A multi-level approach using Gambusia affinis as a bioindicator of environmental pollution in the middle-lower basin of Suquía River

Ecological Indicators

Volumn 48, Issue , 2015, Pages 706-720

  Rautenberg, Gisela Evelín ^a   Amé, María Valeria ^a   Monferrán, Magdalena Victoria ^a   Bonansea, Rocío Inés ^a   Hued, Andrea Cecilia ^a  

^a UNIVERSIDAD NACIONAL DE CÓRDOBA   (Argentina)

Author keywords

Biomarkers; Fish; Freshwater quality; Metals; Pesticides

Indexed keywords

FISH; METALS; PESTICIDES;

BIOINDICATOR; ENVIRONMENTAL POLLUTIONS; GAMBUSIA AFFINIS;

BIOMARKERS;

BIOINDICATOR; BIOMARKER; CYPRINID; ENVIRONMENTAL FATE; HISTOPATHOLOGY; MORPHOLOGY; PESTICIDE; WATER QUALITY;

ARGENTINA; CORDOBA [ARGENTINA]; PRIMERO RIVER; SUQUIA BASIN;

GAMBUSIA AFFINIS;

EID: 84907789811     PISSN: 1470160X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ecolind.2014.09.025     Document Type: Article

References (94)

1. S.S. Albaseer, K. Mukkanti, R.N. Rao, and Y.V. Swamy Analytical artifacts, sample handling and preservation methods of environmental samples of synthetic pyrethroids Trend Anal. Chem. 30 2011 1771 1780
2. M.V. Amé, M.V. Baroni, L.N. Galanti, J.L. Bocco, and D.A. Wunderlin Effects of microcystin-LR on the expression of P-glycoprotein in Jenynsia multidentata Chemosphere 74 2009 1179 1186
3. R.A. Angus, H.B. McNatt, W.M. Howell, and S.D. Peoples Gonopodium development in normal male and 11-ketotestosterone-treated female mosquitofish (Gambusia affinis): a quantitative study using computer image analysis Gen. Comp. Endocrinol. 123 2001 222 234
4. APHA (American Public Health Association), AWWA (American Water Works Association), WEF (Water Environment Federation) A.D. Eaton, L.S. Clesceri, E.W. Rice, A.H. Greenberg, Standard Methods for the Examination of Water and Wastewater 20th ed. 1998 American Public Health Association Washington, DC
5. I. Arismendi, B. Penaluna, and D. Soto Body condition indices as a rapid assessment of the abundance of introduced salmonids in oligotrophic lakes of southern Chile Lake Reserv. Manag. 27 2011 61 69
6. Z. Ayas, G. Ekmekci, M. Ozmen, and S.V. Yerli Histopathological changes in the livers and kidneys of fish in Sariyar Reservoir Turkey Environ. Toxicol. Pharmacol. 23 2007 242 249
7. S.F. Baird, and C.F. Girard Descriptions of new species of fishes collected by Mr. John H. Clark, on the U.S. and Mexican Boundary Survey under Lieutenant Colonel Jas D Graham Proc. Acad. Nat. Sci. Phila. 6 1853 387 390
8. J. Batty, and R. Lim Morphological and reproductive characteristics of male mosquitofish (Gambusia affinis holbrooki) inhabiting sewage-contaminated waters in New South Wales Australia Arch. Environ. Contam. Toxicol. 36 1999 301 307
9. D. Bernet, H. Schmidt, W. Meier, P. Burkhardt-Holm, and T. Wahli Histopathology in fish: proposal for a protocol to assess aquatic pollution J. Fish Dis. 22 1999 25 34
10. D. Bernet, H. Schmidt-Posthaus, T. Wahli, and P. Burkhardt-Holm Evaluation of two monitoring approaches to assess effects of waste water disposal on histological alterations in fish Hydrobiologia 524 2004 53 66
11. C. Björkblom, L. Salste, I. Katsiadaki, T. Wiklund, and L. Kronberg Detection of estrogenic activity in municipal wastewater effluent using primary cell cultures from three-spined stickleback and chemical analysis Chemosphere 73 2008 1064 1070
12. R.I. Bonansea, M.V. Amé, and D.A. Wunderlin Determination of priority pesticides in water samples combining SPE and SPME coupled to GC-MS. A case study: Suquéa River basin (Argentina) Chemosphere 90 2013 1860 1869
13. M.M.P. Camargo, and C.B.R. Martinez Histopathology of gills: kidney and liver of a Neotropical fish caged in an urban stream Neotrop. Ichthyol. 5 2007 327 336
14. CASAFE (Cámara de Sanidad Agropecuaria y Fertilizantes), 2011. Mercado Argentino 2011 de Productos Fitosanitarios. URL http://www.casafe.org (accessed May 17, 2014).
15. CCME (Canadian Council of Ministers of the Environment), 2013. Water Quality Guidelines for the Protection of Aquatic Life. Canadian Environmental Quality Guidelines. URL http://ceqg-rcqe.ccme.ca/ (accessed May 17, 2014).
16. E.I. Cengiz, and E. Ünlü Histopathological changes in the gills of mosquitofish: exposed to endosulfan Bull. Environ. Contam. Toxicol. 68 2002 290 296
17. E.I. Cengiz, and E. Ünlü Histopathology of gills in mosquitofish, Gambusia affinis after long-term exposure to sublethal concentrations of malathion J. Environ. Sci. Health Part B 38 2003 581 589
18. A. Chedid, L.M. Ryan, Y. Dayal, B.C. Wolf, and G. Falkson Morphology and other prognostic factors of hepatocellular carcinoma Arch. Pathol. Lab. Med. 123 1999 524 528
19. S.M. Choi, S.D. Yoo, and B.M. Lee Toxicological characteristics of endocrine-disrupting chemicals: developmental toxicity, carcinogenicity, and mutagenicity J. Toxicol. Environ. Health Part B 7 2010 1 24
20. P. Chomczynski, and N. Sacchi Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction Anal. Biochem. 162 1987 156 159
21. V. Contardo-Jara, L.N. Galanti, M.V. Amé, M.V. Monferrán, D.A. Wunderlin, and C. Wiegand Biotransformation and antioxidant enzymes of Limnoperna fortunei detect site impact in watercourses of Córdoba Argentina Ecotoxicol. Environ. Saf. 72 2009 1871 1880
22. P.M. Costa, S. Caeiro, J. Lobo, M. Martins, A.M. Ferreira, M. Caetano, and M.H. Costa Estuarine ecological risk based on hepatic histopathological indices from laboratory and in situ tested fish Mar. Pollut. Bull. 62 2011 55 65
23. P.M. Costa, M.S. Diniz, S. Caeiro, J. Lobo, M. Martins, A.M. Ferreira, and M.H. Costa Histological biomarkers in liver and gills of juvenile Solea senegalensis exposed to contaminated estuarine sediments: a weighted indices approach Aquat. Toxicol. 92 2009 202 212
24. Di Rienzo, J.A., Casanoves, F., Balzarini, M.G., Gonzalez, L., Tablada, M., Robledo, C.W., 2013. InfoStat Versión 2013. Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Argentina. URL http://www.infostat.com.ar (accessed May 17, 2014).
25. C. Dong, Z. Zeng, and X. Li Determination of organochlorine pesticides and their metabolites in radish after headspace solid-phase microextraction using calixarene arene fiber Talanta 66 2005 721 727
26. C.J. Doyle, and R.P. Lim The effect of 17beta-estradiol on the gonopodial development and sexual activity of Gambusia holbrooki Environ. Toxicol. Chem. 21 2002 2719 2724
27. C.A. Dyer Heavy Metals as Endocrine-Disrupting Chemicals A.C. Gore, Endocrine-Disrupting Chemicals: From Basic Research to Clinical Practice, Contemporary Endocrinology 2007 Humana Press Totowa, NJ 111 133
28. M.S. El-Shahawi, S. Hamza a Bashammakh a, and W.T. Al-Saggaf An overview on the accumulation, distribution, transformations, toxicity and analytical methods for the monitoring of persistent organic pollutants Talanta 80 2010 1587 1597
29. E. Fanta, F.S. Rios, S. Romão, A.C.C. Vianna, and S. Freiberger Histopathology of the fish Corydoras paleatus contaminated with sublethal levels of organophosphorus in water and food Ecotoxicol. Environ. Saf. 54 2003 119 130
30. K.D. Fausch, J. Lyons, J.R. Karr, and P.L. Angermeier Fish communities as indicators of environmental degradation Am. Fish. Soc. Symp. 8 1990 123 144 American Fisheries Society Symposium
31. A. Figueiredo-Fernandes, J.V. Ferreira-Cardoso, S. Garcia-Santos, S.M. Monteiro, J. Carrola, P. Matos, and A. Fontaínhas-Fernandes Histopathological changes in liver and gill epithelium of Nile tilapia Oreochromis niloticus exposed to waterborne copper Pesq. Vet. Bras. 27 2007 103 109
32. C. Flores Quintana Células cloro en peces teleósteos Rev. Vet. 20 2009 57 60
33. B. Fraile, F.J. Sáez, C.A. Vicentini, M.P. Miguel, and R. de Paniagua The testicular cycle of Gambusia affinis holbrooki (Teleostei: Poeciliidae) J. Zool. 228 1992 115 126
34. D.M. Gaiero, G.R. Ross, P.J. Depetris, and S. Kempe Spatial and temporal variability of total non-residual heavy metals content in stream sediments from the Suquia River system, Cordoba, Argentina Water Air Soil Pollut. 93 1997 303 319
35. E. García-Berthou, C. Alcaraz, Q. Pou-Rovira, L. Zamora, G. Coenders, and C. Feo Introduction pathways and establishment rates of invasive aquatic species in Europe Can. J. Fish. Aquat. Sci. 62 2005 453 463
36. C. Gonçalves, and M.F. Alpendurada Assessment of pesticide contamination in soil samples from an intensive horticulture area, using ultrasonic extraction and gas chromatography-mass spectrometry Talanta 65 2005 1179 1189
37. J.G. Haro, and M.A. Bistoni Ictiofauna de la provincia de Córdoba I.E. Di Tada, E.H. Bucher, Biodiversidad de La Provincia de Córdoba, Fauna 1996 Universidad Nacional de Río Cuarto/Centro de Zoología Aplicada Córdoba 169 190
38. A.C. Hued, and M.A. Bistoni Development and validation of a Biotic Index for evaluation of environmental quality in the central region of Argentina Hydrobiologia 543 2005 279 298
39. A.C. Hued, S. Dardanelli, and M.A. Bistoni Temporal and spatial variability of fish assemblages in a river basin with an environmental degradation gradient Community Ecol. 11 2010 41 50
40. A.C. Hued, F.L. Lo Nostro, D.A. Wunderlin, and M.A. Bistoni Reproductive impairment of a viviparous fish species inhabiting a freshwater system with anthropogenic impact Arch. Environ. Contam. Toxicol. 64 2013 281 290
41. ®) alters normal gill and liver histology and affects male sexual activity of Jenynsia multidentata (Anablepidae Cyprinodontiformes) Arch. Environ. Contam. Toxicol. 62 2012 107 117
42. I. Iavicoli, L. Fontana, and A. Bergamaschi The effects of metals as endocrine disruptors J. Toxicol. Environ. Health B. Crit. Rev. 12 2009 206 223
43. INDEC (Instituto Nacional de Estadísticas y Censos de la República Argentina), 2010. Censo Nacional de Población, Hogares y Viviendas 2010. URL http://www.casafe.orgwww.sig.indec.gov.ar/censo2010/ (accessed May 17, 2014).
44. IPCS - WHO. (International Programme on Chemical Safety - World Health Organization), 2010. The WHO recommended classification of pesticides by hazard and guidelines to classification: 2009. URL http://www.who.int/ipcs/publication/pesticides-hazard-2009.pdf (accessed May 17, 2014).
45. L. Järup Hazards of heavy metal contamination Br. Med. Bull. 68 2003 167 182
46. D. Kime Disruption of liver function D.E. Kime, Endocrine Disruption in Fish 1998 Springer US Boston 201 246
47. D.E. Kime, J.P. Nash, and A.P. Scott Vitellogenesis as a biomarker of reproductive disruption by xenobiotics Aquaculture 177 1999 345 352
48. L.D. Koller A note on eosinophilic cytoplasmic bodies in the liver of a rabbit Vet. Pathol. 10 1973 295 298
49. A. Larionov, A. Krause, and W. Miller A standard curve based method for relative real time PCR data processing BMC Bioinformatics 6 2005 62
50. Z. Lengyel, and R. Földényi Acetochlor as a soil pollutant Environ. Sci. Pollut. Res. 10 2003 13 18
51. F.D.L. Leusch, M.R. Van den Heuvel, A.D. Laurie, H.F. Chapman, S.R. Gooneratne, and L.A. Tremblay Quantification of vitellogenin mRNA induction in mosquitofish (Gambusia affinis) by reverse transcription real-time polymerase chain reaction (RT-PCR) Biomarkers 10 2005 429 438
52. H. Lin, and D. Randall 9 proton pumps in fish gills C.M. Wood, T.J. Shuttleworth, Fish Physiology 1995 Elsevier 229 255
53. T. Maggioni, A.C. Hued, M.V. Monferrán, R.I. Bonansea, L.N. Galanti, and M.V. Amé Bioindicators and biomarkers of environmental pollution in the middle-lower basin of the Suquía River (Córdoba Argentina) Arch. Environ. Contam. Toxicol. 63 2012 337 353
54. J. Mallatt Fish gill structural changes induced by toxicants and other irritants: a statistical review Can. J. Fish. Aquat. Sci. 42 1985 630 648
55. M. Mela, M. Randi, D. Ventura, C. Carvalho, E. Pelletier, and C. Oliveira Ribeiro Effects of dietary methylmercury on liver and kidney histology in the neotropical fish Hoplias malabaricus Ecotoxicol. Environ. Saf. 68 2007 426 435
56. C. Merlo, A. Abril, M.V. Amé, G.A. Argüello, H.A. Carreras, M.S. Chiappero, and V.M. Solís Integral assessment of pollution in the Suquía River (Córdoba: Argentina) as a contribution to lotic ecosystem restoration programs Sci. Total Environ. 409 2011 5034 5045
57. M.V. Monferrán, L.N. Galanti, R.I. Bonansea, M.V. Amé, and D.A. Wunderlin Integrated survey of water pollution in the Suquía River basin (Córdoba, Argentina) J. Environ. Monit. 13 2011 398 409
58. National Institutes of Health Guide for the care and use of laboratory animals eighth ed. 2011 National Academy Press Washington
59. V. Nero, A. Farwell, L.E.J. Lee, T. Van Meer, M.D. MacKinnon, and D.G. Dixon The effects of salinity on naphthenic acid toxicity to yellow perch: gill and liver histopathology Ecotoxicol. Environ. Saf. 65 2006 252 264
60. V. Nero, A. Farwell, A. Lister, G. Van der Kraak, L.E.J. Lee, T. Van Meer, and D.G. Dixon Gill and liver histopathological changes in yellow perch (Perca flavescens) and goldfish (Carassius auratus) exposed to oil sands process-affected water Ecotoxicol. Environ. Saf. 63 2006 365 377
61. J. Nimptsch, D.A. Wunderlin, A. Dollan, and S. Pflugmacher Antioxidant and biotransformation enzymes in Myriophyllum quitense as biomarkers of heavy metal exposure and eutrophication in Suquía River basin (Córdoba, Argentina) Chemosphere 61 2005 147 157
62. E. Orlando, W. Davis, T. Edwards, D. Sulkowski, G. Toft, and L. Guillette Mosquitofish as a sentinels of exposure to environmental androgens and estrogens M.C. Uribe, H.J. Grier, Viviparous Fishes 2005 New Life Publications Florida 435 453
63. Pait, A., Nelson, J., 2002. Endocrine Disruption in Fish An Assessment of Recent Research and Results. NOAA Tech. Memo. NOS NCCOS CCMA 149. Silver Spring, MD: NOAA, NOS, Center for Coastal Monitoring and Assessment 55pp.
64. Pasquini, A.I., Formica, S.M., Sacchi, G. a., 2011. Hydrochemistry and nutrients dynamic in the Suquía River urban catchment's, Córdoba, Argentina. Environ. Earth Sci. 65, 453-467.
65. S. Perry, and P. Laurent Adaptational responses of rainbow trout to lowered external NaCl concentration: contribution of the branchial chloride cell J. Exp. Biol. 147 1989 147 168
66. S.F. Pesce, J. Cazenave, M.V. Monferrán, S. Frede, and D.A. Wunderlin Integrated survey on toxic effects of lindane on neotropical fish: Corydoras paleatus and Jenynsia multidentata Environ. Pollut. 156 2008 775 783
67. S.F. Pesce, and D.A. Wunderlin Use of water quality index to verify the impact of Córdoba city (Argentina) on Suquía river Water Res. 34 2000 2915 2926
68. POPRC (Persistent Organic Pollutants Review Committee), 2010. Report of the Persistent Organic Pollutants Review Committee on the work of its sixth meeting (UNEP/POPS/POPRC.6/13), Annex I, Decision POPRC- 6/8. URL http://chm.pops.in/TheConvention/POPsReviewCommittee/Meetings/POPRC6/POPRC6Documents/tabi/783/Default.aspx (accessed May 17, 2014).
69. C.M. Porter, and D.M. Janz Treated municipal sewage discharge affects multiple levels of biological organization in fish Ecotoxicol. Environ. Saf. 54 2003 199 206
70. G.H. Pyke A review of the biology of Gambusia affinis and G holbrooki Rev. Fish Biol. Fish. 15 2005 339 365
71. Rasband, W.S.,2012. ImageJ. U.S. National Institutes of Health, Bethesda, Maryland, USA,1; 1997-2012. URL http://imagej.nih.gov/ij/ (accessed May 17, 2014).
72. S.A. Raut, and R.A. Angus Triclosan has endocrine-disrupting effects in male western mosquitofish: Gambusia affinis Environ. Toxicol. Chem. 29 2010 1287 1291
73. SENASA (Servicio Nacional de Sanidad y Calidad Agroalimentaria), 2011. Resolución 511/2011: Endosulfán. URL http://www.senasa.gov.ar/contenido.php?to=n&in=1501%20&io=17737 (accessed May 17, 2014).
74. P.B. Singh, and V. Singh Cypermethrin induced histological changes in gonadotrophic cells, liver, gonads, plasma levels of estradiol-17b and 11-ketotestosterone, and sperm motility in Heteropneustes fossilis (Bloch) Chemosphere 72 2008 422 431
75. R. Sokal, and F. Rohlf Biometry: The Principles and Practice of Statistics Biological Research third ed. 1995 W.H. Freeman New York
76. K.R. Solomon, J. Carr, L.H. a Du Preez, J.P. Giesy, R.J. Kendall, E.E. Smith, and G.J. Van Der Kraak Effects of atrazine on fish amphibians, and aquatic reptiles: a critical review Crit. Rev. Toxicol. 38 2008 721 772
77. SRHN (Subsecretaría de Recursos Hídricos de la Nación), 2004. Niveles Guía Nacionales de Calidad de Agua Ambiente. Subsecretaría de Recursos Hídricos de la Nación, República Argentina.
78. R.J. Strange Field examination of fish B.R. Murphy, D.W. Willis, Fisheries Techniques 1996 American Fisheries Society Bethesda, Maryland 443 446
79. J.P. Sumpter, and S. Jobling Vitellogenesis as a biomarker for estrogenic contamination of the aquatic environment Environ. Health Perspect. 103 1995 173 178
80. M. Tankiewicz, J. Fenik, and M. Biziuk Determination of organophosphorus and organonitrogen pesticides in water samples TrAC Trend Anal. Chem. 29 2010 1050 1063
81. G. Toft, E. Baatrup, and L.J. Guillete Jr. Altered social behavior and sexual characteristics in mosquitofish (Gambusia holbrooki) living downstream of a paper mill Aquat. Toxicol. 70 2004 213 222
82. G. Toft, T.M. Edwards, E. Baatrup, and L.J. Guillette Disturbed sexual characteristics in male mosquitofish (Gambusia holbrooki) from a lake contaminated with endocrine disruptors Environ. Health Perspect. 111 2003 695 701
83. I.C. Troncoso, J. Cazenave, C. Bacchetta, and Bistoni M. de Histopathological changes in the gills and liver of Prochilodus lineatus from the Salado River basin (Santa Fe, Argentina) Fish Physiol. Biochem. 38 2012 693 702
84. C.L. Turner Morphogenesis of the gonopodium in Gambusia affinis affinis J. Morphol. 69 1941 161 185
85. R. Van der Oost, J. Beyer, and N.P.E. Vermeulen Fish bioaccumulation and biomarkers in environmental risk assessment: a review Environ. Toxicol. Pharmacol. 13 2003 57 149
86. J.C. Van Dyk, G.M. Pieterse, and J.H.J. van Vuren Histological changes in the liver of Oreochromis mossambicus (Cichlidae) after exposure to cadmium and zinc Ecotoxicol. Environ. Saf. 66 2007 432 440
87. J.B. Vázquez, A. López Robles, D.F. Sosa, and M.P. Saez Aguas J.B. Vázquez, R.A. Miatello, M.E. Roque, Geografía Física de La Provincia de Córdoba 1979 Boldt Buenos Aires 139 211
88. I. Velcheva, E. Tomova, D. Arnaudova, and A. Arnaudov Morphological investigation on gills and liver of freshwater fish from Dam Lake Studen Kladenets Bulg. J. Agric. Sci. 16 2010 364 368
89. B. Velmurugan, T. Mathews, and E.I. Cengiz Histopathological effects of cypermethrin on gill, liver and kidney of fresh water fish Clarias gariepinus (Burchell, 1822), and recovery after exposure Environ. Technol. 30 13 2009 1453 1460
90. O. Vidal, E. García-Berthou, P.A. Tedesco, and J.L. García-Marín Origin and genetic diversity of mosquitofish (Gambusia holbrooki) introduced to Europe Biol. Invasions 12 2010 841 851
91. S. Wen-ting, L. Hai-yan, and W. Zhi-jun Estrogenic effect of effluent from municipal sewage treatment plant on juvenile goldfish (Carassius auratus) 2011 International Conference on Electronics, Communications and Control (ICECC) 2011 IEEE 3731 3734
92. B. Wielgomas, and J. Krechniak Effect of alpha-cypermethrin and chlorpyrifos in a 28-day study on free radical parameters and cholinesterase activity in Wistar rats Polish J. Environ. Stud. 16 2007 91 95
93. C.M. Wood Toxic responses of the gill D. Schlenk, W.H. Benson, Target Organ Toxicity in Marine and Freshwater Teleosts vol. 1 2001 Taylor & Francis London, New York 1 89
94. D.A. Wunderlin, M.P. Díaz, M.V. Amé, S.F. Pesce, A.C. Hued, and M.A. Bistoni Pattern recognition techniques for the evaluation of spatial and temporal variations in water quality. A case study: Suquía River Basin (Cordoba-Argentina) Water Res. 35 2001 2881 2894