Biomarkers; Clarias gariepinus; Gonad and liver histopathology; Sex steroids; Tilapia guineensis
Abstract :
[en] To determine the impact of agricultural pesticides used in cotton cultivation on the health status of fish living in a Beninese cotton basin, we compared the reproductive and hepatic systems of fish sampled from rivers located in both contaminated and pristine conditions. Different types of biomarkers, including biometric indices (a condition factor K, a gonadosomatic index GSI, and a hepatosomatic index HSI), plasma levels of sex steroids (11-ketotestosterone 11-KT, testosterone T and estradiol-17beta E2) and the histopathology of the gonads and liver, were investigated for two different trophic levels of the following two fish species: the Guinean tilapia Tilapia guineensis and the African catfish Clarias gariepinus. The fish were captured during both the rainy season (when there is heavy use of pesticides on cotton fields) and the dry season from one site, in Pendjari River (reference site), which is located outside the cotton-producing basin, and from three other sites on the Alibori River within the cotton-producing basin. Comparing fish that were sampled from contaminated (high levels of endosulfan, heptachlor and DDT and metabolites) and reference sites, the results clearly indicated that agricultural pesticides significantly decreased K and GSI while they increased HSI, regardless of the season, species and sex of the fish. These pesticides also induced a decrease in the plasma levels of 11-KT and T and increased those of E2. The histopathology of the testes revealed, in both species, a high rate of testicular oocytes, up to 50% in the African catfish, downstream of the Alibori River, which indicated estrogenic effects from the pesticides. The disruption of male spermatogenesis primarily included necrosis, fibrosis and the presence of foam cells in the lobular lumen. The histopathology of the ovaries revealed high levels of pre-ovulatory follicular atresia, impaired oogenesis, a decrease in the oocyte vitellogenic diameter and other lesions, such as fibrosis, vacuolation and melano-macrophagic centers. The histopathology of the liver revealed the presence of necrosis, hypertrophic hepatocytes, foci of vacuolation, glycogen depletion and hemosiderin. An assessment of the general health of the fish indicated that all of the sampled fish from the polluted sites were in poorer health compared with those from the reference site but that the African catfish appeared much more affected than the Guinean tilapia, regardless of the sex and season. In conclusion, the overall results indicated that agricultural pesticides significantly impair the endocrine regulation of fish living in the Beninese cotton basin and that this would most likely be one of the causes of the severe damage observed in the liver and gonads and the reduced health condition.
Disciplines :
Veterinary medicine & animal health
Author, co-author :
Agbohessi, Prudencio T.
Imorou Toko, Ibrahim
Ouedraogo, Alfred
Jauniaux, Thierry ; Université de Liège - ULiège > Département de morphologie et pathologie > Département de morphologie et pathologie
Mandiki, S. N. M.
Kestemont, Patrick
Language :
English
Title :
Assessment of the health status of wild fish inhabiting a cotton basin heavily impacted by pesticides in Benin (West Africa).
Publication date :
2015
Journal title :
Science of the Total Environment
ISSN :
0048-9697
eISSN :
1879-1026
Publisher :
Elsevier, Netherlands
Volume :
506-507
Pages :
567-584
Peer reviewed :
Peer Reviewed verified by ORBi
Commentary :
Copyright (c) 2014 Elsevier B.V. All rights reserved.
Agagbé A.A. Etude écotoxico-chimique des résidus de pesticides dans le bassin-versant de la rivière Agbado par la technique d'analyse ELISA en phase solide. Thèse d'ingénieur des travaux en aménagement et protection de l'environnement 2008, Université d'Abomey-Calavi, Bénin, [65 pp.].
Agbohessi T.P., Imorou Toko I., Yabi A.J., Dassoundo-Assogba J.F.C., Kestemont P. Caractérisation des pesticides chimiques utilisés en production cotonnière et impact sur les indicateurs économiques dans la Commune de Banikoara au nord du Bénin. Int J Biol Chem Sci 2011, 5:1828-1841.
Agbohessi T.P., Imorou Toko I., Kestemont P. Etat des lieux de la contamination des écosystèmes aquatiques par les pesticides organochlorés dans le bassin cotonnier béninois. Cah Agric 2012, 21:46-56.
Agius C., Roberts R.J. Melano-macrophage centers and their role in fish pathology. J Fish Dis 2003, 9:499-509.
Albinati A.C.L., Moreira E.L.T., Albinati R.C.B., Carvalho J.V., Santos G.B., Lira A.D. Toxicidade aguda do herbicida Roundup_ parapiauçu (Leporinus macrocephalus). Rev Bras Sau'de Prod Anim 2007, 8:184-192.
Albinati A.C.L., Moreira E.L.T., Albinati R.C.B., Carvalho J.V., De Lira A.D., Santos G.B., et al. Histological biomarkers - chronic toxicity for roundup in piauçu (Leporinus macrocephalus). Arq Bras Med Vet Zootec 2009, 61:621-627.
Alvarez M., del C, Fuiman L.A. Environmental levels of atrazine and its degradation products impair survival skills and growth of red drum larvae. Aquat Toxicol 2005, 74:229-241.
Amaral A.F., Alvarado N., Maria G.I., Cunha R., Hylland K., Soto M. Autometallography and metallothione in immunohistochemistry in hepatocytes of turbot (Scophthalmus maximus L.) after exposure to cadmium and depuration treatment. Biomarkers 2002, 7:491-500.
Aravindakshan J., Paquet V., Gregory M., Dufresne J., Fournier M., Marcogliese D.J., et al. Consequences of xenoestrogen exposure on male reproductive function in spottail shiners (Notropis hudsonius). Toxicol Sci 2004, 78:156-165.
Arunachalam S., Jeyalakshmi K., Aboubucker S. Toxic and sublethal effects of carbaryl on a fresh water Catfish, Mystus vittatus. Arch Environ Contam Toxicol 1980, 9:307-316.
Association Interprofessionnelle de Coton Plan de campagne agricole cotonnière 2009-2010 et perspective 2010-2011 2009, Presse de l'AIC, Cotonou, [235 pp.].
Assongba M. Recherche de résidus de pesticides organochlorés et de PCBs dans les exploitations agricoles de Banikoara. Analyse par chromatographie en phase gazeuse couplée à une détection à capture d'électron (CPG/ECD). - Mémoire de fin de formation d'Ingénieur des Travaux en Techniques d'Aménagement et Protection de l'Environnement, APE/CPU 1996, [196 pp.].
Australian Pesticides and Veterinary Medicines Authority Evaluation of the new active flubendiamide in the production BELT 480 SC insecticide and BELT 240 WG insecticide. Commonwealth of Australia Gazette No. APVMA 2-3 Février 2009. Agricultural and veterinary chemicals code Act 1994 2009, [http://www.apvma.gov.au/ registration/ assessment/ docs/prs_flubendiamide.pdf. Accessed 28 Dec 2013].
Barja-Fernandez S., Miguez J.M., Alvarez-Otero R. Histopathological effects of 2,2',4,4'-tetrabromodiphenyl ether (BDE-47) in the gills, intestine and liver of turbot (Psetta maxima). Ecotoxicol Environ Saf 2013, 95:60-68.
Barnhoorn I.E.J., Bornman M.S., Pieterse G.M., Van Vuren J.H.J. Histological evidence of intersex in feral sharptooth catfish (Clarias gariepinus) from an estrogen-polluted water source in Gauteng, South Africa. Environ Toxicol 2004, 19:603-608.
Barse A.V., Chakrabarti T., Ghosh T.K., Pal A.K., Jadhao S.B. Endocrine disruption and metabolic changes following exposure of Cyprinus carpio to diethyl phthalate. Pest Biochem Physiol 2007, 88:36-42.
Bernet D., Schmidt H., Meier W., Berkhardt-Holm P., Wahli T. Histopathology in fish: proposal for a protocol to assess aquatic pollution. J Fish Dis 1999, 22:25-43.
Binkowski Q.J., Sawicka-Kapusta K., Szarek J., Strzyzewska E., Felsmann M. Histopathology of liver and kidneys of wild living Mallards Anas platyrhynchos and Coots Fulica atra with considerable concentrations of lead and cadmium. Sci Total Environ 2013, 450/451:326-333.
Boumaiza M., Ktari M.H., Vitiello P. Acute toxicity for Aphanius fasciatus of various pesticides used in Tunisia. Arch Inst Pasteur Tunis 1979, 56:307-342.
Bucke D., Watermann B., Feist S. Histological variations of hepato-splenic organs from the North Sea dab, Limanda limanda (L.). J Fish Dis 1984, 7:255-268.
Cek S., Yilmaz E. Gonad development and sex ratio of sharptooth catfish (Clarias gariepinus Burchell, 1822) cultured under laboratory conditions. Turk J Zool 2007, 31:35-46.
CENAGREF (Centre National de Gestion des Réserves de Faune) Etude de l'impact de l'utilisation des engrais chimiques et des pesticides par les populations riveraines sur les écosystèmes (eau de surface, végétaux et faunes) des Aires Protégées (Parcs Nationaux et zones cynégétiques) du Bénin. Rapport final d'expertise 2004, [168 pp.].
Cengiz E.I., Unlu E., Balci K. The histopathological effects of thiodan on the liver and gut of mosquitofish, Gambusia affinis. J Environ Sci Health B 2001, 36:75-85.
CeRPA-Borgou/Alibori (Centre Régional pour la promotion Agricole Borgou-Alibori) Rapport du constat de l'empoisonnement d'une poche d'eau du fleuve Ouémé supérieur 2013, [27 pp.].
Chakrabarty S., Rajakumar A., Raqhuveer K., Sridevi P., Mohanachary A., Prathibha Y., et al. Endosulfan and flutamide, alone and in combination, target ovarian growth in juvenile catfish, Clarias batrachus. Comp Biochem Physiol Part C 2012, 155:491-497.
Chang J., Liu S., Zhou S., Wang M., Zhu G. Effects of butachlor on reproduction and hormone levels in adult zebrafish (Danio rerio). Exp Toxicol Pathol 2011, 65:205-209.
Chao W., Guanghua L., Jing C., Perfang W. Sub-lethal effects of pesticide mixtures on selected biomarkers of Carassius auratus. Environ Toxicol Pharmacol 2009, 28:414-419.
Chen H., Xiao J., Hu G., Zhou J., Xiao H., Wang X. Estrogenicity of organophosphorus and pyrethroid pesticides. J Toxicol Environ Health A 2002, 65:1419-1435.
Chinah A.C., Sikoki F.D., Vincent-Akpu I. Toxicity of an organophosphate pesticide (chlorpyrifos) on a common Niger Delta wetland fish Tilapia Guineensis (Blecker 1862). J Appl Sci Environ Manag 2004, 8:11-17.
Christiansen T., Korsgaard B., Jespersen A. Effects of nonylphenol and 17-β oestradiol on vitellogenin synthesis, testicular structure and cytology in male eelpout (Zoarces viviparous). J Exp Biol 1998, 201:179-192.
Coimbra A.M., Figueiredo-Fernandes A., Reis-Henriques M.A. Nile tilapia (Oreochromis niloticus), liver morphology, CYP1A activity and thyroid hormones after endosulfan dietary exposure. Pest Biochem Physiol 2007, 89:230-236.
Cook L.W., Paradise C.J., lom B. The pesticide malathion reduces survival and growth in developing zebrafish. Environ Toxicol Chem 2005, 24:1745-1750.
Corsi I., Mariottini M., Sensini C., Lancini L., Focardi S. Cytochrome P450, acetylcholinesterase and gonadal histology for evaluating contaminant exposure levels in fishes from highly eutrophic brackish ecosystem: the Orbetello Lagon, Italy. Mar Pollut Bull 2003, 46:203-212.
Coz-Rakovac R., Strunjak-Perovic I., Topicpopovic N., Hacmanjek M., Smuc T., Jadan M., et al. Cage culture effects on mullets (Mugilidae) liver histology and blood chemistry profile. J Fish Biol 2008, 72:2557-2569.
Da Cuña R.H., Pandolfi M., Genovese G., Piazza Y., Ansaldo M., Lo Nostro F.L. Endocrine disruptive potential of endosulfan on the reproductive axis of Cichlasoma dimerus (Perciformes, Cichlidae). Aquat Toxicol 2013, 126:299-305.
De Vlaming V.L. Oocyte development patterns and hormone involvements among teleosts. Control processes in Fish physiol 1983, 176-199. Croom Helm, London. J.C. Rankin, T.J. Pitcher, T.J. Duggan (Eds.).
Dem S.B., Cobb J.M., Mullins D.E. Pesticide residues in soil and water from four cotton growing areas of Mali, West Africa. J Agric Food Environ Sci 2007, 1:1-12.
Ezemonye L.I.N., Ikpesu T.O. Evaluation of sub-lethal effects of endosulfan on cortisol secretion, glutathione S-transferase and acetylcholinesterase activities in Clarias gariepinus. Food Chem Toxicol 2011, 49:1898-1903.
Fanta E., Rios F.S., Romano S., Vianna A.C.C., Freiberger S. Histopathology of the fish Corydoras paleatus contaminated with sub-lethal levels of organophosphorus in water and food. Ecotoxicol Environ Saf 2003, 54:119-130.
Flammarion P., Devaux A., Garric J. Marqueurs biochimiques de pollution dans les écosystèmes aquatiques continentaux. Exemples d'utilisation et perspectives pour les gestionnaires. Bull Fr Pêche Piscic 2000, 257/258:209-226.
Foerson L.L., DeFur P.L., Tuberty S. Effects of endosulfan on moulting in juvenile red swamp crayfish, Procambarus clarkii. Annual meeting of the Society of Environmental Toxicology and Chemistry 2001, SETAC Press, Baltimore MD, Pensacola FL.
Fostier A., Jalabert B. Steroidogenesis in rainbow trout (Salmo gairdneri) at various pre-ovulatory stages: changes in plasma hormone levels and in vivo and in vitro responses of the ovary to salmon gonadotropin. Fish Physiol Biochem 1986, 2:87-99.
Gillium R.J. Pesticides in U.S. streams and groundwater. Environ Sci Technol 2007, 41:3407-3413.
Gimeno S., Gerritsen A., Bowmer T., Komen H. Feminization of male carp. Nature 1996, 384:221-222.
Gimeno S., Komen H., Jobling S., Sumpter J., Bowmer T. Demasculinisation of sexually mature male common carp, Cyprinus carpio, exposed to 4-tert-pentylphenol during spermatogenesis. Aquat Toxicol 1998, 43:93-109.
Gingerich W.H. Hepatic toxicology of fishes. Aquat toxicol 1982, 55-105. Raven Press, New York, NY. L.J. Weber (Ed.).
Gounou A. Etude d'impact environnemental et social de l'installation d'une réserve villageoise dans la Commune de Banikoara. Rapport définitif de la mission 003/08/ED/CGP, publie' par l'Association ED, CENAGREF Fondation IGF, Cotonou, Benin, West Africa 2009.
Grébil G., Novak S., Perrin-Ganier C., Schavion M. La dissipation des produits phytosanitaires appliqués au sol. Ingénieries N° special 2001, 31-44.
Gul A. Investigation of acute toxicity of chlorpyrifos - methyl on Nile tilapia (Oreochromis niloticus L.) larvae. Chemosphere 2005, 59:163-166.
Haaparanta A., Valtonen E.T., Hoffmann R., Holmes J. Do macrophage centers in freshwater fishes reflect the differences in water quality?. Aquat Toxicol 1996, 34:253-272.
Handy R.D., Depledge M.H. Physiological responses: their measurement and use as environmental biomarkers in ecotoxicology. Ecotoxicol 1999, 8:329-349.
Hanson R., Dadoo D.K., Essumang D.K., Blay J., Kjr Yankson The effect of some selected pesticides on the growth and reproduction of fresh Oreochromis niloticus, Chrysicthys nigrodigitatus and Clarias gariepinus. Bull Environ Contam Toxicol 2007, 79:544-547.
Hayes T.B., Case P., Chui S., Chung D., Haeffele C., Haston K., et al. Pesticide mixtures, endocrine disruption, and amphibian declines: are we underestimating the impact?. Environ Health Persp 2006, 114:40-50.
Hibiya T. An atlas of fish histology: normal and pathological features, Kodansha Ltd. Tokyo 1982.
Idieti M.E. Variabilité hydro-climatique dans le basin versant de la Pendjari au Bénin (Nord-Ouest du Bénin) 2009, Université d'Abomey-Calavi, [59 pp.].
Iwata H., Tanabe S., Sakal N., Tatsukawa R. Distribution of persistent organochlorines in the oceanic air and surface seawater and the role of ocean on their global transport and fate. Environ Sci Technol 1993, 27:1080-1098.
Jiraungkoorskul W., Upatham E.S., Kruatrachue M., Sahaphong S., Vichasri-Grams S., Pokethitiyook P. Histopathological effects of round up, a glyphosate herbicide on Nile tilapia (Oreochromis niloticus). Sci Asia 2002, 28:121-127.
Jiraungkoorskul W., Upatham E.S., Kruatrachue M., Sahaphong S., Vichasri-Grams S., Pokethitiyook P. Biochemical and histopathological effects of glyphosate herbicide on Nile tilapia (Oreochromis niloticus). Environ Toxicol 2003, 18:260-267.
Jobling S., Sheahan D., Osborne J.A., Matthiessen P., Sumpter J.P. Inhibition of testicular growth in rainbow trout (Oncorhynchus mykiss) exposed to estrogenic alkylphenolic chemicals. Environ Toxicol Chem 1996, 15:194-202.
Katary A. Etude spatio-temporelle de la gestion de la résistance de Helicoverpa armigera (Hubner, 1808) aux Pyréthrinoyides en culture cotonnière au Bénin. Thèse de Docteur d'Etat ès Sciences Naturelles de l'Université d'Abomey-Calavi (Bénin) 2004, [331 pp.].
Lal B., Sarang M.K., Kumar P. Malathion exposure induces the endocrine disruption and growth retardation in the catfish Clarias batrachus (Linn). General and Comparative Endocrinology 2013, 181:139-145.
Langiano V.C., Martinez C.B.R. Toxicity and effects of a glyphosate based herbicide on the neotropical fish Prochilodus lineatus. Comp Biochem Physiol Part C 2008, 147:222-231.
Lavergne-Slove A., Mosnier J.F. Lésions élémentaires des cellules, tissus et organes (Chapitre 2). Copyright AFECAP 2005, [27 pp.].
Leino R.L., Jensen K.M., Ankley G.T. Gonadal histology and characteristic histopathology associated with endocrine disruption in the adult fathead minnow (Pimephales promelas). Environ Toxicol Pharmacol 2005, 19:85-98.
Leknes I.L. Melano-macrophage centers in liver of platyfish, Xiphophorus maculatus, Poeciliidae: Teleostei. Zool 2004, 107:201-204.
Le Mer C., Roy L.R., Pellerin J., Couillard C.M., Maltais D. Effects of chronic exposures to the herbicides atrazine and glyphosate to larvae of the threespine stickleback (Gasterosteus aculeatus). Ecotoxicol Environ Saf 2013, 89:174-181.
Louiz I., Ben-Attia M., Ben-Hassine O.K. Gonadosomatic index and gonad histopathology of Gobius niger (Gobiidea, Teleost) from Bizerta lagoon (Tunisia): evidence of reproduction disturbance. Fish Sci 2009, 100:266-273.
Mandiki S.N., Houbart M., Babiak I., Vandeloise E., Gardeur J.N., Kestemont P. Are sex steroids involved in the sexual growth dimorphism in Eurasian perch juveniles?. Physiol Behav 2004, 80:603-609.
Marchand M.J., Pieterse G.M., Barnhoorn I.E.J. Sperm motility and testicular histology of two feral fish species from a currently DDT-sprayed area, South Africa. J Appl Ichthyol 2008, 24:423-429.
Mawussi G. Bilan environnemental de l'utilisation de pesticides organochlorés dans les cultures de coton, café et cacao au Togo et recherches d'alternatives par l'évaluation du pouvoir insecticide d'extraits de plantes locales contre le scolyte du café (Hypothenemus hampei ferrari). Thèse de doctorat de l'université de Toulouse 2008, [http://ethesis.inp-toulouse.fr/archive/00000935/01/mawussi.pdf].
McCarthy A.R., Thomson B.M., Shaw I.C., Abella A.D. Estrogenicity of pyrethroid insecticide metabolites. J Environ Monit 2006, 8:197-202.
McKinlay R., Plant J.A., Bell J.N.B., Voulvoulis N. Endocrine disrupting pesticides: implications for risk assessment. Environ Int 2007, 34:170-172.
Mckinlay R., Plant J.A., Bell J.N.B., Voulvoulis N. Endocrine disrupting pesticides: implications for risk assessment. Environ Int 2008, 34:168-183.
Mdegela R.H., Braathen M., Mosha R.D., Skaare J.U., Sandvik M. Assessment of pollution in sewage ponds using biomarker responses in wild African sharptooth catfish (Clarias gariepinus) in Tanzania. Ecotoxicol 2010, 19:722-734.
Meier S., Andersen T.E., Norberg B., Thorsen A., Taranger G.L., Kjesbu O.S., et al. Effects of alkylphenols on the reproductive system of Atlantic Cod (Gadus morhua). Aquat Toxicol 2007, 81:207-218.
MEPN (Ministère de l'Environnement et de la Protection de la Nature) Quatrième rapport national du Bénin sur la convention des Nations Unies sur la diversité biologique 2009.
Micheletti C., Critto A., Marcomini A. Assessment of ecological risk from bioaccumulation of PCDD/Fs and dioxin-like PCBs in a coastal lagoon. Environ Int 2007, 33:45-55.
Mills L.J., Gutjahr-Grobell R.E., Haebler R.A., Borsay Horowitz D.J., Jayaraman S., Pruell R.J., et al. Effects of estrogenic (o,p_-DDT; octylphenol) and anti-androgenic (p,p_-DDE) chemicals on the indicators of endocrine status in juvenile male summer flounder (Paralichthys dentatus). Aquat Toxicol 2001, 52:157-176.
Miura C., Takahashi N., Michino F., Miura T. The effect of paranonylphenol on Japanese eel (Anguilla japonica) spermatogenesis in vitro. Aquat Toxicol 2005, 71:133-141.
Mlambo S.S., van Vuren J.H.J., Barnhoorn I.E.J., Bornman M.S. Histopathological changes in the reproductive system (ovaries and testes) of Oreochromis mossambicus following exposure to DDT. Environ Toxicol Pharmacol 2009, 28:133-139.
Murty A.S., Devi A.P. The effect of endosulfan and its isomers on tissue protein, glycogen, and lipids in the fish Channa punctata. Pest Biochem Physiol 1982, 17:280-286.
Nadzialek S., Kestemont P. 17α-Ethinylestradiol induces an imbalance between apoptosis and cell proliferation in a testis culture of gudgeon Gobio gobio. Environ Toxicol Chem 2010, 29:881-886.
Nadzialek S., Pigneur L.M., Wéron B., Kestemont P. Bcl-2 and caspase 3 mRNA levels in the testes of gudgeon, Gobio gobio, exposed to ethinylestradiol (EE2). Aquat Toxicol 2010, 98:304-310.
Noyes P.D., Hinton D.E., Stapleton H.M. Accumulation and debromination of decabromodiphenyl ether (BDE-209) in juvenile fathead minnows (Pimephales promelas) induces thyroid disruption and liver alterations. Toxicol Sci 2011, 122:265-274.
Okounmassoun L., Brochu C., Deblois C. Vitellogenin in tilapia male fishes exposed to organochlorine pesticides in Ouémé River in Republic of Benin. Sci Total Environ 2002, 299:163-172.
Olarinmoye O.M., Taiwo V.O., Clarke E.O., Kumolu-Johson C.A., Aderinola O.J., Adekunbi F. Hepatic pathologies in the brakish water catfish (Chrysicthys nigrodigitatus) from contaminated locations of the Lagos lagoon complex. Afr J Biotechnol 2011, 10:15058-15064.
OMS Environmental health criteria 124 Lindane 1991, [28 pp.].
OMS-PNUE Etat de l'art sur les perturbateurs endocriniens. Extraits choisis concernant les pesticides perturbateurs endocriniens. Publication state of the science of endocrine disrupting chemicals 2012 2013, Rapport OMS-PNUE, [15 pp.].
Oruç E.O. Oxidative stress, steroid hormone concentrations and acetylcholinesterase activity in Oreochromis niloticus exposed to chlorpyrifos. Pest Biochem Physiol 2010, 96:160-166.
Palma P., Palma V.L., Fernandes R.M., Soares A.M.V.M., Barbosa I.R. Acute toxicity of atrazine, endosulfan sulphate and chlorpyrifos to Vibrio fischeri, Thamnocephalus platyurus and Daphnia magna, relative to their concentrations in surface waters from the Alentejo region of Portugal. Bull Environ Contam Toxicol 2008, 81:485-489.
Palma P., Palma V.L., Fernandes R.M., Soares A.M.V.M., Barbosa I.R. Endosulfan sulphate interferes with reproduction, embryonic development and sex differentiation in Daphnia magma. Ecotoxicol Environ Saf 2009, 72:344-350.
Palma P., Palma V.L., Matos C., Fernandes R.M., Bohn A., Soares A.M.V.M., et al. Assessment of the pesticides atrazine endosulfan sulphate and chlorpyrifos for juvenoid-related endocrine activity using Daphnia magna. Chemosphere 2009, 76:335-340.
Pazou E.Y., Lalèyè P., Boko M., van Gestel C.A., Ahissou H., Akpona S., et al. Contamination of fish by organochlorine pesticide residues in the Ouémé River catchment in the Republic of Benin. Environ Int 2006, 32:594-599.
Petri D., Glover C.N., Ylving S., Kolås K., Fremmersvik G., Waagbø R., et al. Sensitivity of Atlantic salmon (Salmo salar) to dietary endosulfan as assessed by haematology, blood biochemistry, and growth parameters. Aquat Toxicol 2006, 80:207-216.
Pieterse G.M., Marchand M.J., van Dyk J.C., Barnhoorn I.E.J. Histological alterations in the testes and ovaries of the sharptooth catfish (Clarias gariepinus) from an urban nature reserve in South Africa. J Appl Ichthyol 2010, 26:789-793.
Primentel D., Levitain L.C. Pesticides. Amounts applied and amount reaching pests. Often, less than 0.1% of pesticides applied to crop reach target pests. Biosci 1986, 36:86-91.
Purdom C.E., Hardiman P.A., Bye V.J., Eno N.C., Tyler C.R., Sumpter J.P. Estrogenic effects of effluents from sewage treatment works. Chem Ecol 1994, 8:275-285.
Rajakumar A., Singh R., Chakrabarty S., Murugananthkumar R., Laldinsangi C., Prathibha Y., et al. Endosulfan and flutamide impair testicular development in the juvenile Asian catfish, Clarias batrachus. Aquat Toxicol 2012, 110/111:123-132.
Rajapakse N., Silva E., Kortenkamp A. Combining xenoestrogens at levels below individual no-observed effect concentration dramatically enhances steroid hormone action. Environ Health Perspect 2002, 10:917-921.
Rinchard J., Kestemont P. Comparative study of reproductive biology in single and multiple spawned cyprinid fish. Morphological and histological features. J Fish Biol 1996, 49:883-894.
Roberts R.J. Fish pathology. 3rd Ed WB Saunders 2001, [Philadelphia].
Rotchell J.M., Ostrander G.K. Molecular markers of endocrine disruption in aquatic organisms. J Toxicol Environ 2003, 302:167-184.
Safahieh A., Hedayati A., Savari A., Movahedinia A. Effect of sub-lethal dose of mercury toxicity on liver cells and tissue of yellow sea bream. Toxicol Ind Health 2012, 28:583-592.
Sayed Ael-D., Mahmoud U.M., Mekkawy I.A. Reproductive biomarkers to identify endocrine disruption in Clarias gariepinus exposed to 4-nonylphenol. Ecotoxicol Environ Saf 2012, 78:310-319.
Scholz S., Gutzeit H.O. 17-Alpha-ethinylestradiol affects reproduction, sexual reproduction, sexual differentiation and aromatase gene expression of the medaka (Oryzias latipes). Aquat Toxicol 2000, 50:363-373.
Simpson E.R., Mahendroo M.S., Means G.D., Kilgore M.W., Hinshelwood M.M., Graham-Laurence S., et al. Aromatase cytochrome P450, the enzyme responsible for estrogen biosynthesis. Endocrinol Rev 1994, 15:342-354.
Singh P.B., Singh V. Exposure and recovery response of isomers of HCH, metabolites of DDT and estradiol-17β in the female catfish, Heteropneustes fossilis. Environ Toxicol Pharmacol 2007, 24:245-251.
Singh P.B., Singh V. Bioaccumulation of hexachlorocyclohexane, dichlorodiphenyltrichloroethane, and estradiol-17β in catfish and carp during pre-monsoon season in India. Fish Physiol Biochem 2008, 34:25-36.
Singh P.B., Singh V. Pesticide bioaccumulation and plasma sex steroids in fishes during breeding phase from north India. Environ Toxicol Pharmacol 2008, 25:342-350.
Soso A.B., Barcellos L.J.G., Ranzani-Paiva M.J., Kreutz L.C., Quevedo R.M., Anziliero D., et al. Chronic exposure to sub-lethal concentration of a glyphosate-based herbicide alters hormone profiles and affects reproduction of female Jundia (Rhamdia quelen). Environ Toxicol Pharmacol 2007, 23:308-313.
Soverchia L., Ruggeri B., Palermo F., Mosconi G., Cardinaletti G., Scortichini G., et al. Modulation of vitellogenin synthesis through estrogen receptor beta-1 in goldfish (Carassius auratus) juveniles exposed to 17-β estradiol and Nonylphenol. Toxicol Appl Pharmacol 2005, 209:236-243.
Spano L., Tyler C.R., van Aerle R., Devos P., Mandiki S.N., Silvestre F., et al. Effects of atrazine on sex steroid dynamics, plasma vitellogenin concentration and gonad development in adult goldfish (Carassius auratus). Aquat Toxicol 2004, 66:369-379.
Srivastava A.K., Srivastava A.K. Effect of chlordecone on gonads of freshwater catfish, Heteropneustes fossilis. Bull Environ Contam Toxicol 1991, 53:186-191.
Sun P.L., Tsai S.S. Intersex tilapia (Oreochromis spp) from a contaminated river in Taiwan: a case study. Toxins 2009, 1:14-24.
Szarek J., Siwicki A., Andrzejewska A., Terech-Majewska E., Banaszkiewickz T. Effects of the herbicide roundup on the ultrastructural pattern of hepatocytes in carp (Cyprinus carpio). Mar Environ Res 2000, 50:263-266.
Tellez-Banuelos M.C., Casa-Solis J., Bravo-Cuellar A., Zaitseva G. Oxidative stress in macrophages from spleen of Nile tilapia (Oreochromis niloticus) exposed to sub-lethal concentration of endosulfan. Fish Shellfish Immunol 2009, 27:105-111.
Tripathi G., Shasmal J. Concentration related responses of chlorpyriphos in antioxidant, anaerobic and protein synthesizing machinery of the freshwater fish Heteropneustes fossilis. Pest Biochem Physiol 2011, 99:215-220.
Van den Belt K., Wester P., van der Ven L.T.M., Verheyen R., Witters H. Time-dependent effects of ethynylestradiol on the reproductive physiology in zebrafish (Danio rerio). Environ Toxicol Chem 2002, 21:767-775.
Van Dyk J.C., Pieterse G.M. A histo-morphological study of the testis of the sharptooth catfish (Clarias gariepinus) as reference for future toxicological assessments. J Appl Ichthyol 2008, 24:415-422.
Van Dyk J.C., Marchand M.J., Smit N.J., Pieterse G.M. A histology-based fish health assessment of four commercially and ecologically important species from the Okavango Delta panhandle, Botswana. Afr J Aquat Sci 2009, 34:273-282.
Van Dyk J.C., Marchand M.J., Pieterse G.M., Barnhoon I.E.J., Bornman M.S. Histological changes in gills of Clarias gariepinus (Teleosti: Clariidae) from a polluted South African urban aquatic system. Afr J Aquat Sci 2009, 34:283-291.
Van Dyk J.C., Cochrane M.J., Wagenaar G.M. Liver histopathology of the sharptooth catfish Clarias gariepinus as a biomarker of aquatic pollution. Chemosphere 2012, 87:301-311.
Vander 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.
Vasanthi A., Revathi P., Mini J., Munuswamy N. Integrated use of histological and ultrastructural biomarkers in Mugil cephalus for heavy metal pollution in Ennore estuary, Chennai. Chemosphere 2013, 91:1156-1164.
Vigliano F.A., Bermúdez R., Quiroga M.I., Nieto J.M. Evidence for melano-macrophage centers of teleost as evolutionary precursors of germinal centers of higher vertebrates: an immuno-histochemical study. Fish Shellfish Immunol 2006, 21:467-471.
Villaverde J., Hildebrandt A., Martinez E., Lacorte S., Morillo E., Maqueda C., et al. Priority pesticides and their degradation products in river sediments from Portugal. Sci Total Environ 2008, 390:507-513.
Wester P.W. Histopathological effects of environmental pollutants HCH and methyl mercury on reproductive organs in freshwater fish. Comp Biochem Physiol 1991, 100:237-239.
Wolkea R.E. Piscine macrophage aggregates: a review. Annu Rev Fish Dis 1992, 2:91-108.
WWF (World Wildlife Fund for nature) Perturbateurs endocriniens et biodiversité. Rapport France 2011, [24 pp.].
Yèhouénou Azéhoun Pazou E. Les résidus de pesticides chimiques de synthèse dans les eaux, les sédiments et les espèces aquatiques du bassin versant du fleuve Ouémé et du lac Nokoué. Thèse de doctorat unique de l'université d'Abomey-Calavi (Bénin) 2005, [167 pp.].
Yèhouénou Azéhoun Pazou E., Lalèyè P., Boko M. Contamination of fish by organochlorine pesticide residues in the Ouémé River catchment in the Republic of Bénin. Environ Int 2006, 32:594-599.
Zimmerli S., Bernet D., Burkhardt-Holm P., Schmidt-Posthaus H., Vonlanthen T.W., Segner H. Assessment of fish health status in four Swiss rivers showing a decline of brown trout catches. Aquat Sci 2007, 69:11-25.
