, Volume 25, Issue 1, pp 192–200 | Cite as

Impact of three phthalate esters on the sexual reproduction of the Monogonont rotifer, Brachionus calyciflorus

  • V. Cruciani
  • C. Iovine
  • J.-P. Thomé
  • C. Joaquim-Justo


Phthalate esters are widespread contaminants that can cause endocrine disruption in vertebrates. Studies showed that molecules with hormonal activities in vertebrates and invertebrates can affect asexual and sexual reproduction in rotifers. We investigated the impact of di-hexylethyl phthalate (DEHP), di-butyl phthalate (DBP) and butylbenzyl phthalate (BBP), on the asexual and sexual reproduction of the freshwater monogonont rotifer Brachionus calyciflorus in order to determine a potential environmental risk for sexual reproduction. We observed that DEHP has no significant impact on both asexual and sexual reproduction up to 2 mg/L. DBP has a positive effect on asexual reproduction at concentrations from 0.05 to 1 mg/L, but depresses it at 2 mg/L. Sexual reproduction is only affected at 2 mg/L and the impact observed is negative. BBP displayed a negative impact on both asexual and sexual reproduction at 1 and 2 mg/L. However we showed that the impacts of BBP on mixis and fertilization rates observed are due to the decrease in population growth rates at these concentrations and not to a direct impact of BBP on the mixis and the fertilization processes. Our results show that sexual reproduction in B. calyciflorus is not more sensitive than asexual reproduction to any of the substances tested which indicates the mode of action of these molecules is related to general toxicity and not to an interference with potential endocrine regulation of sexual reproduction. Comparison of effect concentrations and surface water contamination by phthalate esters suggests these compounds do not constitute a risk for primary consumers in these environments.


Endocrine disruptors Brachionus calyciflorus Rofifera Sexual reproduction 



The authors thank T.W.Snell for kindly providing the cysts. This research was supported by funds from Fond National de la Recherche Scientifique (F.R.S. - F.N.R.S.). We thank two anonymous reviewers for their constructive comments which helped to improve this manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Andersen RA (ed) (2005) Algal culturing techniques. Elsevier Academic Press, London, p 578Google Scholar
  2. Bischoff HW, Bold HC (1963) Phycological studies. IV. Some soil algae from enchanted rock and related algal species, vol 6318. University of Texas Publications, Austin, pp 1–95Google Scholar
  3. Calabrese EJ (2008) Hormesis: why it is important to toxicology and toxicologists. Environ Toxicol Chem 27(7):1451–1474CrossRefGoogle Scholar
  4. Cecchine G, Snell TW (1999) Toxicant exposure increases threshold food levels in freshwater rotifer populations. Environ Toxicol 14(5):523–530CrossRefGoogle Scholar
  5. Fang H, Tong WD, Branham WS, Moland CL, Dial SL, Hong HX, Xie Q, Perkins R, Owens W, Sheehan DM (2003) Study of 202 natural, synthetic, and environmental chemicals for binding to the androgen receptor. Chem Res Toxicol 16(10):1338–1358CrossRefGoogle Scholar
  6. Foster PMD (2005) Mode of action: impaired fetal leydig cell function—effects on male reproductive development produced by certain phthalate esters. Crit Rev Toxicol 35(8/9):713–719CrossRefGoogle Scholar
  7. Foster PMD, Mylchreest E, Gaido KW, Sar M (2001) Effects of phthalate esters on the developing reproductive tract of male rats. Hum Reprod Update 7(3):231–235CrossRefGoogle Scholar
  8. Fromme H, Kuchler T, Otto T, Pilz K, Muller J, Wenzel A (2002) Occurrence of phthalates and bisphenol A and F in the environment. Water Res 36(6):1429–1438CrossRefGoogle Scholar
  9. Gallardo WG, Hagiwara A, Tomita Y, Soyano K, Snell TW (1997) Effect of some vertebrate and invertebrate hormones on the population growth, mictic female production, and body size of the marine rotifer Brachionus plicatilis Muller. Hydrobiologia 358:113–120CrossRefGoogle Scholar
  10. Gilbert JJ (2003) Environmental and endogenous control of sexuality in a rotifer life cycle: developmental and population biology. Evolut Dev 5(1):19–24CrossRefGoogle Scholar
  11. Gray LE, Otsby J, Furr J, Wolf CJ, Lambright C, Parks L, Veeramachaneni DN, Wilson V, Price M, Hotchkiss A, Orlando E, Guillette L (2001) Effects of environmental antiandrogens on reproductive development in experimental animals. Hum Reprod Update 7:248–264CrossRefGoogle Scholar
  12. Harris CA, Henttu P, Parker MG, Sumpter JP (1997) The estrogenic activity of phthalate esters in vitro. Environ Health Perspect 105(8):802–811CrossRefGoogle Scholar
  13. Howdeshell KL, Furr J, Lambright CR, Rider CV, Wilson VS, Gray LE (2007) Cumulative effects of dibutyl phthalate and diethylhexyl phthalate on male rat reproductive tract development: altered fetal steroid hormones and genes. Toxicol Sci 99(1):190–202CrossRefGoogle Scholar
  14. Huang GL, Sun HW, Song ZH (1999) Interactions between dibutyl phthalate and aquatic organisms. Bull Environ Contam Toxicol 63(6):759–765CrossRefGoogle Scholar
  15. Huang L, Zha CW, Xi YL, Zhao LL (2007) Effect of aldrin on life history characteristics of rotifer Brachionus calyciflorus Pallas. Bull Environ Contam Toxicol 79(5):524–528CrossRefGoogle Scholar
  16. Kooijman SALM, Metz JAJ (1984) On the dynamics of chemically stressed populations: the deduction of population consequences from effects on individuals. Ecotoxicol Environ Saf 8(3):254–274CrossRefGoogle Scholar
  17. Martino-Andrade AJ, Chahoud I (2010) Reproductive toxicity of phthalate esters. Mol Nutr Food Res 54(1):148–157CrossRefGoogle Scholar
  18. Mylchreest E, Sar M, Cattley RC, Foster PMD (1999) Disruption of androgen-regulated male reproductive development by Di(n-butyl) phthalate during late gestation in rats is different from flutamide. Toxicol Appl Pharmacol 156(2):81–95CrossRefGoogle Scholar
  19. Nogrady T, Wallace RL, Snell TW (1993) Rotifera, vol. 1: biology, ecology and systematics. SPB Academic Publishing, The HagueGoogle Scholar
  20. Ooms-Wilms AL, Postema G, Gulati RD (2001) population dynamics of rotifers in Lake Loosdrecht, the Netherlands, in relation to their potential food and predators. Freshw Biol 44(1):77–97Google Scholar
  21. OSPAR Commission (2006) OSPAR background document on phthalates. Available at Accessed 10 Dec 2015
  22. Pakerton TF, Konkel WJ (2000) Application of quantitative structure activity relationships for assessing the aquatic toxicity of phthalate esters. Ecotoxicol Environ Saf 45:61–78CrossRefGoogle Scholar
  23. Planelló R, Herrero O, Martínez-Guitarte JL, Morcillo G (2011) Comparative effects of butyl benzyl phthalate (BBP) and di(2-ethylhexyl) phthalate (DEHP) on the aquatic larvae of Chironomus riparius based on gene expression assays related to the endocrine system, the stress response and ribosomes. Aquat Toxicol 105(1–2):62–70CrossRefGoogle Scholar
  24. Preston BL, Snell TW, Robertson TL, Dingmann BJ (2000) Use of freshwater rotifer Brachionus calyciflorus in screening assay for potential endocrine disruptors. Environ Toxicol Chem 19(12):2923–2928CrossRefGoogle Scholar
  25. Saillenfait AM, Laudet-Hesbert A (2005) Phtalates. EMC Toxicol Pathol 2(1):1–13CrossRefGoogle Scholar
  26. Serra M, Smith HA, Weitz JS, Snell TW (2011) Analysing threshold effects in the sexual dynamics of cyclically parthenogenetic rotifer populations. Hydrobiologia 662(1):121–130CrossRefGoogle Scholar
  27. Singh S, Li SS (2011) Phthalates: toxicogenomics and inferred human diseases. Genomics 97(3):148–157CrossRefGoogle Scholar
  28. Snell TW (2011) A review of the molecular mechanisms of rotifer reproduction. Hydrobiologia 662:89–97CrossRefGoogle Scholar
  29. Snell TW, Carmona MJ (1995) Comparative toxicant sensitivity of sexual and asexual reproduction in the rotifer Brachionus calyciflorus. Environ Toxicol Chem 14(3):415–420CrossRefGoogle Scholar
  30. Snell TW, DesRosiers NJD (2008) Effect of progesterone on sexual reproduction of Brachionus manjavacas (Rotifera). J Exp Mar Biol Ecol 363(1–2):104–109CrossRefGoogle Scholar
  31. Snell TW, Joaquim-Justo C (2007) Workshop on rotifers in ecotoxicology. Hydrobiologia 593:227–232CrossRefGoogle Scholar
  32. Snell TW, Moffat BD, Janssen C, Persoone G (1991) Acute toxicity tests using rotifers 4. Effects of cyst age, temperature, and salinity on the sensitivity of brachionus calyciflorus. Ecotoxicol Environ Saf 21(3):308–317CrossRefGoogle Scholar
  33. Snell TW, Kubanek J, Carter W, Payne AB, Kim J, Hicks MK, Stelzer CP (2006) A protein signal triggers sexual reproduction in Brachionus plicatilis (Rotifera). Mar Biol 149(4):763–773CrossRefGoogle Scholar
  34. Staples A, Adams WJ, Parkerton TF, Gorsuch JW, Biddinger GR, Reinert KH (1997) Aquatic toxicity of eighteen phthalate esters. Environ Toxicol Chem 16(5):875–891CrossRefGoogle Scholar
  35. Stelzer CP, Snell TW (2003) Induction of sexual reproduction in Brachionus plicatilis (Monogononta, Rotifera) by a density-dependent chemical cue. Limnol Oceanogr 48(2):939–943CrossRefGoogle Scholar
  36. Stout EP, La Clair JJ, Snell TW, Shearer TL, Kubanek J (2010) Conservation of progesterone hormone function in invertebrate reproduction. Proc Natl Acad Sci USA 107(26):11859–11864CrossRefGoogle Scholar
  37. Summary Risk Assessment Report on DEHP, European Commission (2008). Institute for Health and Consumer Protection, Toxicology and Chemical Substance (TCS), European Chemicals Bureau, Ispra (VA) Italy. ISSN 1018–5593.
  38. Technical Guidance Document on Risk Assessment Part II (2003) in support of Commission Directive 93/67/EEC on Risk Assessment for new notified substances, Commission Regulation (EC) No 1488/94 on Risk Assessment for existing substances, Directive 98/8/EC of the European Parliament and of the Council concerning the placing of biocidal products on the market. European Commission, Joint Research Centre, European Chemicals Bureau, Ispra, ItalyGoogle Scholar
  39. Thompson CJ, Ross SM, Hensley J, Liu KJ, Heinze SC, Young SS, Gaido KW (2005) Differential steroidogenic gene expression in the fetal adrenal gland versus the testis and rapid and dynamic response of the fetal testis to di(n-butyl) phthalate. Biol Reprod 73(5):908–917CrossRefGoogle Scholar
  40. Vandenberg LN, Colborn T, Hayes TB, Heindel JJ, Jacobs DR, Lee D-H Jr, Shioda T, Soto AM, vom Saal FS, Welshons WV, Zoeller RT, Myers JP (2012) Hormones and endocrine-disrupting chemicals: low-dose effects and nonmonotonic dose responses. Endocr Rev 33(3):378–455CrossRefGoogle Scholar
  41. Viroux L (1999) Zooplankton distribution in flowing waters and its implications for sampling: case studies in the River Meuse (Belgium) and the River Moselle (France, Luxembourg). J Plankton Res 21(7):1231–1248CrossRefGoogle Scholar
  42. Wallace RL, Snell TW (1991) Rotifera. In: Thorp J, Covich A (eds) Ecology and classification of North American freshwater invertebrates. Academic Press, New York, pp 187–248Google Scholar
  43. Wuttke W, Jarry H, Seidlova-Wuttke D (2010) Definition, classification and mechanism of action of endocrine disrupting chemicals. Horm Int J Endocrinol Metab 9(1):9–15Google Scholar
  44. Zha CW, Xi YL, Huang L, Zhao LL (2007) Effect of sublethal exposure to chlordecone on life history characteristics of freshwater rotifer Brachionus calyciflorus Pallas. Bull Environ Contam Toxicol 78(1):79–83CrossRefGoogle Scholar
  45. Zhao LL, Xi YL, Huang L, Zha CW (2009) Effects of three phthalate esters on the life-table demography of freshwater rotifer Brachionus calyciflorus Pallas. Aquat Ecol 43(2):395–402CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • V. Cruciani
    • 1
  • C. Iovine
    • 1
  • J.-P. Thomé
    • 1
  • C. Joaquim-Justo
    • 1
  1. 1.Laboratory of Animal Ecology and EcotoxicologyUniversity of LiègeLiègeBelgium

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