-induced plasma lipid peroxidation and effect of antioxidants in human blood: involvement hydroxyl radical formation and depletion of α-tocopherol, J. Toxicol. Environ. Health, Part A, 65, 843, 10.1080/00984100290071162 · DOI
  14. Chen, 2003, Nickel-induced oxidative stress and effect of antioxidants in human lymphocytes, Arch. Toxicol., 77, 123, 10.1007/s00204-002-0427-6 · DOI
  15. de Coen, 1997, The use of biomarkers in Daphnia magna toxicity testing. IV. Cellular Energy Allocation: a new methodology to assess the energy budget of toxicant-stressed Daphnia population, J. Aquat. Ecosyst. Stress Recov., 6, 43, 10.1023/A:1008228517955 · DOI
  16. de Coen, 2003, The missing biomarker link: relationships between effects on the cellular energy allocation biomarker of toxicant-stressed Daphnia magna and corresponding population characteristics, Environ. Toxicol. Chem., 22, 1632, 10.1002/etc.5620220727 · DOI
  17. Diamond, 1999, Evolutionary biology: dirty eating for healthy living, Nature, 400, 120, 10.1038/22014 · DOI
  18. Donker, 1990, Metal binding compounds in hepatopancreas and haemolymph of Porcellio scaber (isopoda) from contaminated and reference areas, Comp. Biochem. Physiol. Part C: Comp. Pharmacol., 97, 119, 10.1016/0742-8413(90)90181-8 · DOI
  19. Ellman, 1961, A new and rapid colorimetric determination of acetylcholinesterase activity, Biochem. Pharmacol., 7, 10.1016/0006-2952(61)90145-9 · DOI
  20. Ferreira, 2015, Biomarkers and energy reserves in the isopod Porcellionides pruinosus: the effects of long-term exposure to dimethoate, Sci. Total Environ., 502, 91, 10.1016/j.scitotenv.2014.08.062 · DOI
  21. Ferreira, 2010, Basal levels of enzymatic biomarkers and energy reserves in Porcellionides pruinosus, Soil Biol. Biochem., 10.1016/j.soilbio.2010.08.008 · DOI
  22. Frasco, 2005, Do metals inhibit acetylcholinesterase (AChE)? Implementation of assay conditions for the use of AChE activity as a biomarker of metal toxicity, Biomarkers, 10, 360, 10.1080/13547500500264660 · DOI
  23. Gilman, 1962, Metal carcinogenesis: II. A study on the carcinogenic activity of cobalt, copper, iron, and nickel compounds, Cancer Res., 22, 158
  24. Goldberg, 1988, Regulation of the erythropoietin gene: evidence that the oxygen sensor is a heme protein, Science, 242, 1412, 10.1126/science.2849206 · DOI
  25. Guilhermino, 1996, Inhibition of acetylcholinesterase activity as effect criterion in acute tests with juvenile Daphnia magna, Chemosphere, 32, 727, 10.1016/0045-6535(95)00360-6 · DOI
  26. Gulick, 1995, Mammalian glutathione S-transferase: regulation of an enzyme system to achieve chemotherapeutic efficacy, Pharmacol. Ther., 66, 237, 10.1016/0163-7258(94)00079-I · DOI
  27. Habig, 1974, Glutathione S-transferases – first enzimatic step on mercapturic acid formation, J. Biol. Chem., 249, 7130, 10.1016/S0021-9258(19)42083-8 · DOI
  28. Hames, 1991, A daily cycle of apocrine secretion by the B cells in the hepatopancreas of terrestrial isopods, Can. J. Zool., 69, 1931, 10.1139/z91-267 · DOI
  29. Heikens, 2001, Bioaccumulation of heavy metals in terrestrial invertebrates, Environ. Pollut., 113, 385, 10.1016/S0269-7491(00)00179-2 · DOI
  30. Hopkin, 1990, Species-specific differences in the net assimilation of zinc, cadmium, lead, copper and iron by the terrestrial isopods Oniscus asellus and Porcellio scaber, J. Appl. Ecol., 460, 10.2307/2404294 · DOI
  31. Jansch, 2005, Acute and chronic isopod testing using tropical Porcellionides pruinosus and three model pesticides, Eur. J. Soil Biol., 41, 143, 10.1016/j.ejsobi.2005.09.010 · DOI · Paper page
  32. Lavelle, 1996, Diversity of soil fauna and ecosystem function, Biol. Int., 33, 3
  33. Lee, 1995, Carcinogenic nickel silences gene expression by chromatin condensation and DNA methylation: a new model for epigenetic carcinogens, Mol. Cell. Biol., 15, 2547, 10.1128/MCB.15.5.2547 · DOI
  34. Lefcort, 2008, Hormetic Effects of Heavy Metals in Aquatic Snails: Is a Little Bit of Pollution Good?, EcoHealth, 5, 10, 10.1007/s10393-008-0158-0 · DOI
  35. Loureiro, 2009, Assessing joint toxicity of chemicals in Enchytraeus albidus (Enchytraeidae) and Porcellionides pruinosus (Isopoda) using avoidance behaviour as an endpoint, Environ. Pollut., 157, 625, 10.1016/j.envpol.2008.08.010 · DOI
  36. Loureiro, 2006, Feeding behaviour of the terrestrial isopod Porcellionides pruinosus Brandt, 1833 (Crustacea, Isopoda) in response to changes in food quality and contamination, Sci. Total Environ., 369, 119, 10.1016/j.scitotenv.2006.05.023 · DOI · Paper page
  37. Loureiro, 2005, Terrestrial avoidance behaviour tests as screening tool to assess soil contamination, Environ. Pollut., 138, 121, 10.1016/j.envpol.2005.02.013 · DOI
  38. Loureiro, 2002, Assimilation efficiency and toxicokinetics of 14C-lindane in the terrestrial isopod Porcellionides pruinosus: the role of isopods in degradation of persistent soil pollutants, Ecotoxicology, 11, 481, 10.1023/A:1021013519330 · DOI
  39. MEA, 2005. Millennium Ecosystem Assessment (MEA), Ecosystems and Human Well-Being: Synthesis, Island Press, Washington.
  40. Mohandas, 1984, Low activities of glutathione – related enzymes as factors in the genesis of urinary-bladder cancer, Cancer Res., 44, 5086
  41. Moore, 2004, An integrated biomarker-based strategy for ecotoxicological evaluation of risk in environmental management, Mutat. Res./Fund. Mol. Mech. Mutagen., 552, 247, 10.1016/j.mrfmmm.2004.06.028 · DOI
  42. Morgado, 2013, Environmental- and growth stage-related differences in the susceptibility of terrestrial isopods to UV radiation, J. Photochem. Photobiol., B: Biol., 126, 60, 10.1016/j.jphotobiol.2013.07.002 · DOI
  43. Morgan, 1999, A short overview of molecular biomarker strategies with particular regard to recent developments in earthworms, Pedobiologia, 43, 574, 10.1016/S0031-4056(24)00583-3 · DOI
  44. Nascarella, 2003, Hormesis and stage specific toxicity induced by cadmium in an insect model, the queen blowfly, Phormia regina Meig, Environ. Pollut., 124, 257, 10.1016/S0269-7491(02)00479-7 · DOI
  45. Ohkawa, 1979, Assay for lipid peroxides in animal – tissues by thiobarbituric acid reaction, Anal. Biochem., 95, 351, 10.1016/0003-2697(79)90738-3 · DOI
  46. Pane, 2003, Acute waterborne nickel toxicity in the rainbow trout (Oncorhynchus mykiss) occurs by a respiratory rather than ionoregulatory mechanism, Aquat. Toxicol., 63, 65, 10.1016/S0166-445X(02)00131-5 · DOI
  47. Phipps, 2002, Essentiality of nickel and homeostatic mechanisms for its regulation in terrestrial organisms, Environ. Rev., 10, 209, 10.1139/a02-009 · DOI
  48. Ribeiro, 1999, Novel bioassay based on acetylcholinesterase and lactate dehydrogenase activities to evaluate the toxicity of chemicals to soil isopods, Ecotoxicol. Environ. Saf., 44, 287, 10.1006/eesa.1999.1837 · DOI
  49. Rousseeuw, 1993, Alternatives to the median absolute deviation, J. Am. Stat. Assoc., 88, 1273, 10.1080/01621459.1993.10476408 · DOI
  50. Santos, 2010, Toxic effects of molluscicidal baits to the terrestrial isopod Porcellionides pruinosus (Brandt, 1833), J. Soils Sediments, 10, 1335, 10.1007/s11368-010-0246-y · DOI
  51. Scott-Fordsmand, 1998, Toxicity of nickel to the earthworm and the applicability of the neutral red retention assay, Ecotoxicology, 7, 291, 10.1023/A:1008824531114 · DOI
  52. Stanek, 2006, Linkage of biomarkers along levels of biological complexity in juvenile and adult diazinon fed terrestrial isopod (Porcellio scaber, Isopoda, Crustacea), Chemosphere, 64, 1745, 10.1016/j.chemosphere.2005.12.070 · DOI
  53. Sunderman, 1985, Increased lipid peroxidation in tissues of nickel chloride-treated rats, Ann. Clin. Lab. Sci., 15, 229
  54. Takeda, 1980, The aggregation pheromone of some terrestrial isopod crustaceans, Experientia, 36, 1296, 10.1007/BF01969598 · DOI
  55. Tarnawska, 2007, Nickel toxicity in the hepatopancreas of an isopod Porcellio scaber (Oniscidea), Nucl. Instrum. Methods Phys. Res., Sect. B: Beam Interact. Mater. Atoms, 260, 213, 10.1016/j.nimb.2007.02.082 · DOI
  56. Tourinho, 2013, Influence of soil pH on the toxicity of zinc oxide nanoparticles to the terrestrial isopod Porcellionides pruinosus, Environ. Toxicol. Chem., 32, 2808, 10.1002/etc.2369 · DOI · Paper page
  57. Valko, 2005, Metals, toxicity and oxidative stress, Curr. Med. Chem., 12, 1161, 10.2174/0929867053764635 · DOI · Paper page
  58. Vandenbrouck, 2009, Nickel and binary metal mixture responses in Daphnia magna: molecular fingerprints and (sub)organismal effects, Aquat. Toxicol., 92, 18, 10.1016/j.aquatox.2008.12.012 · DOI
  59. Verslycke, 2004, Cellular energy allocation and scope for growth in the estuarine mysid Neomysis integer (Crustacea: Mysidacea) following chlorpyrifos exposure: a method comparison, J. Exp. Mar. Biol. Ecol., 306, 1, 10.1016/j.jembe.2003.12.022 · DOI
  60. Vijver, 2004, Internal metal sequestration and its ecotoxicological relevance: a review, Environ. Sci. Technol., 38, 4705, 10.1021/es040354g · DOI
  61. Vijver, 2005, Surface adsorption of metals onto the earthworm Lumbricus rubellus and the isopod Porcellio scaber is negligible compared to absorption in the body, Sci. Total Environ., 340, 271, 10.1016/j.scitotenv.2004.12.018 · DOI
  62. Vink, 1995, The importance of the exposure route when testing the toxicity of pesticides to saprotrophic isopods, Environ. Toxicol. Chem., 14, 1225, 10.1002/etc.5620140715 · DOI
  63. Vink, 1996, Iteroparous reproduction, body growth and energy reserves in a tropical population of the isopod, Porcellionides pruinosus, Pedobiologia, 40, 467, 10.1016/S0031-4056(24)00360-3 · DOI · Paper page
  64. Wu, 2013, Dietary nickel chloride induces oxidative intestinal damage in broilers, Int. J. Environ. Res. Public Health, 10, 2109, 10.3390/ijerph10062109 · DOI
  65. Zimmer, 2002, Is decomposition of woodland leaf litter influenced by its species richness?, Soil Biol. Biochem., 34, 277, 10.1016/S0038-0717(01)00173-0 · DOI
  66. Zimmer, 2003, Leaf litter-colonizing microbiota: supplementary food source or indicator of food quality for Porcellio scaber (Isopoda: Oniscidea)?, Eur. J. Soil Biol., 39, 209, 10.1016/j.ejsobi.2003.07.001 · DOI · Paper page

Metadata

Authors
Ferreira, N. G. C., Cardoso, D. N., Morgado, R., Soares, A. M. V. M., & Loureiro, S.
Affiliations
Centro de Estudos do Ambiente e do Mar (PT)
Corresponding author
  • Ferreira, Nuno G.C.
  • Loureiro, Susana
Venue
Chemosphere
Publisher
Elsevier BV
Published
2015-09
Volume
135
Pages
354-362
ISSN
0045-6535 (ISSN-L)
OpenAlex
W230337351
Cited by
41
References
1
Citations by year
2026: 1 · 2025: 5 · 2024: 2 · 2023: 3 · 2022: 6 · 2021: 2 · 2020: 3 · 2019: 8 · 2018: 6 · 2017: 3 · 2016: 1 · 2015: 1
FWCI
2.30
Type
journal article
Language
en
Open access
Locations
  • Chemosphere (publishedVersion)
  • PubMed (publishedVersion)
  • ORCA Online Research @Cardiff (Cardiff University) (submittedVersion)
Funders
  • FCT-Fundação para a Ciência e Tecnologia
  • ERDF
Topics
  • Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Environmental Toxicology and Ecotoxicology
  • Physical Sciences › Environmental Science › Pollution › Heavy metals in environment
  • Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Heavy Metal Exposure and Toxicity
Keywords
Porcellionides pruinosus, terrestrial isopods, nickel toxicity, energy balance, energy allocation, energy reserves, oxidative stress, detoxification enzymes, acetylcholinesterase, glutathione S-transferase, catalase, lactate dehydrogenase, lipid peroxidation, integrated biomarker response, convalescence, soil contamination
MeSH terms
Acetylcholinesterase, Animals, Canada, Catalase, Inactivation, Metabolic, Nickel, Soil, Water Pollutants, Chemical, Lipid Peroxidation, Biomarkers, Oxidative Stress, Isopoda

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