Endosulfan acute toxicity in Bufo bufo gills: Ultrastructural changes and nitric oxide synthase localization

Aquatic Toxicology

Volumn 86, Issue 3, 2008, Pages 447-456

  Bernabò, Ilaria ^a   Brunelli, Elvira ^a   Berg, Cecilia ^b   Bonacci, Antonella ^a   Tripepi, Sandro ^a  

^a UNIVERSITY OF CALABRIA   (Italy)

^b UPPSALA UNIVERSITY   (Sweden)

Author keywords

Amphibians; Endosulfan; Gills; iNOS; Ultrastructure; Water pollution

Indexed keywords

ENDOSULFAN; INDUCIBLE NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE; ORGANOCHLORINE PESTICIDE;

MORPHOLOGY; NITRIC OXIDE; ORGANOCHLORINE; PESTICIDE; POLLUTION EFFECT; POLLUTION EXPOSURE; SUBLETHAL EFFECT; TOAD; TOXICITY; ULTRASTRUCTURE; WATER POLLUTION;

AGRICULTURE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; ENZYME LOCALIZATION; GAS EXCHANGE; GILL; HYPOXIA; IMMUNOHISTOCHEMISTRY; INFLAMMATION; INTOXICATION; LAMELLAR BODY; MUCUS SECRETION; NONHUMAN; OSMOREGULATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SECRETORY VESICLE; TADPOLE; TOAD; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE; WATER POLLUTION;

ANIMALS; BUFO BUFO; ENDOSULFAN; GENE EXPRESSION REGULATION; GILLS; INSECTICIDES; LARVA; LETHAL DOSE 50; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, ELECTRON, TRANSMISSION; NITRIC OXIDE SYNTHASE; TIME FACTORS; WATER POLLUTANTS, CHEMICAL; WATER-ELECTROLYTE BALANCE;

AMPHIBIA; ANURA; BUFO BUFO;

EID: 39149143014     PISSN: 0166445X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.aquatox.2007.12.006     Document Type: Article

References (78)

1. Alford R.A., and Richards S.J. Global amphibian decline: a problem in applied ecology. Annu. Rev. Ecol. Syst. 30 (1999) 133-165
2. Anand M., Agrawal A.K., Gopal K., Sur R.N., and Seth P.K. Endosulfan and cholinergic (muscarinic) transmission: effect on electroencephalograms and [3H] quinuclidinyl benzilate in pigeon brain. Environ. Res. 40 (1986) 421-426
3. American Society for Testing Material (ASTM), 1997. Standard practice for conducting acute toxicity tests with fishes, macroinvertebrates, and amphibians. E 729-790. In American Society for Testing and Materials Standards, Philadelphia.
4. Ayub S., Verma J., and Das N. Effect of endosulfan and malathion on lipid peroxidation, nitrite and TNF-a release by rat peritoneal macrophages. Int. Immunopharmacol. 3 (2003) 1819-1828
5. Barni S., Boncompagni E., Grosso A., Bertone V., Freitas I., Fasola M., and Fenoglio C. Evaluation of Rana snk esculenta blood cell response to chemical stressors in the environment during the larval and adult phases. Aquat. Toxicol. 81 (2007) 45-54
6. Beebee T.J.C., and Griffiths R.A. The amphibian decline crisis: a watershed for conservation biology?. Biol. Conserv. 125 (2005) 271-285
7. Berrill M., Bertram S., McGillivray L., Kolohon M., and Pauli B. Effects of low concentrations of forest use pesticides on frog embryos and tadpoles. Environ. Toxicol. Chem. 13 (1994) 657-664
8. Berrill M., Coulson D., McGillivray L., and Pauli B. Toxicity of endosulfan to aquatic stage of anuran amphibians. Environ. Toxicol. Chem. 9 (1998) 1738-1744
9. Blaustein A.R., and Kiesecker J.M. Complexity in conservation: lessons from the global decline of amphibian populations. Ecol. Lett. 5 (2002) 597-608
10. Bridges C.M., and Semlitsch R.D. Variation in pesticide tolerance of tadpoles among and within species of Ranidae and patterns amphibian decline. Conserv. Biol. 14 (2000) 490-1499
11. Broomhall S. The effects of endosulfan and variable water temperature on survivorship and subsequent vulnerability to predation in Litoria citropa tadpoles. Aquat. Toxicol. 61 (2002) 243-250
12. Broomhall S. Egg temperature modifies predator avoidance and the effects of the insecticide endosulfan on tadpoles of an Australian frog. J. Appl. Ecol. 41 (2004) 105-113
13. Brunelli E., Perrotta E., and Tripepi S. Ultrastructure and development of the gills in Rana dalmatina (Amphibia, Anura). Zoomorphology 123 (2004) 203-211
14. Carey C., and Bryant C.J. Possible interrelations among environmental toxicants, amphibian development, and decline of amphibian populations. Environ. Health Perspect. 103 (1995) 13-17
15. Carrier J.A., and Beebee T.J.C. Recent, substantial, and unexplained declines of the common toad Bufo bufo in lowland England. Biol. Conserv. 111 (2003) 395-399
16. Clark E.J., Norris D.O., and Jones R.E. Interactions of gonadal steroids and pesticides (DDT, DDE) on gonaduct growth in larval tiger salamanders, Ambystoma tigrinum. Gen. Comp. Endocrinol. 109 (1998) 94-105
17. Coats J.R. Mechanisms of toxic action and structure-activity relationships for organochlorine and synthetic pyrethroid insecticides. Environ. Health Perspect. 87 (1990) 255-262
18. Coleman J.W. Nitric oxide in immunity and inflammation. Int. Immunopharmacol. 1 (2001) 1397-1406
19. Coons A.H., Leduc E.H., and Connolly J.M. Studies on antibody. I. A method for the histochemical demonstration of specific antibody and its application to a study of the hyperimmune rabbit. J. Exp. Med. 102 (1955) 49-59
20. Crittenden P.L., Carr R., and Pruett S.B. Immunotoxicological assessment of methyl parathion in female B6C3F1 mice. J. Toxicol. Environ. Health 54 (1998) 1-20
21. Daniels C.B., Lopatko O.V., and Orgeig S. Evolution of surface activity related functions of vertebrate pulmonary surfactant. Clin. Exp. Pharmacol. Physiol. 25 (1998) 716-721
22. Davidson C., Shaffer H.B., and Jennings M.R. Declines of the California red-legged frog: climate, UVB, habitat and pesticides hypothesis. Ecol. Appl. 11 (2001) 464-479
23. Davidson C., Shaffer H.B., and Jennings M.R. Spatial tests of the pesticide drift, habitat destruction, UV-B, and climate-change hypotheses for California amphibian declines. Conserv. Biol. 16 (2002) 1588-1601
24. Dezfuli B.S., Giari L., Konecny R., Jaeger P., and Manera M. Immunohistochemistry, ultrastructure and pathology of gills of Abramis brama from Lake Mondsee, Austria, infected with Ergasilus sieboldi (Copepoda). Dis. Aquat. Org. 53 (2003) 257-262
25. Duellman W.E., and Trueb L. Biology of Amphibians (1986), McGraw-Hill, New York
26. Ebbesson L.E., Tipsmark C.K., Holmqvist B., Nilsen T., Andersson E., Stefansson S.O., and Madsen S.S. Nitric oxide synthase in the gill of Atlantic salmon: colocalization with and inhibition of Na+, K+-ATPase. J. Exp. Biol. 208 (2005) 1011-1017
27. 50 Software Program, Version 1. 00 (1999), Center for Exposure Assessment Modeling (CEAM) Distribution Center
28. Environmental Protection Agency (EPA). Reregistration Eligibility Decision for Endosulfan. July 31, 2002 (2002), United States Environmental Protection Agency, Office of Prevention, Pesticides, and Toxic Substances
29. Ernst W.R., Jonah P., Doe K., Julien G., and Hennigar P. Toxicity to aquatic organisms of off-target deposition of endosulfan applied by aircraft. Environ. Toxicol. Chem. 10 (1991) 103-114
30. European Commission. Monitoring of Pesticide Residues in Products of Plant Origin in the European Union (2004), Iceland and Lichtenstein, Norway
31. European Food Safety Authority (EFSA). Opinion of the scientific panel on contaminants in the food chain on a request from the commission related to endosulfan as undesirable substance in animal feed. EFSA J. 234 (2005) 1-29
32. Fagotti A., Morosi L., Di Rosa I., Clarioni R., Simoncelli F., Pascolini R., Pellegrino R., Guex G.D., and Hotz H. Bioaccumulation of organochlorine pesticides in frogs of the Rana esculenta complex in central Italy. Amphibia Reptilia 26 (2005) 93-104
33. Fenoglio C., Grosso A., Boncompagni E., Milanesi G., Gandini C., and Barni S. Morphofunctional evidence of changes in principal and mitochondria-rich cells in the epidermis of the frog Rana kl. esculenta living in a polluted habitat. Arch. Environ. Contam. Toxicol. 51 (2006) 690-702
34. Finney D.J. Probit Analysis. third ed. (1971), Cambridge University Press, New York p. 668
35. Franklin G.E. Surface ultrastructure changes in the gills of sockeye salmon (Teleostei: Oncorhynchus nerka) during seawater transfer: comparison of successful and unsuccessful seawater adaptation. J. Morphol. 206 (1990) 13-23
36. German Federal Environment Agency. Draft Dossier Prepared in Support of a Proposal of Endosulfan to be Considered as a Candidate for Inclusion in the UN-ECE LRTAP Protocol on Persistent Organic Pollutants (2004), Umweltbundesamt, Berlin
37. Giusi G., Facciolo R.M., Alò R., Carelli A., Madeo M., Brandmayr P., and Canonaco M. Some environmental contaminants influence motor and feeding behaviors in the Ornate wrasse (Thalassoma pavo) via distinct cerebral histamine receptor subtypes. Environ. Health Perspect. 113 (2005) 1522-1529
38. Gopal K., Khanna R.N., Anand M., and Gupta G.S.D. The acute toxicity of endosulfan to freshwater organism. Toxicol. Lett. 7 (1981) 453-456
39. Gopal K., Anand M., Mehrotra S., and Ray P.K. Neurobehavioral changes in fresh water fish Channa punctatus exposed to endosulfan. J. Adv. Zool. 5 (1985) 74-80
40. Gosner K.L. A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16 (1960) 183-190
41. Han E.H., Hwang Y.P., Kim H.G., and Jeong H.G. Inflammatory effect of endosulfan via NF-jB activation in macrophages. Biochem. Biophys. Res. Commun. 355 (2007) 860-865
42. Harris M.L., Bishop C.A., Struger J., Ripley B., and Bogart J.P. The functional integrity of northern leopard frog (Rana pipiens) and green frog (Rana clamitans) populations in orchard wetlands. II. Effects of pesticides and eutrophic conditions on early life stage development. Environ. Toxicol. Chem. 17 (1998) 1351-1363
43. Harris M.L., Chora L., Bishop C.A., and Bogart J.P. Species- and age-related differences in susceptibility to pesticide exposure for two amphibians, Rana pipiens and Bufo americanus. Bull. Environ. Contam. Toxicol. 64 (2000) 263-270
44. Hermida G.N., Farías A., and Fiorito L.E. Ultrastructural characteristics of the lung of Melanophryniscus stelzneri stelzneri (Weyenberg, 1875) (Anura, Bufonidae). Biocell 26 (2002) 347-355
45. Houlahan J.E., Findlay C.S., Schmidt B.R., Meyer A.H., and Kuzmin S.L. Quantitative evidence for global amphibian population decline. Nature 404 (2000) 752-755
46. Hourdry J. Etude des branchies "internes" puis de leur règression au moment de la metamorphose, chez la larve de Discoglossus pictus (OTTH), Amphibien Anoure. J. Microsc. Paris 20 (1974) 165-182
47. International Union for Conservation of Nature (IUCN). The 2007 IUCN Red List of Threatened Animals (2007), International Union for Conservation of Nature, Gland, Switzerland. http://www.redlist.org/ (available from http://www.redlist.org)
48. Johnson W.W., and Finley M.T. Handbook of Acute Toxicity of Chemicals to Fish and Aquatic Invertebrates (1980), U.S. Department of Interior, Fish and Wildlife Service, Washington, DC (Resource Publication 137)
49. Johnson M.S., Vodela J.K., Reddy G., and Holladay S.D. Fate and the biochemical effects of 2,4,6-trinitrotoluene exposure to tiger salamanders (Ambystoma tigrinum). Ecotoxicol. Environ. Saf. 46 (2000) 186-191
50. Kato S., and Kurihara K. Electron microscopic studies of the external gill epithelium of the salamander, Hynobius dunni Tago, followed throughout larval life. Okajimas Folia Anat. Jpn. 65 (1988) 177-202
51. Kiesecker J.M., Blaustein A.R., and Belden L.K. Complex causes of amphibian population declines. Nature 410 (2001) 681-684
52. Kim J.Y., Choi C.Y., Lee K.J., Shin D.W., Jung K.S., Chung Y.C., Lee S.S., Shin J.G., and Jeong H.G. Induction of inducible nitric oxide synthase and proinflammatory cytokines expression by o,p-DDT in macrophages. Toxicol. Lett. 147 (2004) 261-269
53. Kim J.Y., Oh K.N., Han E.H., Kim D.H., Jeong T.C., Lee E.S., and Jeong H.G. Methoxychlor-induced inducible nitric oxide synthase and proinflammatory cytokines expression in macrophages via NF-jB, ERK, and p38 mitogen-activated protein kinases. Biochem. Biophys. Res. Commun. 333 (2005) 1234-1240
54. Kwon S., Newcomb R.L., and George S.C. Mechanisms of synergistic cytochine-induced nitric oxide production in human alveolar epithelial cells. Nitric Oxide 5 (2001) 534-546
55. Lajmanovich R.C., Izaguirre M.F., and Casco V.H. Paraquat tolerance and alteration of internal gill structure of Scinax nasica tadpoles (Anura: Hylidae). Arch. Environ. Contam. Toxicol. 34 (1998) 364-369
56. Lajmanovich R.C., Cabagna M., Peltzer P.M., Stringhini G.A., and Attademo A.M. Micronucleus induction in erythrocytes of the Hyla pulchella tadpoles (Amphibia: Hylidae) exposed to insecticide endosulfan. Mutat. Res. 587 (2005) 67-72
57. Lakshmana M.K., and Raju T.R. Endosulfan induces small but significant changes in the levels of noradrenaline, dopamine and serotonin in the developing rat brain and deficits in the operant learning performance. Toxicology 91 (1994) 139-150
58. Langston W.J., Chesman B.S., Burt G.R., Pope N.D., and McEvoy J. Metallothionein in liver of eels Anguilla anguilla from the Thames Estuary: an indicator of environmental quality?. Mar. Environ. Res. 53 (2002) 263-293
59. Materna E.J., Rabeni C.F., and Lapoint T.W. Effects of the synthetic pyrethroid insecticide, esfenvalerate, on larval leopard frogs (Rana spp.). Environ. Toxicol. Chem. 14 (1995) 613-622
60. McIndoe R., and Smith D.J. Functional anatomy of the internal gills of the tadpole of Litoria ewingii (Anura, Hylidae). Zoomorphology 104 (1984) 280-291
61. Moncada S., Palmer R.M., and Higgs E.A. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharm. Rev. 43 (1992) 109-142
62. Naqvi S.M., and Vaishnavi C. Bioaccumulation potential and toxicity of endosulfan insecticide to not-target animals. Comp. Biochem. Physiol. C 105 (1993) 347-361
63. Nathan C., and Xie Q. Nitric oxide 3 synthases: roles, tolls, and controls. Cell 78 (1994) 915-918
64. Paul V., and Balasubramaniam E. Effects of single and repeated administration of endosulfan on behaviour and its interaction with centrally acting drugs in experimental animals: a mini review. Environ. Toxicol. Pharmacol. 3 (1997) 151-157
65. Pavignano I., and Giacoma C. Una valutazione ecologica dello stato di conservazione delle zone umide minori della pianura Piemontese - Atti VI Conv. naz. Ass. "A. Chigi", Torino (1989). Mus. reg. Sci. Nat. Torino. (1990) 91-104
66. Rosenberg M., and Warburg M.K. Ultrastructure and histochemistry of ventral epidermis in Pelobates syriacus (Anura; Pelobatidae) tadpoles. Biol. Struct. Morphogen. 4 (1992) 164-170
67. Rosenberg M., and Warburg M.K. The ventral epidermis of Pelobates syriacus (Anura; Pelobatidae). Isr. J. Zool. 39 (1993) 235-243
68. Roy P.K., and Munshi J.S.D. Malathion induced structural and morphometric changes of gills of a fresh water major carp, Cirrhinus mrigala. J. Environ. Biol. 12 (1991) 79-87
69. Schmitz G., and Muller G. Structure and function of lamellar bodies, lipid-protein complexes involved in storage and secretion of cellular lipids. J. Lipid Res. 32 (1991) 1539-1570
70. Singh N., Singh C.P., Kumar H., and Brat G.K. Endosulfan poisoning: a study of 22 cases. J. Assoc. Phys. India 40 (1992) 87
71. Sparling D.W., Fellers F.M., and McDonnell L. Pesticides and amphibian population declines in California, USA. Environ. Toxicol. Chem. 7 (2001) 1591-1595
72. Stuart S.N., Chanson J.S., Cox N.A., Young B.E., Rodrigues A.S., Fischman D.L., and Waller R.W. Status and trends of amphibian declines and extinctions worldwide. Science 306 (2004) 1783-1786
73. Uchiyama M., Yoshizawa H., Wakasugi C., and Oguro C. Structure of internal gills in tadpoles of the crab-eating frog, Rana cancrivora. Zool. Sci. 7 (1990) 623-630
74. Uchiyama M., and Yoshizawa H. Salinity tolerance and structure of external and internal gills in tadpoles of the crab-eating frog, Rana cancrivora. Cell Tissue Res. 267 (1992) 35-44
75. Vardia H.K., Rao P.S., and Durve V.S. Sensitivity of toad larvae to 2,4-D and endosulfan pesticides. Arch. Hydrobiol. 100 (1984) 395-400
76. Venturino A., Rosenbaum E., and Caballero de Castro A. Biomarkers of effect in toads and frogs. Biomarkers 8 (2003) 167-186
77. Wake D.B. Declining amphibian populations. Science 253 (1991) 60
78. Warburg M.K., and Rosenberg M. Structure of gill epithelium in Triturus vittatus larvae. Ann. Anat. 179 (1997) 57-64