945
Views
4
CrossRef citations to date
0
Altmetric
Research Article

A comparative study of the oxidative system in Chironomidae larvae with contrasting feeding strategies

&
Pages 463-474 | Received 22 May 2020, Accepted 10 Aug 2020, Published online: 18 Sep 2020

References

  • Aebi H. 1984. Catalase in vitro. Methods in Enzymology 105:121–126.
  • Ahmad S. 1992. Biochemical defense of pro-oxidant plant allelochemicals by herbivorous insects. Biochemical Systematics and Ecology 20:269–296. DOI: 10.1016/0305-1978(92)90040-K.
  • Ahmad S. 1995. Oxidative stress from environmental pollutants. Archives of Insect Biochemistry and Physiology 29:135–157. DOI: 10.1002/arch.940290205.
  • Al-Shami SA, Rawi CSM, Hassanahmad A, Nor SAM. 2010. Distribution of Chironomidae (Insecta: Diptera) in polluted rivers of the Juru River Basin, Penang, Malaysia. Journal of Environmental Sciences 22(11):1718–1727. DOI: 10.1016/S1001-0742(09)60311-9.
  • Armitage PD, Cranston PS, Pinder LCV. 1995. The Chironomidae: Biology and Ecology of non-biting Midges. London: Chapman & Hall.
  • Baker AS, McLachlan AJ. 1979. Food preferences of Tanypodinae larvae (Diptera: Chironomidea). Hydrobiologia 62(3):283–288. DOI: 10.1007/BF00043546.
  • Bartosz G. 2003. Cookbook for novice researchers, reactive oxygen species. In: Second face oxygen: Free radical in nature. 2nd ed. Warsaw: Wydawnictwo Naukowe PWN.
  • Battarbee RW. 2000. Palaeolimnological approaches to climate change, with special regard to the biological record. Quaternary Science Reviews 19:107–124. DOI: 10.1016/S0277-3791(99)00057-8.
  • Berra E, Forcella M, Giacchini R, Marziali L, Rossaro B, Parenti P 2004. Evaluation of enzyme biomarkers in freshwater invertebrates from Taro and Ticino river, Italy. Annales De Limnologie - International Journal of Limnology 40:169–180. DOI: 10.1051/limn/2004015.
  • Bielen A, Bosnjak I, Sepcic K, Jaklic M, Cvitanic M, Lusic J, et al. 2016. Differences in tolerance to anthropogenic stress between invasive and native bivalves. The Science of the Total Environment 543:449–459. DOI: 10.1016/j.scitotenv.2015.11.049.
  • Bonnail E, Buruaem LM, Araujo GS, Abessa DMS, Del Valls TA. 2016. Multiple Biomarker Responses in Corbicula fluminea Exposed to Copper in Laboratory Toxicity. Archives of Environmental Contamination and Toxicology 71:278–285. DOI: 10.1007/s00244-016-0281-9.
  • Bonnefoy M, Drai J, Kostka T. 2002. Antioxidants to slow aging, facts and perspectives. La Presse medicale 25:1174–1184.
  • Brodersen KP, Pedersen O, Lindegaard C, Chironomids HK. 2004. (Diptera) and oxy-regulatory capacity: An experimental approach to paleolimnological interpretation. Limnology and Oceanography 49:1549–1559. DOI: 10.4319/lo.2004.49.5.1549.
  • Brodersen KP, Pedersen O, Walker IR, Jensen MT. 2008. Respiration of midges (Diptera; Chironomidae) in British Columbian lakes: Oxy-regulation, temperature and their role as palaeo-indicators. Freshwater Biology 53:593–602. DOI: 10.1111/j.1365-2427.2007.01922.x.
  • Brown AR, Bickley LK, Le Page G, Hosken DJ, Paull GC, Hamilton PB, et al. 2011. Are toxicological responses in laboratory (inbred) zebrafish representative of those in outbred (wild) populations?—A case study with an endocrine disrupting chemical. Environmental Science & Technology 45:4166–4172. DOI: 10.1021/es200122r.
  • Bukowska B. 2005. Glutation: Funkcje i czynniki zmniejszające jego stężenie. Medycyna Pracy 56:69–80.
  • Cajaraville MP, Bebianno MJ, Blasco J, Porte C, Sarasquete C, Viarengo A. 2000. The use of biomarkers to assess the impact of pollution in coastal environments of the Iberian Peninsula: A practical approach. The Science of the Total Environment 247:295–311. DOI: 10.1016/S0048-9697(99)00499-4.
  • Campos D, Gravato C,, Quintaneiro C, Soares AMVM, Pestana JLT. 2016. Responses of the aquatic midge Chironomus riparius to DEET exposure. Aquatic Toxicology (Amsterdam, Netherlands) 172:80–85. DOI: 10.1016/j.aquatox.2015.12.020.
  • Cañedo-Argüelles M, Bogan M, Lytle DA, Are Chironomidae PN. 2016. (Diptera) good indicators of water scarcity? Dryland streams as a case study. Ecological Indicators 71:155–162. DOI: 10.1016/j.ecolind.2016.07.002.
  • Choi J, Ha MH. 2009. Effect of cadmium exposure on the globin protein expression in 4th instar larvae of Chironomus riparius Mg. (Diptera: Chironomidae): An ecotoxicoproteomics approach. Proteomics 9:31–39. DOI: 10.1002/pmic.200701197.
  • Choi J, Roche H, Caquet T. 1999. Characterization of superoxide dismutase activity in Chironomus riparius Mg. (Diptera. Chironomidae) larvae, a potential biomarker. Comparative Biochemistry and Physiology - Part C: Toxicology 124:73–81.
  • Choi J, Roche H, Caquet T. 2000. Effects of physical (hypoxia, hyperoxia) and chemical (potassium dichromate, fenitrothion) stress on antioxidant enzyme activities in Chironomus riparius Mg. (Diptera, Chironomidae) larvae: Potential biomarkers. Environmental Toxicology And Chemistry / SETAC 19:495–500.
  • Choi J, Roche H, Caquet T. 2001. Hypoxia, hyperoxia and exposure to potassium dichromate or fenitrothion alter the energy metabolism in Chironomus riparius Mg. (Diptera: Chironomidae) larvae. Comparative Biochemistry and Physiology - Part C: Toxicology 130:11–17.
  • Cossu C, Doyotte A, Babut M, Exinger A, Vasseur P. 2000. Antioxidant biomarkers in freshwater bivalves, Unio tumidus, in response to different contamination profiles of aquatic sediments. Ecotoxicology and Environmental Safety 45:106–121. DOI: 10.1006/eesa.1999.1842.
  • Cummins KW. 1962. An evaluation of some techniques for the collection and analysis of benthic samples with special emphasis on lotic waters. The American Midland Naturalist 67:477–504. DOI: 10.2307/2422722.
  • Cytryńska M, Wojda I, Jakubowicz T. 2016. How insects combat infections. In: Ballarin L, Cammarata M, editors. Lessons in immunity: From single-cell organisms to mammals. Amsterdam-Boston-Heidelberg-London-New York-Oxford-Paris-San Diego-San Francisco-Singapore-Sydney-Tokyo:.Academic Press/ Elsevier. pp. 117–128.
  • De Bisthoven LJ, Gerhardt A, Soares AMVM. 2005. Chironomidae larvae as bioindicators of an acid mine drainage in Portugal. Hydrobiologia 532:181–191. DOI: 10.1007/s10750-004-1387-z.
  • De Bisthoven LJ, Van Looy E, Ceusters R. 1992. Gullentrop,s F., Ollevier, F. Densities of Prodiamesa olivacea (Meigen) (Diptera: Chironomidae) in a second order stream, the Laan (Belgium): Relation to river dynamics. Netherlands Journal of Aquatic Ecology 26:485–490. DOI: 10.1007/BF02255279.
  • De Haas EM, Reuvers B, Moermond CTA, Koelmans AA, Kraak MHS. 2002. Responses of benthic invertebrates to combined toxicant and food input in floodplain lake sediment. Environmental Toxicology And Chemistry / SETAC 21:2165–2171. DOI: 10.1002/etc.5620211020.
  • De Haas EM, Wagner C, Koelmans AA, Kraak MHS, Admiraal W. 2006. Habitat selection by chironomid larvae: Fast growth requires fast food. Journal of Animal Research 75:148–155. DOI: 10.1111/j.1365-2656.2005.01030.x.
  • de Lafontaine Y, Gagne´ F, Blaise C, Costan G, Gagnon P, Chan HM. 2000. Biomarkers in zebra mussels (Dreissena polymorpha) for the assessment and monitoring of water quality of the St Lawrence River (Canada). Aquatic Toxicology (Amsterdam, Netherlands) 50:51–71. DOI: 10.1016/S0166-445X(99)00094-6.
  • Domingues I, Guilhermino L, Soares AMVM, Nogueira AJA. 2007. Assessing dimethoate contamination in temperate and tropical climates: Potential use of biomarkers in bioassays with two chironomid species. Chemosphere 69:145–154. DOI: 10.1016/j.chemosphere.2007.04.013.
  • Doyotte A, Cossu C, Jacquin MC, Babut M, Vasseur P. 1997. Antioxidant enzymes, glutathione and lipid peroxidation as relevant biomarkers of experimental or field exposure in the gills and the digestive gland of the freshwater bivalve Unio tumidus. Aquatic Toxicology (Amsterdam, Netherlands) 39:93–110. DOI: 10.1016/S0166-445X(97)00024-6.
  • Dziock F, Henle K, Foeckler F, Follner K, Scholz M 2006. Biological indicator systems in floodplains - a review. International Review of Hydrobiology 4:271–291. DOI: 10.1002/iroh.200510885.
  • Ellman G. 1959. Tissue sulfhydryl groups. Archives of Biochemistry and Biophysics 82:70–77. DOI: 10.1016/0003-9861(59)90090-6.
  • Gagliardi BS, Long SM, Pettigrove VJ, Hoffmann AA. 2015. The Parthenogenetic Cosmopolitan Chironomid, Paratanytarsus grimmii, as a New Standard Test Species for Ecotoxicology: Culturing Methodology and Sensitivity to Aqueous Pollutants. Bulletin of Environmental Contamination and Toxicology 95:350–356. DOI: 10.1007/s00128-015-1578-5.
  • Gallagher EP, Sheehy KM, Janssen PL, Eaton DL, Collier TK. 1998. Isolation and cloning of homologous glutathione S-transferase cDNAs from English sole and starry flounder liver. Aquatic Toxicology (Amsterdam, Netherlands) 44:171–182. DOI: 10.1016/S0166-445X(98)00077-0.
  • Goldberg ED, Bertine KK. 2000. Beyond the Mussel Watch - new directions for monitoring marine pollution. The Science of the Total Environment 247:165–174. DOI: 10.1016/S0048-9697(99)00488-X.
  • Goltermann HL, Clymos RS, Ohmstad MAM. 1978. Methods for Physical and Chemical Analysis of Fresh Water. Oxford: Blackwell Scientific Publication.
  • Guéraud F, Atalay M, Bresgen N, Cipak A, Eckl PM, Huc L, Jouanin I, Siems W, Uchida K. 2010. Chemistry and biochemistry of lipid peroxidation products. Free Radical Research 44:1098–1124. DOI: 10.3109/10715762.2010.498477.
  • Ha MH, Choi J. 2008. Effect of environmental contaminants on hemoglobin of larvae of aquatic midge. Chironomus riparius (Diptera: Chironomidae); a potential biomarker for ecotoxicity monitoring. Chemosphere 71:1928–1936. DOI: 10.1016/j.chemosphere.2008.01.018.
  • Habig WH, Pabst MJ, Jakoby WB. 1974. Glutathione S-Transferases. The first enzymatic step in mercapturic acid formation. The Journal of Biological Chemistry 249:7130–7139.
  • Halliwell B, Gutteridge J. 2007. Free radicals in biology and medicine. New York: Oxford University Press. p. 704.
  • Halpern M, Gasith A, Broza M. 2002. Does the tube of a benthic chironomid larva play a role in protecting its dweller against chemical toxicants? Hydrobiologia 470:49–55. DOI: 10.1023/A:1015665027535.
  • Hodge S, Longley M, Booth L, Heppelthwaite V, O’Halloran K. 2000. An Evaluation of Glutathione S-Transferase activity in the Tasmanian Lacewing (Micromus tasmaniae) as a Biomarker of Organophosphate Contamination. Bulletin of Environmental Contamination and Toxicology 65:8–15. DOI: 10.1007/s0012800087.
  • Huggett RJ, Kimerle RA, Mehrle PM, Bergman HL. 1992. Biomarkers. Biochemical, physiological, and histological markers of anthropogenic stress. Boca Raton, FL: Lewis Publishers.
  • Lee SW, Choi J. 2009. Multi-level ecotoxicity assay on the aquatic midge, Chironomus tentans (Diptera, Chironomidae) exposed to octachlorostyrene. Environmental Toxicology and Pharmacology 28:269–274. DOI: 10.1016/j.etap.2009.05.004.
  • Livingstone DR. 1993. Biotechnology and pollution monitoring: Use of molecular biomarkers in the aquatic environment. Journal of Chemical Technology & Biotechnology 57:195–211. DOI: 10.1002/jctb.280570302.
  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. 1951. Protein measurement with the Folin phenol reagent. The Journal of Biological Chemistry 193:265–275.
  • Lushchak VI. 2012. Glutathione homeostasis and functions: Potential targets for medical interventions. Journal of Amino Acids 2012(Article ID 736837):26. DOI: 10.1155/2012/736837.
  • Marziali L, Lencioni V, Rossaro B. 2006. Adaptations of pupae of Chironomidae (Insecta: Diptera) to oxygen-poor habitats. Polish Journal of Ecology 54:687–693.
  • Marziali L, Rossaro B. 2013. Response of chironomid species (Diptera, Chironomidae) to water temperature: Effects on species distribution in specific habitats. Journal of Entomological and Acarological Research 45:73–89. DOI: 10.4081/jear.2013.e14.
  • McLoughlin N, Yin D, Maltby L, Wood RM, Yu H. 2000. Evaluation of sensitivity and specificity of two crustacean biochemical biomarkers. Environmental Toxicology And Chemistry / SETAC 19:2085–2092. DOI: 10.1002/etc.5620190818.
  • Melgar Riol MJ, Novoa Valinas MC, Garcia Fernandez MA, Perez Lopez M. 2001. Glutathione S-transferases from rainbow trout liver and freshly isolated hepatocytes: Purification and characterization. Comparative Biochemistry and Physiology - Part C: Toxicology 128:227–235. DOI: 10.1016/s1532-0456(00)00196-4.
  • Meregalli G, Vermeulen ACV, Ollevier F. 2000. The use of chironomid deformation in an in situ test for sediment toxicity. Ecotoxicology and Environmental Safety 47:231–238. DOI: 10.1006/eesa.2000.1981.
  • Mohanty D, Luna S. 2016. Multivariate analysis of potential biomarkers of oxidative stress in Notopterus notopterus tissues from Mahanadi River as a function of concentration of heavy metals. Chemosphere 155:28–38. DOI: 10.1016/j.chemosphere.2016.04.035.
  • Mousavi SK, Primicerio R, Amundsen PA. 2003. Diversity and structure of Chironomidae (Diptera) communities along a gradient of heavy metal contamination in a subarctic watercourse. The Science of the Total Environment 307:93–110. DOI: 10.1016/S0048-9697(02)00465-5.
  • Negishi JN, Nagayama S, Kume M. 2013. Unionoid mussels as an indicator of fish communities: A conceptual framework and empirical evidence. Ecological Indicators 24:127–137. DOI: 10.1016/j.ecolind.2012.05.029.
  • Negre-Salvayre A, Auge N, Ayala V, Basaga H, Boada J, Brenke R, et al. 2010. Pathological aspects of lipid peroxidation. Free Radical Research 44:1125–1171. DOI: 10.3109/10715762.2010.498478.
  • Newman MC. 1998. Fundamentals of ecotoxicology. Chelsea, MI: Sleeping Bear/Ann Arbor Press.
  • Nowak C, Vogt C, Diogo JB, Schwenk K. 2007. Genetic impoverishment in laboratory cultures of the test organism Chironomus riparius. Environmental Toxicology and Chemistry 26:1018–1022. DOI: 10.1897/06-349R.1.
  • Osman A, Wuertz S, Mekkawy I, Exner H, Kirschbaum F. 2007. Lead Induced Malformations in Embryos of the African Catfish Clarias gariepinus (Burchell, 1822). Environmental Toxicology 22:375–389. DOI: 10.1002/tox.20272.
  • Osmulski PA, Leyko W. 1986. Structure, function and physiological role of Chironomus haemoglobin. Comparative Biochemistry and Physiology B 85B:701–722. DOI: 10.1016/0305-0491(86)90166-5.
  • Palacio-Cortes AM, Signorini-Souza IDL, Hara ELY, Disner RG, Rebechi D, Grassi MT, et al. 2017. Polybrominated diphenyl ethers (PBDEs) effects on Chironomus sancticaroli larvae after short-term exposure. Ecotoxicology and Environmental Safety 139:308–315. DOI: 10.1016/j.ecoenv.2017.01.052.
  • Pander J, Geist J. 2013. Ecological indicators for stream restoration success. Ecological Indicators 30:106–118. DOI: 10.1016/j.ecolind.2013.01.039.
  • Péry ARR, Garric J. 2006. Modelling effects of temperature and feeding level on the life cycle of the midge Chironomus riparius: An energy-based modelling approach. Hydrobiologia 553:59–66. DOI: 10.1007/s10750-005-1284-0.
  • Petersen RC, Cummins KW, Ward GM. 1989. Microbial and animal processing of detritus in a woodland stream. Ecological Monographs 59:21–39. DOI: 10.2307/2937290.
  • Porter DL. 1971. Oogenesis and chromosomal heterozygosity in the thelytokous midge, Lundstroemia parthenogenetica (Diptera, Chironomidae). Chromosoma 32:332–342. DOI: 10.1007/BF00284841.
  • Quinn JM, Hickey CW. 1990. Characterization and classification of benthic invertebrate communities in 88 New Zealand rivers in relation to environmental factors. New Zealand Journal of Marine and Freshwater Research 24:387–409. DOI: 10.1080/00288330.1990.9516432.
  • Rasmussen JB. 1985. Effects of density and microdetritus enrichment on the growth of chironomid larvae in a small pond. Canadian JJournal of Fisheries and Aquatic Sciences 42:1418–1422. DOI: 10.1139/f85-177.
  • Rebechi D, Navarro-Silva MA. 2012. Setting the reference for the use of Chironomus sancticaroli (Diptera: Chironomidae) as bioindicator: Ontogenetic pattern of larval head structures. Zoologia (Curitiba) 29:167–171.
  • Rosenberg DM. 1992. Freshwater biomonitoring and Chironomidae. Netherlands Journal of Aquatic Ecology 26:101–122. DOI: 10.1007/BF02255231.
  • Saether OA. 1979. Chironomid communities as water quality indicators. Holarctic Ecology 2:65–74.
  • Sasikumar G, Krishnakumar PK. 2011. Aquaculture planning for suspended bivalve farming systems: The integration of physiological response of green mussel with environmental variability in site selection. Ecological Indicators 11:734–740. DOI: 10.1016/j.ecolind.2010.06.008.
  • Schneider S, Lindstrøm EA. 2009. Bioindication in Norwegian rivers using non-diatomaceous benthic algae: The acidification index periphyton (AIP). Ecological Indicators 9:1206–1211. DOI: 10.1016/j.ecolind.2009.02.008.
  • Servia MJ, Cobo F, Gonzalez MA. 1998. Deformities in larval Prodiamesa olivacea (Meigen, 1818) (Diptera, Chironomidae) and their use as bioindicators of toxic sediment stress. Hydrobiology 385:153–162. DOI: 10.1023/A:1003466012110.
  • Sheehan D, Power A. 1999. Effects of seasonality on xenobiotic and antioxidant defence mechanisms of bivalve molluscs. Comparative Biochemistry and Physiology - Part C: Toxicology 123:193–199. DOI: 10.1016/s0742-8413(99)00033-x.
  • Słowińska M, Nynca J, Wilde J, Bąk B, Siuda M, Ciereszko A. 2016. Total antioxidant capacity of honeybee haemolymph in relation to age and exposure to pesticide, and comparison to antioxidant capacity of seminal plasma. Apidologie 47:227–236. DOI: 10.1007/s13592-015-0391-9.
  • StatSoft Inc. Statistica (data analysis software system), version 10. Avaiable at: http://www.statsoft.com (2011).
  • Stocks J, Dormandy T. 1971. The Autoxidation of Human Red Cell Lipids Induced by Hydrogen Peroxide. British Journal of Haematology 20:95–111. DOI: 10.1111/j.1365-2141.1971.tb00790.x.
  • Valavanidis A, Vlahogianni T, Dassenakis M, Scoullos M. 2006. Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotoxicology and Environmental Safety 64(9):178–189. DOI: 10.1016/j.ecoenv.2005.03.013.
  • Vallenduuk HJ, Moller Pillot HKM. 2007. Chironomidae Larvae of the Netherlands and Adjacent Lowlands. General Ecology and Tanypodinae. Zeist: KNNV Publishing.
  • Van der Oost R, Vindimian E, van den Brink P, Satumalay K, Heida H, Vermeulen NPE. 1997. Biomonitoring aquatic pollution with feral eel (Anguilla anguilla): III. Statistical analyses of relationships between contaminant exposure and biomarkers. Aquatic Toxicology (Amsterdam, Netherlands) 39:45–75. DOI: 10.1016/S0166-445X(96)00851-X.
  • Vertuani S, Angusti A, Manfredini S. 2004. The antioxidants and pro-antioxidants network: An overview. Current Pharmaceutical 10:1677–1694. DOI: 10.2174/1381612043384655.
  • Viarengo A, Lowe D, Bolognesi C, Fabbri E, Koehler A. 2007. The use of biomarkers In biomonitoring: A 2-tier approach assessing the level of pollutant-induced stress syndrome in sentinel organisms. Home Journals Comparative Biochemistry and Physiology - Part C: Toxicology & Pharmacology 146:281–300.
  • Weltje L, Rufli H, Heimbach F, Wheeler J, Vervliet Scheebaum M, Hamer M. 2010. The chironomid acute toxicity test: Development of a new test system. Integrated Environmental Assessment and Management 6:301–307. DOI: 10.1897/IEAM_2009-069.1.
  • Wiederholm T, ed. 1983. The larvae of Chironomidae (Diptera) of the Holartcic region - Keys and diagnoses. Scandinavian Entomology 19:1–457.
  • Wiederholm T, ed. 1986. The pupae of Chironomidae (Diptera) of the Holarctic region - Keys and diagnoses. Scandinavian Entomology 28:1–482.
  • Wiederholm T, ed. 1989. The adult males of Chironomidae (Diptera) of the Holarctic region - Keys and diagnoses. Scandinavian Entomology 34:1–532.
  • Wiegand C, Plussmacher S. 2005. Ecological effects of selected cyanobacterial secondary metabolites: A short review. Toxicology and Applied Pharmacology 203:201–218. DOI: 10.1016/j.taap.2004.11.002.
  • Winner RW, Boesel MW, Farrell MP. 1980. Insect community structure as an index of heavy-metal pollution in lotic ecosystems. Canadian JJournal of Fisheries and Aquatic Sciences 37:647–655. DOI: 10.1139/f80-081.
  • Wojtal-Frankiewicz A, Bernasinska J, Frankiewicz P, Gwoździnski K, Jurczak T. 2017. The role of environmental factors in the induction of oxidative stress in zebra mussel (Dreissena polymorpha). Aquatic Ecology 51:289–306. DOI: 10.1007/s10452-017-9617-4.
  • Wojtal-Frankiewicz A, Bernasinska J, Jurczak T, Gwoździnski K, Frankiewicz P, Wielanek M. 2013. Microcystin assimilation and detoxification by Daphnia spp. in two ecosystems of different cyanotoxin concentrations. Journal of Limnology 72:154–171. DOI: 10.4081/jlimnol.2013.e13.