The use of a lacertid lizard as a model for reptile ecotoxicology studies: Part 2 - Biomarkers of exposure and toxicity among pesticide exposed lizards

Chemosphere

Volumn 87, Issue 7, 2012, Pages 765-774

  Amaral, Maria José ^a,b   Bicho, Rita C ^a   Carretero, Miguel A ^b   Sanchez Hernandez, Juan C ^c   Faustino, Augusto M R ^d   Soares, Amadeu M V M ^a   Mann, Reinier M ^a,e,f  

^a UNIVERSITY OF AVEIRO   (Portugal)

^b CENTRO DE INVESTIGAÇÃO EM BIODIVERSIDADE E RECURSOS GENÉTICOS   (Portugal)

^c UNIVERSITY OF CASTILLA LA MANCHA   (Spain)

^d UNIVERSITY OF PORTO   (Portugal)

^e UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

^f NONE

Author keywords

Agro environments; Field study; Multi biomarker approach; Pesticides; Reptiles

Indexed keywords

BIOELECTRIC POTENTIALS; ENZYME ACTIVITY; METABOLISM; PESTICIDES;

AGRO-ENVIRONMENTS; FIELD STUDIES; LIPID PEROXIDATION; MULTI-BIOMARKER APPROACHES; OXIDATIVE PATHWAYS; REPTILE ECOTOXICOLOGY; REPTILES; WEIGHT OF EVIDENCE APPROACH;

BIOMARKERS;

BIOLOGICAL MARKER; GLUTATHIONE; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; GLUTATHIONE TRANSFERASE; IRON; PESTICIDE;

AGRONOMY; BIOMARKER; BODY CONDITION; ECOTOXICOLOGY; ENZYME ACTIVITY; HISTOLOGY; LIZARD; LOCOMOTION; METABOLISM; PARASITE PREVALENCE; PESTICIDE; POLLUTION EXPOSURE; TOXICITY TEST;

ANIMAL TISSUE; ARTICLE; CELL VACUOLE; ECOTOXICOLOGY; ENZYME ACTIVITY; IRON METABOLISM; LIPID PEROXIDATION; LIVER CELL; LIVER HISTOLOGY; LIZARD; LOCOMOTION; NONHUMAN; OXIDATION; TESTIS;

PORTUGAL;

ANIMALIA; LACERTIDAE; PODARCIS BOCAGEI; REPTILIA; SQUAMATA; ZEA MAYS;

EID: 84858623750     PISSN: 00456535     EISSN: 18791298     Source Type: Journal    
DOI: 10.1016/j.chemosphere.2012.01.048     Document Type: Article

References (85)

1. Abarikwu S., Adesiyan A., Oyeloja T., Oyeyemi M., Farombi E. Changes in sperm characteristics and induction of oxidative stress in the testis and epididymis of experimental rats by a herbicide, atrazine. Arch. Environ. Contam. Toxicol. 2010, 58:874-882.
2. Albers P.H., Heinz G.H., Hall R.J. Approaches for assessment of terrestrial vertebrate responses to contaminants: moving beyond individual organisms. Environmental Contaminants and Terrestrial Vertebrates: Effects on Populations, Communities, and Ecosystems, SETAC Special Publication 2000, 10-148. SETAC Press, Pensacola, FL. P.H. Albers, G.H. Heinz, H.M. Ohlendorf (Eds.).
3. Alexander G.J., Horne D., Hanrahan S.A. An evaluation of the effects of deltamethrin on two non-target lizard species in the Karoo, South Africa. J. Arid Environ. 2002, 50:121-133.
4. Amaral M.J., Carretero M.A., Soares A.M.V.M., Mann R.M. The use of a lacertid lizard as a model for reptile ecotoxicology studies: Part 1 - Field demographics and morphology. Chemosphere 2012, 87:757-764.
5. Amo L., López P., Martín J. Prevalence and intensity of haemogregarine blood parasites and their mite vectors in the common wall lizard, Podarcis muralis. Parasitol. Res. 2005, 96:378-381.
6. Amo L., López P., Martín J. Nature-based tourism as a form of predation risk affects body condition and health state of Podarcis muralis lizards. Biol. Conserv. 2006, 131:402-409.
7. Amo L., López P., Martín J. Habitat deterioration affects body condition of lizards: a behavioral approach with Iberolacerta cyreni lizards inhabiting ski resorts. Biol. Conserv. 2007, 135:77-85.
8. Ballinger R.E. Reproductive strategies: food availability as a source of proximal variation in a lizard. Ecology 1977, 58:628-635.
9. Bancroft J.D., Stevens A. Theory and practice of histological techniques 1996, Churchill Livingstone, Edinburgh, UK. fourth ed.
10. Banks J.E., Stark J.D. What is ecotoxicology? An ad-hoc grab bag or an interdisciplinary science?. Integr. Biol. 1998, 5:195-204.
11. Bauwens D., Garland T., Castilla A.M., Van Damme R. Evolution of sprint speed in lacertid lizards: morphological, physiological and behavioral covariation. Evolution 1995, 49:848-863.
12. Bennet A.F., Dawson W.R. Metabolism. Biology of the Reptilia 1976, vol. 5:127-223. Academic Press, London.
13. Bradford M.M. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye binding. Anal. Biochem. 1976, 72:248-254.
14. Brouwer A., Murk A., Koeman J. Biochemical and physiological approaches in ecotoxicology. Funct. Ecol. 1990, 4:275-281.
15. Brown M. Assessing Body Condition in Birds 1996, Plenum Press, New York.
16. Brown R., Pérez-Mellado V., Diego-Rasilla J., Garcia J., Naranjo A., Speakman J. Individual and population energetics of a lizard on a Mediterranean islet. Oecologia 1992, 91:500-504.
17. Congdon J.D., Dunham A.E., Twinkle D.W. Energy budgets and life histories of reptiles. Biology of the Reptilia 1982, vol. 13:233-271. Academic Press, New York.
18. Cork S., Alley M., Stockdale P. A quantitative assessment of haemosiderosis in wild and captive birds using image analysis. Avian Pathol. 1995, 24:239-254.
19. De Coen W.M., Janssen C.R., Giesy J.P. Biomarker applications in ecotoxicology: bridging the gap between toxicology and ecology. New Microbiotests for Routine Toxicity Screening and Biomonitoring 2000, Kluwer Academic, Plenum Publishers, New York. Persoone (Ed.).
20. Dorcas M.E., Hopkins W.A., Roe J.H. Effects of body mass and temperature on standard metabolic rate in the eastern diamondback rattlesnake (Crotalus adamanteus). Copeia 2004, 2004:145-151.
21. DuRant S.E., Hopkins W.A., Talent L.G. Energy acquisition and allocation in an ectothermic predator exposed to a common environmental stressor. Comp. Biochem. Physiol. C: Toxicol. Pharmacol. 2007, 145:424-448.
22. DuRant S.E., Hopkins W.A., Talent L.G. Impaired terrestrial and arboreal locomotor perfomance in the wester fence lizard (Sceloporus occidentalis) after exposure to an AChE-inhibiting pesticide. Environ. Pollut. 2007, 149:18-24.
23. Eurostat, 2007. The use of plant protection products in the European Union - Data 1992-2003. In: Eurostat (Ed.). European Commission.
24. Galdón M.A., Roca V., Barbosa D., Carretero M.A. Intestinal helminth communities of Podarcis bocagei and Podarcis carbonelli (Sauria: Lacertidae) in NW Portugal. Helminthologia 2006, 43:37-41.
25. Guillette L.J., Gross T.S., Masson G.R., Matter J.M., Percival H.F., Woodward A.R. Developmental abnormalities of the gonad and abnormal sex hormone concentrations in juvenile alligators from contaminated and control lakes in Florida. Environ. Health Perspect. 1994, 182:680-688.
26. Habig W.H., Pabst M.J., Jakoby W.B. Glutathione S-transferases. J. Biol. Chem. 1974, 249:7130-7139.
27. Hermes-Lima M., Zenteno-Savín T. Animal response to drastic changes in oxygen availability and physiological oxidative stress. Comp. Biochem. Physiol. C: Toxicol. Pharmacol. 2002, 133:537-556.
28. Hinton D.E., Lauren D.J. Liver structural alterations accompanying chronic toxicity in fishes: potential biomarkers of exposure. Biomarkers of Environmental Contamination 1990, 17-57. CRC Press, Boca Raton, FL. J.R. McCarthy, L.R. Shugart (Eds.).
29. Hissin P.J., Hilf R. A fluorometric method for determination of oxidized and reduced glutathione in tissues. Anal. Biochem. 1976, 74:214-226.
30. Holem R.R., Hopkins W.A., Talent L.G. Effect of acute exposure to malathion and lead on sprint performance of the western fence lizard (Sceloporus occidentalis). Arch. Environ. Contam. Toxicol. 2006, 51:111-116.
31. Holem R.R., Hopkins W.A., Talent L.G. Effects of repeated exposure to malathion on growth, food consumption, and locomotor perfomance of the western fence lizard (Sceloporus occidentalis). Environ. Pollut. 2008, 152:92-98.
32. Hopkins W.A. Use of tissue residues in reptile ecotoxicology: a call for integration and experimentalism. Toxicology of Reptiles 2006, 35-62. Taylor and Francis, New York. S.C. Gardner, E. Oberdorster (Eds.).
33. Hopkins W.A., Winne C.T. Influence of body size on swimming perfomance of four species of neonatal natricine snakes acutely exposed to a cholinesteras-inhibiting pesticide. Environ. Toxicol. Chem. 2006, 25:1208-1213.
34. Hopkins W.A., Rowe C.L., Congdon J.D. Elevated trace element concentrations and standard metabolic rate in banded water snakes (Nerodia fasciata) exposed to coal combustion wastes. Environ. Toxicol. Chem. 1999, 18:1258-1263.
35. Hopkins W.A., Roe J.H., Snodgrass J.W., Staub B.P., Jackson B.P., Congdon J.D. Effects of chronic dietary exposure to trace elements on banded water snakes (Nerodia fasciata). Environ. Toxicol. Chem. 2002, 21:906-913.
36. Jena B.S., Das S., Patnaik B.K. Effect of age on lipid peroxidation in a short-lived species of reptile, Calotes versicolor. Arch. Gerontol. Geriatr. 1995, 20:263-272.
37. Jones L., Gossett D.R., Banks S.W., McCallum M.L. Antioxidant defense system in tadpoles of the American bullfrog (Lithobates catesbeianus) exposed to paraquat. J. Herpetol. 2010, 44:222-228.
38. Jorge F., Roca V., Perera A., Harris D.J., Carretero M.A. Host-parasite cophylogeny: no simple answers for Spauligodon atlanticus (Nematoda: Pharyngodonidae), parasite of the Gallotia lizards. Syst. Parasitol. 2011, 80:53-66.
39. Kelly W.R. The liver and biliary system. Pathology of Domestic Animals 1993, 319-406. Academic Press, San Diego, California. K.V.F. Jubb, P.C. Kennedy, N. Palmer (Eds.).
40. Koivula M.J., Eeva T. Metal-related oxidative stress in birds. Environ. Pollut. 2010, 158:2359-2370.
41. Lailvaux S.P., Irschick D.J. A functional perspective on sexual selection: insights and future prospects. Anim. Behav. 2006, 72:263-273.
42. Lambert M.R.K. Lizards as bioindicators. Biologist 1999, 46:12-16.
43. Lambert M.R.K. Lizards used as bioindicators to monitor pesticide contamination in sub-Saharan Africa: a review. Appl. Herpetol. 2005, 2:99-107.
44. Lawrence R.A., Burk R.F. Glutathione peroxidase activity in selenium-deficient rat liver. Biochem. Biophys. Res. Commun. 1976, 71:952-958.
45. Mandal A., Chakraborty S., Lahiri P. Hematological changes produced by lindane ([gamma]-HCH) in six species of birds. Toxicology 1986, 40:103-111.
46. Mann R.M. Methodological approaches in amphibian toxicology. Appl. Herpetol. 2005, 2:223-230.
47. Mann R.M., Hyne R.V., Choung C.B., Wilson S.P. Amphibians and agricultural chemicals: review of the risks in a complex environment. Environ. Pollut. 2009, 157:2903-2927.
48. McFarland C.A., Quinn M.J.J., Bazar M.A., Remick A.K., Talent L.G., Johson M.S. Toxicity of oral exposure to 2,4,6-trinitrotoluene in the western fence lizard (Sceloporus occidentalis). Environ. Toxicol. Chem. 2008, 27:1102-1111.
49. Mikula P., Blahova J., Kruzikova K., Havelkpva M., Nemethova D., Hulak M., Svobodova Z. Effects of the herbicide Lasso MTX (alachlor 42% W/V) on biometric parameters and liver biomarkers in the common carp (Cyprinus carpio). Pesticide Biochem. Physiol. 2009, 93:13-17.
50. Mitchelmore C.L., Rowe C.L., Place A.R. Tools for assessing contaminant exposure and effects in reptiles. Toxicology of Reptiles 2006, 63-122. Taylor & Francis Group, Boca Raton. S.C. Gardner, E. Oberdorster (Eds.).
51. Moore M.N., Simpson M.G. Molecular and cellular pathology in environmental impact assessment. Aquat. Toxicol. (Amst.) 1992, 22:313-322.
52. Murphy M., Hecker M., Coady K., Tompsett A., Jones P., Newsted J., Wong H., du Preez L., Solomon K., Carr J., Smith E., Kendall R., Van Der Kraak G., Giesy J. Sediment TCDD-EQs and EROD and MROD activities in ranid frogs from agricultural and nonagricultural sites in Michigan (USA). Arch. Environ. Contam. Toxicol. 2006, 51:467-477.
53. Ohkawa H., Ohishi N., Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal. Biochem. 1979, 95:351-358.
54. Olsson M., Wapstra E., Madsen T., Silverin B. Testosterone, ticks and travels: a test of the immunocompetence-handicap hypothesis in free-ranging male sand lizards. Proc. R. Soc. London, B: Biol. Sci. 2000, 267:2339.
55. Osborn D. Seasonal changes in the fat, protein and metal content of the liver of the starling Sturnus vulgaris. Environ. Pollut. 1979, 19:145-155.
56. Overmann S.R., Krajicek J.J. Snapping turtles (Chelydra serpentina) as biomonitors of lead contamination of the big river in missouri's old lead belt. Environ. Toxicol. Chem. 1995, 14:689-695.
57. Özelmas ü., Akay M.T. Histopathological investigations of the effects of malathion on dwarf lizards (Lacerta parva, Boulenger 1887). Bull. Environ. Contam. Toxicol. 1995, 55:730-737.
58. Pafilis P., Meiri S., Foufopoulos J., Valakos E. Intraspecific competition and high food availability are associated with insular gigantism in a lizard. Naturwissenschaften 2009, 96:1107-1113.
59. Peakall D.B. The role of biomarkers in environmental assessement (1). Introduction. Ecotoxicology 1994, 3:157-160.
60. Pinho C., Harris D., Ferrand N. Contrasting patterns of population subdivision and historical demography in three western Mediterranean lizard species inferred from mitochondrial DNA variation. Mol. Ecol. 2007, 16:1191-1205.
61. Pinho C., Kaliontzopoulou A., Harris D.J., Ferrand N. Recent evolutionary history of the Iberian endemic lizardsPodarcis bocagei (Seoane, 1884) andPodarcis carbonelli Pérez Mellado, 1981 (Squamata: Lacertidae) revealed by allozyme and microsatellite markers. Zool. J. Linn. Soc 2011.
62. Ramos-Martinez J.I., Bartolomé T.R., Pernas R.V. Purification and properties of glutathione reductase from hepatopancreas of Mytilus edulis L. Comp. Biochem. Physiol., B: Comp. Biochem. 1983, 75:689-692.
63. Rania-Ganser L., Hopkins W.A., O'Neill L., Hasse S., Roe J.H., Sever D.M. Liver histopathology of the southern watersnake Nerodia fasciata fasciata following chronic exposure to trace element-contaminated prey from a coal ash disposal site. J. Herpetol. 2003, 37:219-226.
64. Richardson N., Gordon A., Muller W., Pletschke B., Whitfield A. The use of liver histopathology, lipid peroxidation and acetylcholinesterase assays as biomarkers of contaminant-induced stress in the Cape stumpnose, Rhabdosargus holubi (Teleostei: Sparidae), from selected South African estuaries. Water SA (Online) 2010, 36.
65. Roca V., Galdón M.A. Haemogregarine blood parasites in the lizards Podarcis bocagei (Seoane) and P. carbonelli (Pérez-Mellado) (Sauria: Lacertidae) from NW Portugal. Syst. Parasitol. 2010, 75:75-79.
66. Roca V., Carretero M.A., Marques A., Barbosa D., Galdón M.A. Relationships between helminth communities and host traits in Podarcis bocagei and Podarcis carbonelli from NW Portugal. Ital. J. Zool. 2006, 73:213-217.
67. Rohr J.R., Schotthoefer A.M., Raffel T.R., Carrick H.J., Halstead N., Hoverman J.T., Johnson C.M., Johnson L.B., Lieske C., Piwoni M.D., Schoff P.K., Beasley V.R. Agrochemicals increase trematode infections in a declining amphibian species. Nature 2008, 455:1235-1239.
68. Sanchez-Hernandez J.C., Carbonell R., Henri{dotless}quez Perez A., Montealegre M., Gomez L. Inhibition of plasma butyrylcholinesterase activity in the lizard Gallotia galloti palmae by pesticides: a field study. Environ. Pollut. 2004, 132:479-488.
69. Santos X., Llorente G.A. Lipid dynamics in the viperine snake, Natrix maura, from the Ebro Delta (NE Spain). Oikos 2004, 105:132-140.
70. Schaffner F. The liver. Biology of the Reptilia - Morphology G Visceral Organs 1998, 485-531. Society for the Study of Amphibians and Reptiles, Ithaca, NY. C. Gans, A.S. Gaunt (Eds.).
71. Schulte-Hostedde A.I., Zinner B., Millar J.S., Hickling G.J. Restitution of mass-size residuals: validating body condition indices. Ecology 2005, 86:155-163.
72. Simão F. The Effects of Distinct Herbicides Regimes in Soil Arthropods 2011, Departamento de Biologia. Universidade de Aveiro, Aveiro, p. 71.
73. Sparling D.W., Linder G., Bishop C.A., Krest S.K. Recent advancements in amphibian and reptile ecotoxicology. Ecotoxicology of Amphibians and Reptiles 2010, Taylor and Francis, New York. D.W. Sparling, G. Linder, C.A. Bishop, S.K. Krest (Eds.).
74. Stentiford G.D., Longshaw M., Lyons B.P., Jones G., Green M., Feist S.W. Histopathological biomarkers in estuarine fish species for the assessment of biological effects of contaminants. Mar. Environ. Res. 2003, 55:137-159.
75. Storey K.B. Oxidative stress: animal adaptations in nature. Braz. J. Med. Biol. Res. 1996, 29:1715-1733.
76. Sures B. Environmental parasitology: relevancy of parasites in monitoring environmental pollution. Trends Parasitol. 2004, 20:170-177.
77. Sures B. Environmental parasitology. Interactions between parasites and pollutants in the aquatic environment. Parasite 2008, 15:434-438.
78. Telford S.R.J. Hemoparasites of Reptilia Color Atlas and Text 2009, CRC Press, Boca Raton.
79. Uller T., Olsson M. Prenatal exposure to testosterone increases ectoparasite susceptibility in the common lizard (Lacerta vivipara). Proc. R. Soc. Biol. Sci. Ser. B 2003, 270:1867-1870.
80. Valdivia P.A., Zenteno-Savín T., Gardner S.C., Alonso Aguirre A. Basic oxidative stress metabolites in eastern Pacific green turtles (Chelonia mydas agassizii). Comp. Biochem. Physiol., C: Comp. Pharmacol. 2007, 146:111-117.
81. van der Oost R., Beyer J., Vermeulen N.P.E. Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ. Toxicol. Pharmacol. 2003, 13:57-149.
82. Voituron Y., Servais S., Romestaing C., Douki T., Barré H. Oxidative DNA damage and antioxidant defenses in the European common lizard (Lacerta vivipara) in supercooled and frozen states. Cryobiology 2006, 52:74-86.
83. Willemsen R.E., Hailey A. Effects of spraying the herbicides 2,4-D and 2,4,5-T on a population of the tortoise Testudo hermanni in southern Greece. Environ. Pollut. 2001, 113:71-78.
84. Yi X., Ding H., Lu Y., Liu H., Zhang M., Jian W. Effects of long-term alachlor exposure on hepatic antioxidant defense and detoxifying enzyme activities in crucian carp (Carassius auratus). Chemosphere 2007, 68:1576-1581.
85. Zar J.H. Biostatistical Analysis 1996, Prentice Hall, Upper Saddle River.