Skip to main content
Log in

The effects of environmentally relevant concentrations of aldrin and methoxychlor on the testes and sperm of male Clarias gariepinus (Burchell, 1822) after short-term exposure

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

The organochlorine pesticides aldrin (0.14 μg/L) and methoxychlor (0.23 μg/L) were both present in the Albasini Dam, Limpopo Province, South Africa, during a field survey in 2014. The use of aldrin has been banned in the USA since 1987 and restricted in South Africa since 1992. The use of methoxychlor, however, remains undefined with little information available about its registration in South Africa despite being banned in Europe (2002) and USA (2003). The aim of this study was to determine the potential effects of environmentally relevant concentrations of aldrin and methoxychlor on the reproductive system of male catfish, Clarias gariepinus. Males were exposed for 96 h to the two pesticides under controlled laboratory conditions. Following exposure, each fish was weighed and measured, and a necropsy performed to determine any macroscopic abnormalities and the general health of the fish. The fish were killed and dissected and the testes removed, weighed and measured to determine the gonadosomatic index (GSI). The right testis of each fish was sectioned for histopathological assessment and to calculate the testes index (IT). The left testis was used for computer-assisted sperm analysis (CASA). The histopathological assessment of the testes showed histopathological changes such as of melano-macrophage centres (MMCs) and vacuolation of spermatogonia and spermatocytes. However, the classification of these changes indicated that the testes tissue structure was normal with slight histological changes. No statistically significant differences (p > 0.05) were found in the CASA parameters between exposure groups. The results of this study showed that the environmentally relevant concentrations of aldrin and methoxychlor did not have a negative effect on the motility of the mature sperm, but adverse effects were noted in the early stages of spermatogenesis, indicating possible effects over longer exposure periods.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Acosta IB, Varela AS Jr, Silva EF, Cardoso TF, Caldas JS, Jardima RD, Corcini CD (2016) Effects of exposure to cadmium in sperm cells of zebrafish, Danio rerio. Toxicol Rep 3:696–700. https://doi.org/10.1016/j.toxrep.2016.08.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Adams SM, Brown AM, Goede RW (1993) A quantitative health assessment index for rapid evaluation of fish condition in the field. Trans Am Fish Soc 12:63–73

    Article  Google Scholar 

  • Alavi SMH, Cosson J (2005) Sperm motility in fishes. (I). Effects of temperature and pH: a review. Cell Biol Int 29(2):101–110. https://doi.org/10.1016/j.cellbi.2004.11.021

    Article  PubMed  Google Scholar 

  • Alavi SMH, Cosson J (2006) Sperm motility in fishes. (II) effects of ions and osmolality: a review. Cell Biol Int 30(1):1–14. https://doi.org/10.1016/j.cellbi.2005.06.004

    Article  CAS  PubMed  Google Scholar 

  • Aly HAA, Azhar AS (2013) Methoxychlor induced biochemical alterations and disruptions of spermatogenesis in adult rats. Reprod Toxicol 40:8–15. https://doi.org/10.1016/j.reprotox.2013.05.002

    Article  CAS  PubMed  Google Scholar 

  • ATSDR (Agency for Toxic Substances and Disease Registry) (2002a) Toxicological profile for methoxychlor—U.S. Department of Health and Human Services. Accessed 20 Jan 2015. https://www.atsdr.cdc.gov/toxprofiles/tp47.pdf

  • ATSDR (Agency for Toxic Substances and Disease Registry) (2002b) Toxicological profile for aldrin/dieldrin—U.S. Department of Health and Human Services. Accessed 20 Jan 2015. https://www.atsdr.cdc.gov/toxprofiles/tp47.pdf

  • Bernet D, Schmidt H, Meier W, Burkhardt-Holm P, Wahli T (1999) Histopathology in fish: proposal for a protocol to assess aquatic pollution. J Fish Dis 22(1):25–34. https://doi.org/10.1046/j.1365-2761.1999.00134.x

    Article  Google Scholar 

  • Blazer VS (2002) Histopathological assessment of gonadal tissue in wild fishes. Fish Physiol Biochem 26(1):85–101. https://doi.org/10.1023/A:1023332216713

    Article  CAS  Google Scholar 

  • Bornman MS, Aneck-Hahn NH, de Jager C, Wagenaar GM, Bouwman H, Barnhoorn IEJ, Patrick SM, Vandenberg LN, Kortenkamp A, Blumberg B, Kimmins S, Jegou B, Auger J, DiGangi J, Heindel JJ (2017) Endocrine disruptors and health effects in Africa: a call for action. Environ Health Perspect 125(8):085005. https://doi.org/10.1289/EHP1774

    Article  PubMed  PubMed Central  Google Scholar 

  • Boryshpolets S, Kowalski RK, Dietrich GJ, Dzyuba B, Ciereszko A (2013) Different computer-assisted sperm analysis (CASA) systems highly influence sperm motility parameters. Theriogenology 80(7):758–765. https://doi.org/10.1016/j.theriogenology.2013.06.019

    Article  CAS  PubMed  Google Scholar 

  • Bray JJ, Cragg PA, Macknight ADC, Mills RG (1999) Lecture notes on human physiology, 4th edn. Blackwell Scientific Publications, Oxford

    Google Scholar 

  • Bruslé J, Gonzàlez G (1996) The structure and function of fish liver. In: Muneshi JSD, Dutta HM (eds) Fish morphology. Science Publisher Inc, New York, p 77–93

    Google Scholar 

  • Carlander KD (ed) (1969) Handbook of freshwater fishery biology. Lowa State University Press, Lowa

    Google Scholar 

  • Casteel SW, Satalowhich FT, Kendall JD, Rottinghaus GE, Gosser HS, Schneider NR (1993) Aldrin intoxication and clearance of associated dieldrin residues in a group of feedlot cattle. J Am Vet Med Assoc 202:83–85

    CAS  PubMed  Google Scholar 

  • Cummings AM (1997) Methoxychlor as a model for environmental estrogens. Crit Rev Toxicol 27:367–379

    Article  CAS  Google Scholar 

  • DWAF (Department of Water Affairs and Forestry) (1996) South African water quality guidelines (first edition). Volume 8: field guide

  • Fabbrocini A, D’Adamo R, Pelosi S, Oliveira LFJ, Del Prete F, Silvestri F, Vitiello V, Sansone G (2015) Sperm motility evaluation following long-term storage (5 years) of cryopreserved sea bream (Sparus aurata) semen. J Appl Ichthyol 31:104–107. https://doi.org/10.1111/jai.12726

    Article  CAS  Google Scholar 

  • Fort DJ, Thomas JH, Rogers RL, Noll A, Spaulding CD, Guiney PD, Weeks JA (2004) Evaluation of the development and reproductive toxicity of methoxychlor using an anuran (Xenopus tropicalis) chronic exposure model. Toxicol Sci 81:1–35

    Article  Google Scholar 

  • Hodge HC, Maynard EA, Thomas JF, Blanchet HJ, Wilt WG, Mason KE (1950) Short-term oral toxicity tests of methoxychlor (2,2 di-(p-methoxy phenyl)-1,1,1-trichlorethane) in rats and dogs. J Pharmacol Exp Ther 99(1):140–148

    CAS  PubMed  Google Scholar 

  • Honeycott M, Shirley S (2014) Aldrin. Enc Toxicol 1:126–129

    Article  Google Scholar 

  • International Programme on Chemical Safety (IPCS) (2002) Global assessment of the state of the science of endocrine disruptors. In: Damstra T, Barlow S, Bergman A, KavlockR, van der Kraak G. (eds) World Health Organization WHO/PCS/EDC/02.2

  • Jooste A, Marr S, Addo-Bediako A, Luus-Powell WJ (2015) Sharptooth catfish shows its metal: a case study of metal contamination at two impoundments in the Olifants River, Limpopo river system, South Africa. Ecotoxicol Environ Safe 112:96–104. https://doi.org/10.1016/j.ecoenv.2014.10.033

    Article  CAS  Google Scholar 

  • Jorgenson JL (2001) Aldrin and dieldrin: a review of research on their production, environmental deposition and fate, bioaccumulation, toxicology, and epidemiology in the United States. Environ Health Perspect 109:113–139

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kabir ER, Rahman MS, Rahman I (2015) A review on endocrine disruptors and their possible impacts on human health. Environ Toxicol Pharm 40:241–258

    Article  CAS  Google Scholar 

  • Kavlock RJ, Daston GP, DeRosa C, Fenner-Crisp P, Gray LE, Kaattari S, Lucier G, Luster M, Mac MJ, Maczka C, Miller R, Moore J, Rolland R, Scott G, Sheehan DM, Sinks T, Tilson HA (1996) Research needs for the risk assessment of health and environmental effects of endocrine disruptors: A report of the U.S EPA-sponsored workshop. Environ Health Perspect 104(4):715–740

    PubMed  PubMed Central  Google Scholar 

  • Kime DE, Ebrahimi M, Nysten K, Roelants KI, Rurangwa E, Moore HDM, Ollevier F (1996) Use of computer assisted sperm analysis (CASA) for monitoring the effects of pollution on sperm quality of fish; application to the effects of heavy metals. Aquat Toxicol 36(3-4):223–237. https://doi.org/10.1016/S0166-445X(96)00806-5

    Article  CAS  Google Scholar 

  • Kime DE, Van Look KJW, McAllister BG, Huyskens G, Rurangwa E, Ollevier F (2001) Computer-assisted sperm analysis (CASA) as a tool for monitoring sperm quality in fish. Comp Biochem Phys C 130:425–433

    CAS  Google Scholar 

  • Marchand MJ, Pieterse GM, Barnhoorn IEJ (2008) Preliminary results on sperm motility and testicular histology of two feral fish species, Oreochromis mossambicus and Clarias gariepinus, from a currently DDT-sprayed area, South Africa. J Appl Ichthyol 24(4):423–429. https://doi.org/10.1111/j.1439-0426.2008.01141.x

    Article  Google Scholar 

  • Marchand MJ, Pieterse GM, Barnhoorn IEJ (2010) Sperm motility and testicular histology as reproductive indicators of fish health of two feral fish species from a currently DDT sprayed area, South Africa. J Appl Ichthyol 26(5):707–714. https://doi.org/10.1111/j.1439-0426.2010.01558.x

    Article  CAS  Google Scholar 

  • Manikkam M, Haque MM, Guerrero-Bosagne C, Nilsson EE, Skinner MK (2014) Pesticide methoxychlor promotes the epigenetic transgenerational inheritance of adult-onset disease through the female germline. PLoS One 9(7):1–19

    Article  Google Scholar 

  • Morely NJ, Costa HH, Lewis JW (2010) Effects of a chemically polluted discharge on the relationship between fecundity and parasitic infections in the chub (Leuciscus cephalus) from a river in the southern England. Arch Environ Contam Toxicol 58:783–792

    Article  Google Scholar 

  • NDA (National Development Agency) (2017) Banned and restricted substances in the Republic of South Africa. Accessed July 2017. http://www.nda.agric.za

  • Nibamureke UMC, Barnhoorn IEJ, Wagenaar GM (2016) Health assessment of freshwater fish species from Albasini Dam, outside a DDT-sprayed area in Limpopo province, South Africa: a preliminary study. Afr J Aquat Sci 41:1–12

    Article  Google Scholar 

  • Oropesa AL, Martín-Hidalgo D, Fallola C, Gil MC (2015) Effects of exposure to 17-alpha-ethynylestradiol on sperm quality of tench (Tinca tinca). Ecotoxicol Environ Saf 120:318–325. https://doi.org/10.1016/j.ecoenv.2015.06.016

    Article  CAS  PubMed  Google Scholar 

  • Pacheco M, Santos MA (2002) Biotransformation, genotoxic, and histopathological effects of environmental contaminants in European eel (Anguilla anguilla L.). Ecotoxicol Environ Saf 53:331–347

    Article  CAS  Google Scholar 

  • Papoulias DM, Villalobos SA, Meadows J, Noltie DB, Giesy JP, Tillitt DE (2003) In ovo exposure to o,p_-DDE affects sexual development but not sexual differentiation in Japanese medaka (Oryzias latipes). Environ Health Persp 111:29–32

    Article  CAS  Google Scholar 

  • Pieterse GM, Marchand MJ, van Dyk JC, Barnhoorn IEJ (2010) Histological alterations in the testes and ovaries of the sharptooth catfish (Clarias gariepinus) from an urban nature reserve in South Africa. J App Ichthy 26(5):789–793. https://doi.org/10.1111/j.1439-0426.2010.01557.x

    Article  Google Scholar 

  • Rurangwa E, Biegniewska A, Slominska E, Skorkowski EF, Ollevier F (2002) Effect of tributyltin on adenylate content and enzyme activities of teleost sperm: a biochemical approach to study the mechanisms of toxicant reduced spermatozoa motility. Comp Biochem Physiol 131(3):335–344

    CAS  Google Scholar 

  • Rurangwa E, Kime DE, Ollevier F, Nash JP (2004) The measurement of sperm motility and factors affecting sperm quality in cultured fish. Aquaculture 234(1-4):1–28. https://doi.org/10.1016/j.aquaculture.2003.12.006

    Article  Google Scholar 

  • Schmitt CJ, Dethloff GM (eds) (2000) Biomonitoring of environmental status and trends (BEST) program: selected methods for monitoring chemical contaminants and their effects in aquatic ecosystems. U.S. Geological Survey, Biological Resources Division. Information and Technology Report USGS/BRD-2000-0005, Columbia

  • Schulz RW, de França LR, Lareyre J-J, LeGac F, Chiarini-Garcia H, Nobrega RH, Miura T (2010) Spermatogenesis in fish. Gen Comp Endocrinol 165:390–411

    Article  CAS  Google Scholar 

  • Singh PB, Sahu V, Singh V, Nigam SK, Singh HK (2008) Sperm motility in the fishes of pesticide exposed and from polluted rivers of Gomti and Ganga of north India. Food Chem Toxicol 46(12):3764–3769. https://doi.org/10.1016/j.fct.2008.09.066

    Article  CAS  PubMed  Google Scholar 

  • Skelton P (2001) A complete guide to the freshwater fishes of South Africa. Struik Publishers, Cape Town

    Google Scholar 

  • Stern AH (2014) Hazard identification of the potential for dieldrin carcinogenicity to humans. Environ Res 131:188–214

    Article  CAS  Google Scholar 

  • Stockholm Convention (2008) Listing of POPs in the Stockholm Convention. Accessed 16 Feb 2016. http://chm.pops.int/TheConvention/ThePOPs/The12InitialPOPs/tabid/296/Default.aspx

  • Tomar LR, Agarwal MP, Avasthi R, Tyagi V, Mustafa M, Banerjee BD (2013) Serum organochlorine pesticide levels in patients with metabolic syndrome. Indian J Endorinol Metab 17(1):342–344

    Article  Google Scholar 

  • Toppari J, Larsen J, Christiansen P, Giwercman A, Grandjean P, Guillette LJ Jr, Jegou B, Jensen TK, Jouannet P, Keiding N, Leffers H, McLachlan JA, Meyer O, Miiller J, Rajpert-De Meyts E, Scheike T, Sharpe R, Sumpter J, Skakkebaek NE (1996) Male reproductive health and environmental xenoestrogens. Environ Health Perspect 104(4):741–803. https://doi.org/10.1289/ehp.96104s4741

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van Dyk JC (2006) A qualitative and quantitative assessment of the normal histology of selected target organs of Clarias gariepinus and Oreochromis mossambicus. PhD Thesis. University of Johannesburg

  • van Dyk JC, Pieterse GM (2008) A histo-morphological study of the testis of the sharptooth catfish (Clarias gariepinus) as reference for future toxicological assessments. J Appl Ichthyol 24:415–422

    Article  Google Scholar 

  • van Dyk JC, Marchand MJ, Smit NJ, Pieterse GM (2009) A histology-based fish health assessment of four commercially and ecologically important species from the Okavango Delta panhandle, Botswana. Afr J Aquat Sci 34(3):273–282

    Article  Google Scholar 

  • Wagenaar G, Botha T, Barnhoorn I (2012) Sperm motility and testicular histology as reproductive indicators in Clarias gariepinus from an eutrophic impoundment, South Africa. J Appl Ichthyol 28(6):990–997. https://doi.org/10.1111/jai.12065

    Article  Google Scholar 

  • Wrobel MH, Grzeszczyk M, Mlynarczuk J, Kotwica J (2015) The adverse effects of aldrin and dieldrin on both myometrial contractions and the secretory functions of bovine ovaries and uterus in vitro. Toxicol Appl Pharm 285(1):23–31. https://doi.org/10.1016/j.taap.2015.03.005

    Article  CAS  Google Scholar 

  • Zimmerli S, Bernet D, Burkhardt-Holm P, Schmidt-Posthaus H, Vonlanthen TW, Segner H (2007) Assessment of fish health status in four Swiss rivers showing a decline of brown trout catches. Aquat Sci 69(1):11–25. https://doi.org/10.1007/s00027-006-0844-3

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors would like to thank the following institutions for the financial and logistic support: National Research Foundation of South Africa (Incentive Funding for Rated Researchers, UIDs:86056), Scarce Skills Bursary funds, grant no. 89871, Department of Germplasm, Conservation and Reproduction Biotechnologies - Agricultural Research Council, Irene for assistance with the sperm analysis and Ms. J van Staden from STATKON at the University of Johannesburg for her assistance with the statistical analysis of the data.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to G. M. Wagenaar.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Das Neves, J., Barnhoorn, I.E.J. & Wagenaar, G.M. The effects of environmentally relevant concentrations of aldrin and methoxychlor on the testes and sperm of male Clarias gariepinus (Burchell, 1822) after short-term exposure. Fish Physiol Biochem 44, 1421–1434 (2018). https://doi.org/10.1007/s10695-018-0474-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-018-0474-4

Keywords

Navigation