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Environmental Science and Pollution Research

, Volume 26, Issue 18, pp 18533–18540 | Cite as

Reprotoxicity of 4-nonylphenol to Biomphalaria alexandrina snails at certain temperatures

  • Marwa T. A. Abdel–WarethEmail author
  • Sara S. M. Sayed
Research Article
  • 44 Downloads

Abstract

One of the most common compounds in pesticide formulations, plastics, and papers is 4-nonylphenol (4-NP). It is contained in agricultural, industrial, and wastewater effluents, which when discharged into surface waters affect aquatic fauna. Therefore, the present study aimed to use Biomphalaria alexandrina snails to evaluate the chronic toxicity of 4-NP. Its concentrations in collected water samples from Giza Governorate ranged from 400 to 1600 μg/l. Based on these environmentally relevant concentrations, laboratory experiments were carried out using standard 4-NP to investigate the effect of three concentrations; namely 400, 750, and 1600 μg/l. Survival rate of the exposed snails to 4-NP concentrations was affected after 4 weeks. Reproduction of the exposed snails to 4-NP concentrations was lower than that of the control at 30 °C, while the exposed snails to 400 μg/l of 4-NP showed maximum reproduction at 15 °C. The lowest hatchability percentage was recorded with egg masses laid by the exposed snails to 400 and 1600 μg/l of 4-NP at 15 and 30 °C, respectively. Furthermore, the results showed fluctuated levels of progesterone, estradiol, and testosterone depending upon the concentration and the temperature, which played a key role in determining the degree of 4-NP toxicity.

Keywords

Estradiol 4-Nonylphenol Progesterone Snails Temperature Testosterone 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Adenusi AA, Odaibo A (2009) Effects of varying concentrations of the crude aqueous and ethanolic extracts of Dalbergia sissoo plant parts on Biomphalaria pfeifferi egg masses. Afr J Tradit Complement Altern Med 6:139–149Google Scholar
  2. Alon G, Shore LS, Steinberger Y (2007) Correlation between levels of sex hormones (progesterone, testosterone, and estrogen) and ecophysiological-behavior stages in two species of desert snails (Sphincterochila zonata and Sphincterochila prophetarum) in the Northern Negev Desert. Gen Comp Endocrinol 151:122–127CrossRefGoogle Scholar
  3. Barbosa ND, Pimentel-Souza F, Sampaio IB (1987) The effect of seasonal temperature and experimental illumination on reproductive rate in the snail Biomphalaria glabrata. Braz J Med Biol Res 20:685–696Google Scholar
  4. Benachour N, Moslemi S, Sipahutar H, Seralini GE (2007) Cytotoxic effects and aromatase inhibition by xenobiotic endocrine disrupters alone and in combination. Toxicol Appl Pharmacol 222:129–140CrossRefGoogle Scholar
  5. Bennie DT (1999) Review of the environmental occurrence of alkylphenols and alkylphenol ethoxylates. Water Qual Res J 34:79–122CrossRefGoogle Scholar
  6. Brooke LT (1993) Acute and chronic toxicity of nonylphenol to ten species of aquatic organisms. Report to the WS. Environmental Protection Agency, Duluth, MN (contract no. 68-C1–0034). Lake Superior Research Institute, University of Wisconsin-Superior, Superior, WiscGoogle Scholar
  7. Brooke LT, Thursby G (2005) Aquatic life ambient water quality criteria—nonylphenol. US Environmental Protection Agency (EPA), Office of Water Office of Science and Technology, Washington DC, 88Google Scholar
  8. Cochón AC, Della Penna AB, Kristoff G, Piol MN, De Viale LSM, Guerrero NV (2007) Differential effects of paraquat on oxidative stress parameters and polyamine levels in two freshwater invertebrates. Ecotoxicol Environ Saf 68:286–292CrossRefGoogle Scholar
  9. Coutellec MA, Lagadic L (2006) Effects of self-fertilization, environmental stress and exposure to xenobiotics on fitness-related traits of the freshwater snail Lymnaea stagnalis. Ecotoxicol 15:199–213CrossRefGoogle Scholar
  10. Czech P, Weber K, Dietrich DR (2001) Effects of endocrine modulating substances on reproduction in the hermaphroditic snail Lymnaea stagnalis L. Aquat Toxicol 53:103–114CrossRefGoogle Scholar
  11. de Freitas Tallarico L, Borrely SI, Hamada N, Grazeffe VS, Ohlweiler FP, Okazaki K, Granatelli AT, Pereira IW, de Bragança Pereira CA, Nakano E (2014) Developmental toxicity, acute toxicity and mutagenicity testing in freshwater snails Biomphalaria glabrata (Mollusca: Gastropoda) exposed to chromium and water samples. Ecotoxicol Environ Saf 110:208–215CrossRefGoogle Scholar
  12. Ducrot V, Askem C, Azam D, Brettschneider D, Brown R, Charles S, Coke M, Collinet M, Delignette-Muller ML, Forfait-Dubuc C, Holbech H (2014) Development and validation of an OECD reproductive toxicity test guideline with the pond snail Lymnaea stagnalis (Mollusca, Gastropoda). Regul Toxicol Pharmacol 70:605–614CrossRefGoogle Scholar
  13. Duft M, Schulte-Oehlmann U, Weltje L, Tillmann M, Oehlmann J (2003) Stimulated embryo production as a parameter of estrogenic exposure via sediments in the freshwater mudsnail Potamopyrgus antipodarum. Aquat Toxicol 64:437–449CrossRefGoogle Scholar
  14. EPA US (2005) Aquatic life ambient water quality criteria—nonylphenol. EPA-822-R-05Google Scholar
  15. EU European Union Risk Assessment Report (2002) 4-Nonylphenol (branched) and nonylphenol. 2nd priority list volume: 10Assessment ER. 4-Nonylphenol (branched) and Nonylphenol.”European Commission. Institute for Health and Consumer Protection, European Chemicals BureauGoogle Scholar
  16. Giusti A, Ducrot V, Joaquim-Justo C, Lagadic L (2013) Testosterone levels and fecundity in the hermaphroditic aquatic snail Lymnaea stagnalis exposed to testosterone and endocrine disruptors. Environ Toxicol Chem 32:1740–1745CrossRefGoogle Scholar
  17. Goupy P, Hugues M, Boivin P, Amiot MJ (1999) Antioxidant composition and activity of barley (Hordeum vulgare) and malt extracts and of isolated phenolic compounds. J Sci Food Agric 79:1625–1634CrossRefGoogle Scholar
  18. Hammond B, Katzenellenbogen BS, Krauthammer N, McConnell J (1979) Estrogenic activity of the insecticide chlordecone (Kepone) and interaction with uterine estrogen receptors. Proc Nat Acad Sci 76:6641–6645CrossRefGoogle Scholar
  19. Haszprunar G, Wanninger A (2012) Molluscs. Curr Biol 22:510–514CrossRefGoogle Scholar
  20. Hathaway JJ, Adema CM, Stout BA, Mobarak CD, Loker ES (2010) Identification of protein components of egg masses indicates parental investment in immunoprotection of offspring by Biomphalaria glabrata (Gastropoda, Mollusca). Dev Comp Immunol 34:425–435CrossRefGoogle Scholar
  21. Heugens EH, Hendriks AJ, Dekker T, Straalen NMV, Admiraal W (2001) A review of the effects of multiple stressors on aquatic organisms and analysis of uncertainty factors for use in risk assessment. Crit Rev Toxicol 31:247–284CrossRefGoogle Scholar
  22. Holmstrup M, Bindesbøl AM, Oostingh GJ, Duschl A, Scheil V, Köhler HR, Loureiro S, Soares AM, Ferreira AL, Kienle C, Gerhardt A (2010) Interactions between effects of environmental chemicals and natural stressors: a review. Sci Total Environ 408:3746–3762CrossRefGoogle Scholar
  23. Hooper MJ, Ankley GT, Cristol DA, Maryoung LA, Noyes PD, Pinkerton KE (2013) Interactions between chemical and climate stressors: a role for mechanistic toxicology in assessing climate change risks. Environ Toxicol Chem 32:32–48CrossRefGoogle Scholar
  24. Jessica D, Robert M, Frédéric S, Arnaud B, Delphine L, Jean-Pierre T, Patrick K (2007) Do sewage treatment plant discharges substantially impair fish reproduction in polluted rivers. Sci Total Environ 372:497–514CrossRefGoogle Scholar
  25. Jobling S, Sumpter JP, Sheahan D, Osborne JA, Matthiessen P (1996) Inhibition of testicular growth in rainbow trout (Oncorhynchus mykiss) exposed to estrogenic alkylphenolic chemicals. Environ Toxicol Chem 15:194–202CrossRefGoogle Scholar
  26. Kimberly DA, Salice CJ (2014a) Complex interactions between climate change and toxicants: evidence that temperature variability increases sensitivity to cadmium. Ecotoxicol 23:809–817CrossRefGoogle Scholar
  27. Kimberly DA, Salice CJ (2014b) If you could turn back time: understanding transgenerational latent effects of developmental exposure to contaminants. Environ Pollut 184:419–425CrossRefGoogle Scholar
  28. Kristoff G, Guerrero NRV, Cochón AC (2010) Inhibition of cholinesterases and carboxylesterases of two invertebrate species, Biomphalaria glabrata and Lumbriculus variegatus, by the carbamate pesticide carbaryl. Aquat Toxicol 96:115–123CrossRefGoogle Scholar
  29. Kubiriza GK, Madsen H, Likongwe JS, Stauffer JR, Kang'Ombe J, Kapute F (2010) Effect of temperature on growth, survival and reproduction of Bulinus nyassanus (Smith, 1877) (Mollusca: Gastropoda) from Lake Malawi. Afr Zool 45:315–320Google Scholar
  30. Lahlou M (2004) Study of the molluscicidal activity of some phenolic compounds: structure-activity relationship. Pharm Biol 42:258–261CrossRefGoogle Scholar
  31. Madigou T, Le Goff P, Salbert G, Cravedi JP, Segner H, Pakdel F, Valotaire Y (2001) Effects of nonylphenol on estrogen receptor conformation, transcriptional activity and sexual reversion in rainbow trout (Oncorhynchus mykiss). Aquat Toxicol 53:173–186CrossRefGoogle Scholar
  32. Marie MA, El-Deeb FA, Hasheesh WS, Mohamed RA, Sayed SSM (2015) Impact of seasonal water quality and trophic levels on the distribution of various freshwater snails in four Egyptian governorates. Appl Ecol Environ Sci 3:117–126Google Scholar
  33. McCreesh N, Arinaitwe M, Arineitwe W, Tukahebwa EM, Booth M (2014) Effect of water temperature and population density on the population dynamics of Schistosoma mansoni intermediate host snails. Parasit Vectors 7:503CrossRefGoogle Scholar
  34. McLachlan JA (1993) Functional toxicology: a new approach to detect biologically active xenobiotics. Environ Health Perspect 101:386–387CrossRefGoogle Scholar
  35. Metcalfe CD, Hoover L, Sang S (1996) Nonylphenol ethoxylates and their use in Canada. Report to the World Wildlife Fund Canada, pp 1–33Google Scholar
  36. Naokuni T (1979) Induction of egg-laying by steroid hormones in slugs. Comp Biochem Physiol A Physiol 62:273–278CrossRefGoogle Scholar
  37. Nduku WK, Harrison AD (1980) Cationic responses of organs and haemolymph of Biomphalaria pfeifferi (Krauss), Biomphalaria glabrata (Say) and Helisoma trivolvis (Say) (Gastropoda: Planorbirdae) to cationic alterations of the medium. Hydrobiol 68:119–138CrossRefGoogle Scholar
  38. OECD (Organization for Economic Cooperation and Development) (2010) Detailed review paper (DRP) on molluscs life-cycle toxicity testing. OECD 830 series on testing and assessment no. 121, OECD, Paris, FranceGoogle Scholar
  39. Oketola AA, Fagbemigun TK (2013) Determination of nonylphenol, octylphenol and bisphenol-A in water and sediments of two major rivers in Lagos, Nigeria. J Environ Prot 4:38–45CrossRefGoogle Scholar
  40. Oliveira-Filho EC, Grisolia CK, Paumgartten FJR (2009) Trans-generation study of the effects of nonylphenol ethoxylate on the reproduction of the snail Biomphalaria tenagophila. Ecotoxicol Environ Saf 72:458–465CrossRefGoogle Scholar
  41. Olivier L, Haskins WT (1960) The effects of low concentrations of sodium pentachlorophenate on the fecundity and egg viability of Australorbis glabratus. Am J Trop Med Hyg 9:199–205CrossRefGoogle Scholar
  42. Rizk MZ, Metwally NS, Hamed MA, Mohamed AM (2012) Correlation between steroid sex hormones, egg laying capacity and cercarial shedding in Biomphalariaalexandrina snails after treatment with Haplophyllum tuberculatum. Exp Parasitol 132:171–179CrossRefGoogle Scholar
  43. Santos MM, Castro LF, Vieira MN, Micael J, Morabito R, Massanisso P, Reis-Henriques MA (2005) New insights into the mechanism of imposex induction in the dogwhelk Nucella lapillus. Comp Biochem Physiol Part C: Toxicol Pharmacol 141:101–109Google Scholar
  44. Seppälä O, Jokela J (2011) Immune defence under extreme ambient temperature. Biol Lett 7:119–122CrossRefGoogle Scholar
  45. Servos MR (1999) Review of the aquatic toxicity, estrogenic responses and bioaccumulation of alkylphenols and alkylphenol polyethoxylates. Water Qual Res J 34:123–178CrossRefGoogle Scholar
  46. Sharpe RM, Fisher JS, Millar MM, Jobling S, Sumpter JP (1995) Gestational and lactational exposure of rats to xenoestrogens results in reduced testicular size and sperm production. Environ Health Perspect 103:1136–1143CrossRefGoogle Scholar
  47. Simpson ER, Mahendroo MS, Means GD, Kilgore MW Hinshelwood MM, Graham-Lorence S, Amarneh B, Ito T, Fisher CR, Michael MD, Mendelson CR (1994) Aromatase cytochrome P450, the enzyme responsible for estrogen biosynthesis. End Rev 15:342–355Google Scholar
  48. Sternberg RM, Hotchkiss AK, LeBlanc GA (2008) The contribution of steroidal androgens and estrogens to reproductive maturation of the eastern mud snail Ilyanassa obsoleta. Gen Comp Endocrinol 156:15–26CrossRefGoogle Scholar
  49. Takeda N (1977) Stimulation of egg-laying by nerve extracts in slugs. Nature 267(5611):513–514CrossRefGoogle Scholar
  50. Watanabe H, Suzuki A, Goto M, Lubahn DB, Handa H, Iguchi T (2004) Tissue-specific estrogenic and non-estrogenic effects of a xenoestrogen, nonylphenol. J Mol Endocrinol 33:243–252CrossRefGoogle Scholar
  51. White R, Jobling S, Hoare SA, Sumpter JP, Parker MG (1994) Environmentally persistent alkylphenolic compounds are estrogenic. Endocrinol 135:175–182CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Marwa T. A. Abdel–Wareth
    • 1
    Email author
  • Sara S. M. Sayed
    • 1
  1. 1.Environmental Research and Medical Malacology DepartmentTheodor Bilharz Research InstituteGizaEgypt

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