Cholinesterase and glutathione-S-transferase activities in freshwater invertebrates as biomarkers to assess pesticide contamination

Environmental Toxicology and Chemistry

Volumn 29, Issue 1, 2010, Pages 5-18

  Domingues, Inês ^a   Agra, Ana Raquel ^a   Monaghan, Kieran ^a   Soares, Amadeu M V M ^a   Nogueira, António J A ^a  

^a UNIVERSITY OF AVEIRO   (Portugal)

Author keywords

Biomarkers; Cholinesterase; Glutathione S transferase; Pesticide risk assessment

Indexed keywords

ANIMALS; PESTICIDES; RISK ASSESSMENT; RISK MANAGEMENT; TOXICITY;

AQUATIC INVERTEBRATES; AQUATIC SYSTEM; BIOMARKER RESPONSE; BIOMONITORING; BIOTIC FACTORS; ECOLOGICAL RELEVANCE; ENVIRONMENTAL CONTAMINANT; FRESHWATER INVERTEBRATES; GLUTATHIONE-S-TRANSFERASE; IN-SITU; PESTICIDE RISK ASSESSMENT;

BIOMARKERS;

AZINPHOS METHYL; BIOLOGICAL MARKER; CARBAMIC ACID; CHLORPYRIFOS; CHOLINESTERASE; DIMPYLATE; FRESH WATER; GLUTATHIONE TRANSFERASE; ORGANOPHOSPHATE PESTICIDE; PESTICIDE; PIPERONIL BUTOXIDE; PYRETHROID; TRIAZINE; UNCLASSIFIED DRUG; WATER POLLUTANT;

AQUATIC ORGANISM; BIOMARKER; BIOMONITORING; BIOTIC FACTOR; ENZYME ACTIVITY; FRESHWATER ECOSYSTEM; INVERTEBRATE; PESTICIDE; RISK ASSESSMENT; TOXICITY; TOXIN;

ANNELID WORM; CRUSTACEA; ENVIRONMENTAL FACTOR; ENZYME ACTIVITY; IN SITU HYBRIDIZATION; INSECT; INTRASPECIFIC VARIATION; INVERTEBRATE; MOLLUSC; MONITORING; NONHUMAN; PHYSICAL CHEMISTRY; POLLUTION; PRIORITY JOURNAL; REVIEW; TOXICOLOGICAL PARAMETERS; ANIMAL; ENVIRONMENTAL MONITORING; ENZYMOLOGY; METABOLISM; PROCEDURES; RISK ASSESSMENT; TOXICITY; WATER POLLUTANT;

INVERTEBRATA;

ANIMALS; BIOLOGICAL MARKERS; CHOLINESTERASES; ENVIRONMENTAL MONITORING; FRESH WATER; GLUTATHIONE TRANSFERASE; INVERTEBRATES; PESTICIDES; RISK ASSESSMENT; WATER POLLUTANTS, CHEMICAL;

EID: 77952309945     PISSN: 07307268     EISSN: 15528618     Source Type: Journal    
DOI: 10.1002/etc.23     Document Type: Review

References (122)

1. Mel'nikov NN. 1968. The trend in the development of pesticide production and application. Zhurnal Vsesoiuznogo Khimicheskogo Obshchestva im. D. I. Mendeleeva 13: 248-262.
2. Lagadic L. 2002. Biomarkers: Useful tools for the monitoring of aquatic environments. Rev Med Vet 153: 581-588.
3. Huggett RJ, Kimerle RA, Mehrle PMJ, Bergman HL. 1992. Biomarkers: Biochemical, Physiological and Histological Markersof Anthropogenic Stress. Lewis, Boca Raton, FL, USA.
4. McLoughlin N, Yin D, Maltby L, Wood RM, Yu H. 2000. Evaluation of sensitivity and specificity of two crustacean biochemical biomarkers. Environ Toxicol Chem 19: 2085-2092.
5. McCarty LS, Power M, Munkittrick KR. 2002. Bioindicators versus biomarkers in ecological risk assessment. Hum Ecol Risk Assess 8: 159-164.
6. National Research Council Committee on Biological Markers. 1987. Biological markers in environmental health research. Environ Health Perspect 74: 3-9.
7. Adams SM, Giesy JP, Tremblay LA, Eason CT. 2001. The use of biomarkers in ecological risk assessment: Recommendations from the Christ Church Conferenceon Biomarkers in Ecotoxicology. Biomarkers 6: 1-6.
8. McCarty LS, Munkittrick KR. 1996. Environmental biomarkers in aquatic toxicology: Fiction, fantasyorfunctional? Hum Ecol Risk Assess 2: 268-274.
9. Garcia LM, Castro B, Ribeiro R, Guilhermino L. 2000. Characterization of cholinesterase from guppy (Poecilia reticulata) muscle and its in vitro inhibition by environmental contaminants. Biomarkers 5: 274-284.
10. Galloway TS, Handy R. 2003. Immunotoxicity of organophosphorous pesticides. Ecotoxicology 12: 345-363.
11. Olsen T, Ellerbeck L, Fisher T, Callaghan A, Crane M. 2001. Variability in acetylcholinesterase and glutathione-S-transferase activities in Chironomus riparius Meigen deployed in situ at uncontaminated field sites. Environ Toxicol Chem 20: 1725-1732.
12. Hyne RV, Maher WA. 2003. Invertebrate biomarkers: Links to toxicosis that predict population decline. Ecotoxicol Environ Saf 54: 366-374.
13. Enayati AA, Ranson H, Hemingway J. 2005. Insect glutathione transferases and insecticide resistance. Insect Mol Biol 14: 3-8.
14. 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: 169 169-180.
15. Vidal M-L, Basseres A, Narbonne J-F. 2002. Influence of temperature, pH, oxygenation, water-type and substrate on biomarker responses in the freshwater clam Corbicula fluminea (Muller). Comp Biochem Physiol C 132: 93-104.
16. Robillard S, Beauchamp G, Laulier M. 2003. The role of abiotic factors and pesticide levels on enzymatic activity in the freshwater mussel Anodonta cygnea at three different exposure sites. Comp Biochem Physiol C 135: 49-59.
17. Timofeyev MA. 2006. Antioxidant enzyme activity in endemic Baikalean versus Palaearctic amphipods: Tagma-and size-related changes. Comp Biochem Physiol B 143: 302-308.
18. Guilhermino L, Lopes MC, Carvalho AP, Soares AMVM. 1996. Acetylcholinesterase activity in juvenile Daphnia magna strauss. Bull Environ Contam Toxicol 57: 979-985.
19. Printes LB, Callaghan A. 2003. Intraclonal variability in Daphnia acetylcholinesterase activity: The implications for its applicability as a biomarker. Environ Toxicol Chem 22: 2042-2047.
20. Bhavan PS, Geraldine P. 2001. Biochemical stress responsesintissuesof the prawn Macrobrachium malcolmsonii on exposure to endosulfan. Pestic Biochem Physiol 70: 27-41.
21. Mora P, Michel X, Narbonne JF. 1999. Cholinesterase activity as potential biomarker intwo bivalves. Environ Toxicol Pharmacol 7: 253-260.
22. Chang C-C, Lee P-P, Hsu J-P, Yeh S-P, Cheng W. 2006. Survival, and biochemical, physiological, and histopathological responses of the giant freshwater prawn, Macrobrachium rosenbergii, to shortterm trichlorfon exposure. Aquaculture 253: 653-666.
23. Beauvais SL, Atchison GJ, Stenback JZ, Crumpton WG. 1999. Use of cholinesterase activity to monitor exposure of Chironomus riparius (Diptera: Chironomidae) to a pesticide mixture in hypoxic wetland mesocosms. Hydrobiologia 416: 163-170.
24. Choi J, Roche H, Caquet T. 1999. Characterization of superoxide dismutase activity in Chironomus riparius Mg. (Diptera, Chironomidae) larvae. A potential biomarker. Comp Biochem Physiol C 124: 73-81.
25. Vidal M-L, Basseres A, Narbonne J-F. 2002. Influence of temperature, pH, oxygenation, water-type and substrate on biomarker responses in the freshwater clam Corbicula fluminea (Muller). Comp Biochem Physiol C 132: 93-104.
26. Domingues I, Guilhermino L, Soares A, 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.
27. Moulton CA, Fleming WJ, Purnell CE. 1996. Effects of two cholinesterase-inhibiting pesticides on freshwater mussels. Environ Toxicol Chem 15: 131-137.
28. Callaghan A, Fisher TC, Grosso A, Holloway GJ, Crane M. 2002. Effect of temperature and pirimiphos methyl on biochemical biomarkers in Chironomus riparius Meigen. Ecotoxicol Environ Saf 52: 128-133.
29. Kristoff G, Guerrero NV, de D'Angelo AMP, Cochon AC. 2006. Inhibition of cholinesterase activity by azinphos-methyl in two freshwater invertebrates: Biomphalaria glabrata and Lumbriculus variegatus. Toxicology 222: 185-194.
30. Guilhermino L, Lopes MC, Carvalho AP, Soares AMVM. 1996. Inhibition of acetylcholinesterase activity as effect criterion in acute test with juvenile Daphnia magna. Chemosphere 32: 727-738.
31. Sturm A, Hansen P-D. 1999. Alteredcholinesteraseandmonooxygenase levels in Daphnia magna and Chironomus riparius exposed to environmental pollutants. Ecotoxicol Environ Saf 42: 9-15.
32. Printes LB, Callaghan A. 2004. A comparative study on the relationship between acetylcholinesterase activity and acute toxicity in Daphnia magna exposed to anticholinesterase insecticides. Environ Toxicol Chem 23: 1241-1247.
33. Barata C, Solayan A, Porte C. 2004. Role of B-esterases in assessing toxicity of organophosphorus (chlorpyrifos, malathion) and carbamate (carbofuran) pesticides to Daphnia magna. Aquat Toxicol 66: 125-139.
34. Barata C, Baird DJ, Soares AMVM, Guilhermino L. 2001. Biochemical factors contributing to response variation among resistant and sensitive clones of Daphnia magna Straus exposed to ethyl parathion. Ecotoxicol Environ Saf 49: 155-163.
35. Steevens JA, Benson WH. 1999. Toxicological interactions of chlorpyrifos and methyl mercury in the amphipod, Hyalella azteca. Toxicol Sci 52: 168-177.
36. Escartin E, Porte C. 1996. Acetylcholinesterase inhibition in the crayfish Procambarus clarkii exposed to fenitrothion. Ecotoxicol Environ Saf 34: 160-164.
37. Rider CV, LeBlanc GA. 2005. An integrated addition and interaction model for assessing toxicity of chemical mixtures. Toxicol Sci 87: 520-528.
38. Crane M, Sildanchandra W, Kheir R, Callaghan A. 2002. Relationship between biomarker activity and developmental endpoints in Chironomus riparius Meigen exposed to an organophosphate insecticide. Ecotoxicol Environ Saf 53: 361-369.
39. Day KE, Scott IM. 2002. Use of acetylcholinesterase activity to detect sublethal toxicity in stream invertebrates exposed to low concentrations of organophosphate insecticides. Aquatic Toxicol 18: 101-114.
40. Brewer SK, Atchison GJ. 1999. The effects of chlorpyrifos on cholinesterase activity and foraging behavior in the dragonfly, Anax junius (Odonata). Hydrobiologia 394: 201-208.
41. Maycock DS, Prenner MM, Kheir R, Morris S, Callaghan A, Whitehouse P, Morritt D, Crane M. 2003. Incorporation of in situ and biomarker assays in higher-tier assessment of the aquatic toxicity of insecticides. Water Res 37: 4180-4190.
42. Ibrahim H, Kheir R, Helmi S, Lewis J, Crane M. 1998. Effects of organophosphorus, carbamate, pyrethroid and organochlorine pesticides, and a heavy metal on survival and cholinesterase activity of Chironomus riparius Meigen. Bull Environ Contam Toxicol 60: 448-455.
43. Kheir R, Ibrahim H, Lewis J, Callaghan A, Crane M. 2001. Comparison of acetylcholinesterase and glutathione-S-transferase activity in Chironomus riparius Meigen exposed to chemical-spiked sediments. Bull Environ Contam Toxicol 66: 603-610.
44. Moreira-Santos M, Fonseca AL, Moreira SM, Osten JR-V, Silva EMd, Soares AMVM, Guilhermino L, Ribeiro R. 2005. Short-term sublethal (sediment and aquatic roots of floating macrophytes) assays with a tropical chironomid based on postexposure feeding and biomarkers. Environ Toxicol Chem 24: 2234-2242.
45. Jin-Clark Lydy MJ, Zhu KY. 2001. Effects of atrazine and cyanazine on chlorpyrifos toxicity in Chironomus tentans (Diptera: Chironomidae). Environ Toxicol Chem 21: 598-603.
46. Doran WJ, Cope WG, Rada RG, Sandheinrich MB. 2001. Acetylcholinesterase inhibition in the threeridge mussel (Amblema plicata) by chlorpyrifos: Implications for biomonitoring. Ecotoxicol Environ Saf 49: 91-98.
47. Oneto ML, Basack SB, Casabe NB, Fuchs JS, Kesten EM. 2005. Biological responses in the freshwater bivalve Corbicula fluminea and the earthworm Eiseniafetida exposed to fenitrothion. Fresenius Environ Bull 14: 716-720.
48. Mora BR, Martinez-Tabche L, Sanchez-Hidalgo E, Hernandez GC, Ruiz MCG, Murrieta FF. 2000. Relationship between toxicokinetics of carbaryl and effect on acetylcholinesterase activity in Pomacea patula snail. Ecotoxicol Environ Saf 46: 234-239.
49. Cooper NL, Bidwell JR. 2006. Cholinesterase inhibition and impacts on behavior of the Asian clam, Corbicula fluminea, after exposure to an organophosphate insecticide. Aquat Toxicol 76: 258-267.
50. Mora P, Fournier D, Narbonne J F. 1999. Cholinesterases from the marine mussels Mytilus galloprovincialis Lmk.and M-edulis L. and from the freshwater bivalve Corbiculafluminea Muller. Comp Biochem Physiol C 122: 353-361.
51. Lagadic L, Caquet T, Ramade F. 1994. The role of biomarkers in environmental assessment (5). Invertebrate populations and communities. Ecotoxicology (Historical Archive) 3: 193-208.
52. Bond J-A, Bradley BP. 1997. Resistance to malathion in heat shocked Daphnia magna. Environ Toxicol Chem 16: 705-712.
53. Barata C, Varo I, Navarro JC, Arun S, Porte C. 2005. Antioxidant enzyme activities and lipid peroxidation in the freshwater cladoceran Daphnia magna exposed to redox cycling compounds. Comp Biochem Physiol C 140: 175-186.
54. Mosleh YY, Paris-Palacios S, Couderchet M, Biagianti-Risbourg S, Vernet G. 2005. Effects of the herbicide isoproturon on metallothioneins, growth, and antioxidative defenses in the aquatic worm Tubifex tubifex (Oligochaeta, Tubificidae). Ecotoxicology 14: 559-571.
55. Boyer S, David J-P, Rey D, Lemperiere G, Ravanel P. 2006. Response of Aedes aegypti (Diptera: Culicidae) larvae to three xenobiotic exposures: Larval tolerance and detoxifying enzyme activities. Environ Toxicol Chem 25: 470-476.
56. Berra E, Forcella M, Giacchini R, Rossaro B, Parenti P. 2006. Biomarkers in caddisfly larvae of the species Hydropsyche pellucidula (Curtis, 1834) (Trichoptera: Hydropsychidae) measured in natural populations and after short term exposure to fenitrothion. Bull Environ Contam Toxicol 76: 863-870.
57. 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. Environ Toxicol Chem 19: 495-500.
58. Hirthe G, Fisher TC, Crane M, Callaghan A. 2001. Short-term exposure to sub-lethal doses of lindane affects developmental parameters in Chironomus riparius Meigen, but has no effect on larval glutathione-S-transferase activity. Chemosphere 44: 583-589.
59. Baturo W, Lagadic L. 1996. Benzo[a]pyrene hydrixylase and glutathione-S-transferase activities as biomarkers in Lumnaea palustris (Mollusca, Gastropoda) exposed to atrazine and hexachlorobenzene in freshwater mesocosms. Environ Toxicol Chem 15: 771-781.
60. Looise BAS, Holwerda DA, Foekema EM. 1996. Induction of glutathione-S-transferase in the freshwater bivalve Sphaerium corneum as a biomarker for short-term toxicity tests? Comp Biochem Physiol C 113: 103-107.
61. Wu RSS, Siu WHL, Shin PKS. 2005. Induction, adaptation and recovery of biological responses: Implications for environmental monitoring. Mar. Pollut Bull 51: 623-634.
62. Thompson HM. 1999. Esterases as markers of exposure to organophosphates and carbamates. Ecotoxicology 8: 369-384.
63. Andersen TH, Tjornhoj R, Wollenberger L, Slothuus T, Baun A. 2006. Acute and chronic effects of pulse exposure of Daphnia magna to dimethoate and pirimicarb. Environ Toxicol Chem 25: 1187-1195.
64. Zhao Y, Newman MC. 2006. Effects of exposure duration and recovery time during pulsed exposures. Environ Toxicol Chem 25: 1298-1304.
65. Naddy RB, Johnson KA, Klaine SJ. 2000. Response of Daphnia magna to pulsed exposures of chlorpyrifos. Environ Toxicol Chem 19: 423-431.
66. Naddy RB, Klaine SJ. 2001. Effect of pulse frequency and interval on the toxicity of chlorpyrifos to Daphnia magna. Chemosphere 45: 497-506.
67. Kallander DB, Fisher SW, Lydy MJ. 1997. Recovery following pulsed exposure to organophosphorus and carbamate insecticides in the midge, Chironomus riparius. Arch Environ Contam Toxicol 33: 29-33.
68. Duquesne S, Reynaldi S, Liess M. 2006. Effects of the organophosphate paraoxon-methyl on survival and reproduction of Daphnia magna: Importance of exposure duration and recovery. Environ Toxicol Chem 25: 1196-1199.
69. Kendall RJ, Anderson TA, Baker RJ, Bens CM, Carr JA, Chiodo LA, Cobb GP III, Dickerson RL, Dixon KR, Fram LT, Hooper MJ, Martin CF, McMurry ST, Patino R, Smith EE, Theodorakis CW. 2001. Ecotoxicology. In Klaassen CD, ed, Casarettand Doull' s Toxicology: The Basic Science of Poisons. McGraw-Hill, New York, NY, USA, pp 1013-1045.
70. Scholz NL, Hopkins WA. 2006. Ecotoxicology of anticholinesterase pesticides: Data gaps and research challenges. Environ Toxicol Chem 25: 1185-1186.
71. Crane M, Attwood C, Sheahan D, Morris S. 1999. Toxicity and bioavailability of the organophosphorus insecticide pirimiphos methyl to the freshwater amphipod Gammarus pulex L-in laboratory and mesocosm systems. Environ Toxicol Chem 18: 1456-1461.
72. Callaghan A, Hirthe G, Fisher T, Crane M. 2001. Effect of short-term exposure to chlorpyrifos on developmental parameters and biochemical biomarkers in Chironomus riparius Meigen. Ecotoxicol Environ Saf 50: 19-24.
73. Tessier L, Boisvert JL, Vought LBM, Lacoursiere JO. 2000. Anomalies on capture nets of Hydropsyche slossonae larvae (Trichoptera; Hydropsychidae), a potential indicator of chronic toxicity of malathion (organophosphate insecticide). Aquat Toxicol 50: 125-139.
74. Cuppen JG, Crum SJH, Heuvel HHVD, Smidt RA, Brink PJVD. 2002. Effects of a mixture of two insecticides in freshwater microcosms: I. Fate of chlorpyrifos and lindane and responses of macroinvertebrates. Ecotoxicology 11: 165-180.
75. Van der Hoeven N, Gerritsen AAM. 1997. Effects of chlorpyrifos on individuals and populations of Daphniapulex in the laboratory and field. Environ Toxicol Chem 16: 2438-2447.
76. Van Leeuwen CJ. 1995. Ecotoxicological effects. In Van Leeuwen CJ, Hermens JLM, eds, Risk Assessment of Chemicals: An Introduction. Kluwer Academic, Dordrecht, The Netherlands, pp 175-222.
77. Backhaus T, Altenburger R, Boedeker W, Faust M, Scholze M, Grimme LH. 2000. Predictability of the toxicity of a multiple mixture of dissimilarly acting chemicals to Vibrio fischeri. Environ Toxicol Chem 19: 2348-2356.
78. Choi JH, Caquet T, Roche H. 2002. Multilevel effects of sublethal fenitrothion exposure in Chironomus riparius Mg. (Diptera, Chironomidae) larvae. Environ Toxicol Chem 21: 2725-2730.
79. Faust M, Altenburger R, Backhaus T, Blanck H, Boedeker W, Gramatica P, Hamer V, Scholze M, Vighi M, Grimme LH. 2001. Predictingthejoint algal toxicity of multi-component s-triazine mixtures at low-effect concentrations of individual toxicants. Aquat Toxicol 56: 13-32.
80. Van den Brink PJ, Hartgers EM, Gylstra R, Bransen F, Brock TCM. 2002. Effects of a mixture of two insecticides in freshwater microcosms: II. Responses of plankton and ecological risk assessment. Ecotoxicology 11: 181-197.
81. Faust M, Altenburger R, Backhaus T, Blanck H, Boedeker W, Gramatica P, Hamer V, Scholze M, Vighi M, Grimme LH. 2003. Joint algal toxicity of 16 dissimilarly acting chemicals is predictable by the concept of independent action. Aquat Toxicol 63: 43-63.
82. Lydy M, Belden J, Wheelock CE, Hammock BD, Denton D. 2004. Challenges in regulating pesticides mixtures. Ecology and Society 9: 1.
83. Belden JB, Gilliom RJ, Lydy MJ. 2007. How well can we predict the toxicity of pesticide mixtures to aquatic life? IEAM 3: 364-372.
84. Lydy MJ, Austin KR. 2004. Toxicity assessment of pesticide mixtures typical of the Sacramento-San Joaquim delta using Chironomus tentans. Arch Environ Contam Toxicol 48: 49-55.
85. Bailey HC, Miller JL, Miller MJ, Wiborg LC, Deanovic L, Shed T. 1997. Joint acute toxicity of diazinon and chlorpyrifos to Ceriodaphnia dubia. Environ Toxicol Chem 16: 2304-2308.
86. Woods M, Kumar A, Correll R. 2002. Acute toxicity of mixtures of chlorpyrifos, profenofos, and endosulfan to Ceriodaphnia dubia. Bull Environ Contam Toxicol 68: 801-808.
87. Belden JB, Lydy MJ. 2006. Joint toxicity of chlorpyrifos and esfenvalerate to fathead minnows and midge larvae. Environ Toxicol Chem 25: 623-629.
88. Tripathi AM, Agarwal RA. 1998. Molluscicidal and anti-AChE activity of tertiary mixtures of pesticides. Arch Environ Contam Toxicol 34: 271-274.
89. Corbel V, Chandre F, Darriet F, Lardeux F, Hougard JM. 2003. Synergism between permethrin and propoxur against Culex quinquefasciatus mosquito larvae. Med Vet Entomol 17: 158-164.
90. Mueller-Beilschmidt D. 1990. Toxicology and environmental fate of synthetic pyrethroids. J Pestic Reform 10: 32-37.
91. Anderson TD, Lydy MJ. 2002. Increased toxicity to invertebrates associated with a mixture of atrazine and organophosphate insecticides. Environ Toxicol Chem 21: 1507-1514.
92. Pape Lindstrom PA, Lydy MJ. 1997. Synergistic toxicity of atrazine and organophosphate insecticides contravenes the response addition mixture model. Environ Toxicol Chem 16: 2415-2420.
93. Belden JB, Lydy MJ. 2000. Impact of atrazine on organophosphate insecticide toxicity. Environ Toxicol Chem 19: 2266-2274.
94. Schuler L, Trimble A, Belden J, Lydy M. 2005. Joint toxicity of triazine herbicides and organophosphate insecticides to the midge Chironomus tentans. Arch Environ Contam Toxicol 49: 173-177.
95. Anderson TD, Zhu KY. 2004. Synergistic and antagonistic effects of atrazine on the toxicity of organophosphorodithioate and organophosphorothioate insecticides to Chironomus tentans (Diptera: Chironomidae). Pestic Biochem Physiol 80: 54-64.
96. Belden JB, Lydy MJ. 2001. Effects of atrazine on acetylcholinesterase activity in midges (Chironomus tentans) exposed to organophosphorus insecticides. Chemosphere 44: 1685-1689.
97. Miota F, Siegfried BD, Scharf ME, Lydy MJ. 2000. Atrazine induction of cytochrome P450 in Chironomus tentans larvae. Chemosphere 40: 285-291.
98. Londono DK, Siegfried BD, Lydy MJ. 2004. Atrazine induction of a family 4 cytochrome P450 gene in Chironomus tentans (Diptera: Chironomidae). Chemosphere 56: 701-706.
99. Ankley GT, Collyard SA. 1995. Influence of piperonyl butoxide on the toxicity of organophosphate insecticides to 3 species of fresh-water benthic invertebrates. Comp Biochem Physiol C 110: 149-155.
100. El-Merhibi A, Kumar A, Smeaton T. 2004. Role of piperonyl butoxide in the toxicity of chlorpyrifos to Ceriodaphnia dubia and Xenopus laevis. Ecotoxicol Environ Saf 57: 202-212.
101. Ankley GT, Dierkes JR, Jensen DA, Peterson GS. 1991. Piperonyl butoxide as a tool in aquatic toxicological research with organophosphate insecticides. Ecotoxicol Environ Saf 21: 266-274.
102. Corbel V, Raymond M, Chandre F, Darriet F, Hougard JM. 2003. Efficacy of insecticide mixtures against larvae of Culex quinquefasciatus (Say) (Diptera: Culicidae) resistant to pyrethroids and carbamates. Pestic Manag Sci 60: 375-380.
103. Denton DL, Wheelock CE, Murray SA, Deanovic LA, Hammock BD, Hinton DE. 2003. Joint acute toxicity of esfenvalerate and diazinon to larval fathead minnows (Pimephalespromelas). Environ Toxicol Chem 22: 336-341.
104. Amweg EL, Weston DP, Johnson CS, You J, Lydy MJ. 2006. Effect of piperonyl butoxide on permethrin toxicity in the amphipod Hyalella azteca. Environ Toxicol Chem 25: 1817-1825.
105. Fleming WJ, Augspurger TP, Alderman JA. 1995. Fresh-water mussel die-off attributed to anticholinesterase poisoning. Environ Toxicol Chem 14: 877-879.
106. Wepener V, Vuren JHJ, Chatiza FP, Mbizi Z, Slabbert L, Masola B. 2005. Active biomonitoring in freshwater environments: Early warning signals from biomarkers in assessing biological effects of diffuse sources of pollutants. Physics and Chemistry of the Earth 30: 751-761.
107. Crane M, Delaney P, Watson S, Parker P, Walker C. 1995. Theeffectof malathion 60 on Gammarus pulex (L.) below watercress beds. Environ Toxicol Chem 14: 1181-1188.
108. Domingues I, Satapornvanit K, Yakupitiyage A, Soares A, Nogueira AJA. 2008. In situ assay with the midge Kiefferulus calligaster for contamination evaluation in aquatic agro-systems in central Thailand. Chemosphere 71: 1877-1887.
109. Crane M, Delaney P, Mainstone C, Clarke S. 1995. Measurement by in situ bioassay of water quality in an agricultural catchment. Water Res 29: 2441-2448.
110. Munawar M, Munawar IF, Mayfield CI, McCarthy LH. 1989. Probing ecosystem health-A multi-disciplinary and multi-trophic assay strategy. Hydrobiologia 188: 93-115.
111. Vidal M-L, Basseres A, Narbonne J-F. 2001. Interest of a multibiomarker approach in the assessment of freshwater ecosystem quality: Laboratory and field studies. Water Sci Technol 44: 305-312.
112. Beliaeff B, Burgeot T. 2002. Integrated biomarker response: A useful tool for ecological risk assessment. Environ Toxicol Chem 21: 1316-1322.
113. Forbes VE, Palmqvist A, Bach L. 2006. The use and misuse of biomarkers in ecotoxicology. Environ Toxicol Chem 25: 272-280.
114. Lagadic L. 1999. Biomarkers in invertebrates: Evaluating the effects of chemicals on populations and communities from biochemical and physiological changes in individuals. In Peakall DB, ed, Biomarkers: A Pragmatic Basis for Remediation of Severe Pollution in Eastern Europe. Kluwer Academic, Dordrecht, The Netherlands, pp 153-175.
115. Ankley GT, Brooks BW, Huggett DB, Sumpter JP. 2007. Repeating history: Pharmaceuticals in the environment. Environ Sci Technol 41: 8211-8217.
116. Beauvais SL, Atchison GJ, Stenback JZ, Crumpton WG 1999. Use of cholinesterase activity to monitor exposure of Chironomus riparius (Diptera: Chironomidae) to a pesticide mixture in hypoxic wetland mesocosms. Hydrobiologia 416: 163-170.
117. Guilhermino L, Lopes MC, Carvalho AP, Soares AMVM. 1996. Acetylcholinesterase activity in juvenile Daphnia magna strauss. Bull Environ Contam Toxicol 57: 979-985.
118. Martínez-Tabche L, Solís MR, López EL, Martínez MG. 1999. Efecto tóxico del DDT, clordano y agua de la presa Ignacio Ramírez (México), sobre Daphnia Magna (Crustaceae: Daphnidae). Rev Biol Trop 47: 681-690.
119. Fisher TC, Crane M, Callaghan A. 2000. An optimized microtiterplate assay to detect acetylcholinesterase activity in individual Chironomus riparius Meigen. Environ Toxicol Chem 19: 1749-1752.
120. Basack SB, Oneto ML, Fuchs JS, Wood EJ, Kesten EM. 1998. Esterases of Corbicula fluminea as biomarkers of exposure to organophosphorus pesticides. Bull Environ Contam Toxicol 61: 569-576.
121. Cooper NL, Bidwell JR. 2006. Cholinesterase inhibitionandimpacts on behaviour of the Asian clam, Corbicula fluminea, after exposure to an organophosphate insecticide. Aquat Toxicol 76: 258-267.
122. Rajyalakshmi T, Srinivas T, Swamy KV, Prasad NS, Mohan PM. 1996. Action of the herbicide butachlor on cholinesterases in the freshwater snail Pila globosa (swainson). Drug Chem Toxicol 19: 325-331.