Behavioural, physiological and biochemical markers in damselfly larvae (Ischnura elegans) to assess effects of accumulated metal mixtures

Science of the Total Environment

Volumn 470-471, Issue , 2014, Pages 208-215

  Van Praet, Nander ^a   De Jonge, Maarten ^a   Blust, Ronny ^a   Stoks, Robby ^b   Bervoets, Lieven ^a  

^a UNIVERSITY OF ANTWERP   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Biomonitoring; Damselfly larvae; Endpoints; Metal; Metal load index; Mixture

Indexed keywords

BIOCHEMISTRY; LAKES; MIXTURES; PHYSIOLOGY;

ACETYLCHOLINESTERASE; BIOCHEMICAL MARKERS; BIOMONITORING; DAMSELFLY LARVAE; ENDPOINTS; ENERGY AVAILABILITY; GLUTATHIONE-S-TRANSFERASE; LOAD INDEX;

METALS;

ACETYLCHOLINESTERASE; ARSENIC; CADMIUM; CHROMIUM; COBALT; COPPER; GLUTATHIONE TRANSFERASE; LEAD; METAL; NICKEL; SILVER; ZINC;

BIOACCUMULATION; BIOCHEMISTRY; BIOMARKER; BIOMONITORING; INSECT; LARVA; PHYSIOLOGY; TOXICITY;

ANIMAL TISSUE; ARTICLE; BELGIUM; BIOACCUMULATION; BIOLOGICAL MONITORING; CONTROLLED STUDY; DIPTERA; FOOD INTAKE; FOOD WEB; ISCHNURA ELEGANS; LARVA; LOCOMOTION; NATURAL POPULATION; NONHUMAN; PRIORITY JOURNAL;

ISCHNURA ELEGANS; ZYGOPTERA;

BIOMONITORING; DAMSELFLY LARVAE; ENDPOINTS; METAL; METAL LOAD INDEX; MIXTURE;

ACETYLCHOLINESTERASE; ANIMALS; BEHAVIOR, ANIMAL; BIOLOGICAL MARKERS; ENVIRONMENTAL MONITORING; GLUTATHIONE TRANSFERASE; LARVA; METALS; ODONATA; WATER POLLUTANTS, CHEMICAL;

EID: 84886245284     PISSN: 00489697     EISSN: 18791026     Source Type: Journal    
DOI: 10.1016/j.scitotenv.2013.09.093     Document Type: Article

References (62)

1. Barata C., Lekumberri I., Vila-Escale M., Prat N., Porte C. Trace metal concentration, antioxidant enzyme activities and susceptibility to oxidative stress in the Trichoptera larvae Hydropsyche exocellata from the Llobregat river basin (NE Spain). Aquat Toxicol 2005, 74:3-19.
2. Bervoets L., Knaepkens G., Eens M., Blust R. Fish community responses to metal pollution. Environ Pollut 2005, 138:338-349.
3. Bervoets L., Voets J., Covaci A., Chu S., Qadah D., Smolsers R., Schepens P., Blust R. Use of transplanted zebra mussels (Dreissena polymorpha) to assess the bioavailability of microcontaminants in Flemish surface waters. Environ Sci Technol 2005, 39:1492-1505.
4. Bervoets L., Van Campenhout K., Reynders H., Knapen D., Covaci A., Blust R. Bioaccumulation of micropollutants and biomarker responses in caged carp (Cyprinus carpio). Ecotoxicol Environ Saf 2009, 72:720-728.
5. Bligh E.G., Dyer W.J. A rapid method of total lipid extraction and purification. Can J Biochem Physiol 1959, 37:911-917.
6. Blust R., Vanderlinden A., Verheyen E., Decleir W. Evaluation of microwave-heating digestion and graphite-furnace atomic-absorption spectrometry with continuum source background correction for the determination of iron, copper and cadmium in brine shrimp. J Anal At Spectrom 1988, 3:387-393.
7. Bradford M.M. Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal Biochem 1976, 72:248-254.
8. Brix K.V., DeForset D.K., Adams W.J. The sensitivity of aquatic insects to devalent metals: a comparative analysis of laboratory and field data. Sci Total Environ 2011, 409:4187-4197.
9. Brooks A.C., Gaskell P.N., Maltby L.L. Sublethal effects and predator-prey interactions: implications for ecological risk assessment. Environ Toxicol Chem 2009, 28:2449-2457.
10. Calow P., Sibly R.M. A physiological-basis of population processes - ecotoxicological implications. Funct Ecol 1990, 4:283-288.
11. Campero M., Slos S., Ollevier F., Stoks R. Sublethal pesticide concentrations and predation jointly shape life history: behavioral and physiological mechanisms. Ecol Appl 2007, 17:2111-2122.
12. Clements W.H., Carlisle D.M., Lazorchak J.M., Johnson P.C. Heavy metals structure benthic communities in Colorado mountain streams. Ecol Appl 2000, 10:626-638.
13. Corbi J.J., Froehlich C.G., Trivinho-Strixino S., dos Santos A. Evaluating the use of predatory insects as bioindicators of metals contamination due to sugarcane cultivation in neotropical streams. Environ Monit Assess 2011, 177:545-554.
14. De Coen W.M., Janssen C.R. The use of biomarkers in Daphnia magna toxicity testing. 2. Digestive enzyme activity in Daphnia magna exposed to sublethal concentrations of cadmium, chromium and mercury. Chemosphere 1997, 35:1053-1067.
15. De Coen W.M., Janssen C.R. 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 2003, 22:1632-1641.
16. De Jonge M., Van de Vijver B., Blust R., Bervoets L. Responses of aquatic organisms to metal pollution in a lowland river in Flanders: a comparison of diatoms and macroinvertebrates. Sci Total Environ 2008, 407:615-629.
17. De Jonge M., Blust R., Bervoets L. The relation between Acid Volatile Sulfides (AVS) and metal accumulation in aquatic invertebrates: implications of feeding behavior and ecology. Environ Pollut 2010, 158:1381-1391.
18. De Jonge M., Teuchies J., Meire P., Blust R., Bervoets L. The impact of increased oxygen conditions on metal-contaminated sediments part II: effects on metal accumulation and toxicity in aquatic invertebrates. Water Res 2012, 46:3387-3397.
19. Dell'Omo G. Behavioural ecotoxicology 2002, Wiley.
20. Domingues I., Agra A.R., Monaghan K., Soares A.M.V.M., Nogueira A.J.A. Cholinesterase and glutathione-S-transferase activities in freshwater invertebrates as biomarkers to assess pesticide contamination. Environ Toxicol Chem 2010, 29:5-18.
21. EC Guidance Document No. 27 for deriving environmental quality standards under the Water Framework Directive. European Commission Common Implementation Strategy for the Water Framework Directive Technical Report-2011-055 2011.
22. Ellman G.L., Courtney K.D., Andres V., Featherstone R.M. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 1961, 7:88-95.
23. Fossi M.C., Leonzio C., Massi A., Lari L., Casini S. Serum esterase inhibition in birds - a nondestructive biomarker to assess organophosphorus and carbamate contamination. Arch Environ Contam Toxicol 1992, 23:99-104.
24. Fulton M.H., Key P.B. Acetylcholinesterase inhibition in estuarine fish and invertebrates as an indicator of organophosphorus insecticide exposure and effects. Environ Toxicol Chem 2001, 20:37-45.
25. Gill T.S., Tewari H., Pande J. Use of the fish enzyme-system in monitoring water-quality - effects of mercury on tissue enzymes. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 1990, 97:287-292.
26. Guilhermino L., Barros P., Silva M.C., Soares A.M.V.M. Should the use of inhibition of cholinesterases as a specific biomarker for organophosphate and carbamate pesticides be questioned?. Biomarkers 1998, 3:157-163.
27. Habig W.H., Pabst M.J., Jakoby W.B. Glutathione S-transferases-first enzymatic step in mercapturic acid formation. J Biol Chem 1974, 249:7130-7139.
28. Hardersen S., Wratten S.D. Sensitivity of aquatic life stages of Xanthocnemis zealandica (Odonata: Zygoptera) to azinphos-methyl and carbaryl. N Z J Mar Freshw Res 2000, 34:117-123.
29. Huggett R.J. Biomarkers: biochemical, physiological, and histological markers of anthropogenic stress 1992, Lewis Publishers.
30. Hyne R.V., Maher W.A. Invertebrate biomarkers: links to toxicosis that predict population decline. Ecotoxicol Environ Saf 2003, 54:366-374.
31. Janssens L., Stoks R. How does a pesticide pulse increase vulnerability to predation? Combined effects on behavioral antipredator traits and escape swimming. Aquat Toxicol 2012, 110:91-98.
32. Jemec A., Drobne D., Tisler T., Trebse P., Ros M., Sepcic K. The applicability of acetylcholinesterase and glutathione S-transferase in Daphnia magna toxicity test. Comp Biochem Physiol C Toxicol Pharmacol 2007, 144:303-309.
33. Jemec A., Tisler T., Drobne D., Sepcic K., Jamnik P., Ros M. Biochemical biomarkers in chronically metal-stressed daphnids. Comp Biochem Physiol C Toxicol Pharmacol 2008, 147:61-68.
34. Jensen C.S., Garsdal L., Baatrup E. Acetylcholinesterase inhibition and altered locomotor behavior in the carabid beetle Pterostichus cupreus. A linkage between biomarkers at two levels of biological complexity. Environ Toxicol Chem 1997, 16:1727-1732.
35. Karouna-Renier N.K., Sparling D.W. Relationships between ambient geochemistry, watershed land-use and trace metal concentrations in aquatic invertebrates living in stormwater treatment ponds. Environ Pollut 2001, 112:183-192.
36. Ketterer B., Coles B., Meyer D.J. The role of glutathione in detoxication. Environ Health Perspect 1983, 49:59-69.
37. Luoma S.N., Rainbow P.S. Why is metal bioaccumulation so variable? Biodynamics as a unifying concept. Environ Sci Technol 2005, 39:1921-1931.
38. Luoma S.N., Rainbow P.S. Metal contamination in aquatic environments: science and lateral management 2008, Cambridge University Press.
39. Martin C.A., Luoma S.N., Cain D.J., Buchwalter D.B. Cadmium ecophysiology in seven stone fly (Plecoptera) species: delineating sources and estimating susceptibility. Environ Sci Technol 2007, 41:7171-7177.
40. McLoughlin N., Yin D.Q., Maltby L., Wood R.M., Yu H.X. Evaluation of sensitivity and specificity of two crustacean biochemical biomarkers. Environ Toxicol Chem 2000, 19:2085-2092.
41. Mogren C.L., Trumble J.T. The impacts of metals and metalloids on insect behavior. Entomol Exp Appl 2010, 135:1-17.
42. Newman M.C. Fundamentals of ecotoxicology 2010, CRC Press, Boca Raton.
43. Norwood W.P., Borgmann U., Dixon D.G., Wallace A. Effects of metal mixtures on aquatic biota: a review of observations and methods. Hum Ecol Risk Assess 2003, 9:795-811.
44. Nriagu J.O., Pacyna J.M. Quantitative assessment of worldwide contamination of air, water and soils by trace-metals. Nature 1988, 333:134-139.
45. Nummelin M., Lodenius M., Tulisalo E., Hirvonen H., Alanko T. Predatory insects as bioindicators of heavy metal pollution. Environ Pollut 2007, 145:339-347.
46. Rainbow P.S. Trace metal concentrations in aquatic invertebrates why and so what?. Environ Pollut 2002, 120:497-507.
47. Rainbow P.S. Trace metal bioaccumulation: models, metabolic availability and toxicity. Environ Int 2007, 33:576-582.
48. Riddell D.J., Culp J.M., Baird D.J. Behavioral responses to sublethal cadmium exposure within an experimental aquatic food web. Environ Toxicol Chem 2005, 24:431-441.
49. Roe J.H., Dailey R.E. Determination of glycogen with anthrone reagent. Anal Biochem 1966, 15:245-250.
50. Roy I., Hare L. Relative importance of water and food as cadmium sources to the predatory insect Sialis velata (Megaloptera). Can J Fish Aquat Sci 1999, 56:1143-1149.
51. Schmidt T.S., Clements W.H., Mitchell K.A., Church S.E., Wanty R.B., Fey D.L., Verplanck P.L., San Juan C.A. Development of a new toxic-unit model for the bioassessment of metals in streams. Environ Toxicol Chem 2010, 29:2432-2442.
52. Smith G.R., Vaala D.A., Dingfelder H.A. Distribution and abundance of macroinvertebrates within two temporary ponds. Hydrobiologia 2003, 497:161-167.
53. Stoks R., Córdoba-Aguilar A. Evolutionary ecology of Odonata: a complex life cycle perspective. Annu Rev Entomol 2012, 57:249-265.
54. Tsangaris C., Papathanasiou E., Cotou E. Assessment of the impact of heavy metal pollution from a ferro-nickel smelting plant using biomarkers. Ecotoxicol Environ Saf 2007, 66:232-243.
55. U.S.Environmental Protection Agency National recommended water quality criteria: 2002. EPA-822-F-09-001 2009, Office of Water, Washington, D.C.
56. Van de Meutter F., Stoks R., De Meester L. Behavioral linkage of pelagic prey and littoral predators: microhabitat selection by Daphnia induced by damselfly larvae. Oikos 2004, 107:265-272.
57. Van Gestel C.A.M., Jonker M.J., Kammenga J.E., Svendsen C., Laskowski R. Mixture toxicity: linking approaches from ecological and human toxicology 2010, Setac Press.
58. Van Gossum H., Bots J., Snijkers T., Meyer J., Van Wassenbergh S., De Coen W., De Bruyn L. Behaviour of damselfly larvae (Enallagma cyathigerum) (Insecta, Odonata) after long-term exposure to PFOS. Environ Pollut 2009, 157:1332-1336.
59. Van Praet N., Covaci A., Teuchies J., De Bruyn L., Van Gossum H., Stoks R., Bervoets L. Levels of persistent organic pollutants in larvae of the damselfly Ischnura elegans (Odonata, Coenagrionidae) from different ponds in Flanders, Belgium. Sci Total Environ 2012, 423:162-167.
60. Voets J., Talloen W., de Tender T., van Dongen S., Covaci A., Blust R., Bervoets L. Microcontaminant accumulation, physiological condition and bilateral asymmetry in zebra mussels (Dreissena polymorpha) from clean and contaminated surface waters. Aquat Toxicol 2006, 79:213-225.
61. Wang W.X. Interactions of trace metals and different marine food chains. Mar Ecol Prog Ser 2002, 243:295-309.
62. Zhou Q.F., Zhang J.B., Fu J.J., Shi J.B., Jiang G.B. Biomonitoring: an appealing tool for assessment of metal pollution in the aquatic ecosystem. Anal Chim Acta 2008, 606:135-150.