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Reproduction recovery of the crustacean Daphnia magna after chronic exposure to ibuprofen

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Abstract

In mammals, the pharmaceutical ibuprofen (IB), a non-steroidal anti-inflammatory drug, primarily functions by reversibly inhibiting the cyclooxygenase (COX) pathway in the synthesis of eicosanoids (e.g. prostaglandins). Previous studies suggest that IB may act in a similar manner to interrupt production of eicosanoids reducing reproduction in the model crustacean Daphnia magna. On this basis withdrawal of IB should lead to the recovery of D. magna reproduction. Here we test whether the effect of IB is reversible in D. magna, as it is in mammals, by observing reproduction recovery following chronic exposure. D. magna (5-days old) were exposed to a range of IB concentrations (0, 20, 40 and 80 mg l−1) for 10 days followed by a 10 day recovery period in uncontaminated water. During the exposure period, individuals exposed to higher concentrations produced significantly fewer offspring. Thereafter, IB-stressed individuals produced offspring faster during recovery, having similar average population growth rates (PGR) (1.15–1.28) to controls by the end of the test. It appears that maternal daphnids are susceptible to IB during egg maturation. This is the first recorded recovery of reproduction in aquatic invertebrates that suffered reproductive inhibition during chronic exposure to a chemical stressor. Our results suggest a possible theory behind the compensatory fecundity that we referred to as ‘catch-up reproduction’.

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References

  • Baird DJ, Barber I, Bradley MC, Calow P, Girling A, Soares AMVM (1989) The long-term maintenance of Daphnia magna Straus for use in ecotoxicity tests: problems and prospects. In: Løkke H, Tyle H, Bro-Rasmussen F (eds) Proceedings of the first European conference on ecotoxicology. National Environmental Research Institute, Lyngby, Denmark, pp 144–148

    Google Scholar 

  • Belanger SE, Farris JL, Cherry DS, Cairns J (1986) Growth of Asiatic clams (Corbicula sp.) during and after long-term zinc exposure in field-located and laboratory artificial streams. Arch Environ Contam Toxicol 15:427–434

    Article  CAS  Google Scholar 

  • Charlier C, Michaux C (2003) Dual inhibition of cyclooxygenase-2 (COX-2) and 5-lipoxygenase (5-LOX) as a new strategy to provide safer non-steroidal anti-inflammatory drugs. Eur J Med Chem 38:645–659

    Article  CAS  Google Scholar 

  • Forbes VE, Calow P (1999) Is the per capita rate of increase a good measure of population-level effects in ecotoxicology? Environ Toxicol Chem 18:1544–1556

    Article  CAS  Google Scholar 

  • Funk CD (2001) Prostaglandins and leukotrienes: advances in eicosanoid biology. Science 294:1871–1875

    Article  CAS  Google Scholar 

  • Heckmann LH, Boutard A, Hill C, Sibly R, Callaghan A (2007a) A simple and rapid method for preserving RNA of aquatic invertebrates for ecotoxicogenomics. Ecotoxicology 16:445–447

    Article  CAS  Google Scholar 

  • Heckmann LH, Callaghan A, Hooper HL, Connon R, Hutchinson TH, Maund SJ, Sibly RM (2007b) Chronic toxicity of ibuprofen to Daphnia magna: effects on life history traits and population dynamics. Toxicol Lett 172:137–145

    Article  CAS  Google Scholar 

  • Heckmann LH, Connon R, Hutchinson TH, Maund SJ, Sibly RM, Callaghan A (2006) Expression of target and reference genes in Daphnia magna exposed to ibuprofen. BMC Genomics 7:175

    Article  CAS  Google Scholar 

  • Heckmann LH, Sibly RM, Connon R, Hooper HL, Hutchinson TH, Maund SJ, Hill C, Boutard A, Callaghan A (submitted). Systems biology meets stress ecology: linking molecular and organismal stress responses in Daphnia magna. Genome Biol

  • Hooper HL, Connon R, Callaghan A, Fryer G, Yarwood-Buchanan S, Biggs J, Maund SJ, Hutchinson TH, Sibly RM (in press) Characterizing the ecological niche using population growth rate: How pH and calcium affect the field distribution of Daphnia magna. Ecology

  • Hooper HL, Connon R, Callaghan A, Maund SJ, Liess M, Duquesne S, Hutchinson TH, Moggs JG, Sibly RM (2006) The use of image analysis methods to estimate population growth rate in Daphnia magna. J Appl Ecol 43:828–834

    Article  Google Scholar 

  • Kooijman SALM (2000) Dynamic energy and mass budgets in biological systems. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Medeiros MN, Mendonca LH, Hunter AL, Paiva-Silva GO, Mello FG, Henze IP, Masuda H, Maya-Monteiro CM, Machado EA (2004) The role of lipoxygenase products on the endocytosis of yolk proteins in insects: participation of cAMP. Arch Insect Biochem Physiol 55:178–187

    Article  CAS  Google Scholar 

  • Nisbet RM, McCauley E, Gurney WSC, Murdoch WW, Wood SN (2004) Formulating and testing a partially specified dynamic energy budget model. Ecology 85:3132–3139

    Article  Google Scholar 

  • Nisbet RM, Muller EB, Lika K, Kooijman SALM (2000) From molecules to ecosystems through dynamic energy budget models. J Anim Ecol 69:913–926

    Article  Google Scholar 

  • OECD (1998) OECD guidelines for testing of chemicals. No. 211. Daphnia magna reproduction test. Organization for Economic Cooperation and Development, Paris, 21 pp

    Google Scholar 

  • Olmstead AW, Leblanc GA (2002) Juvenoid hormone methyl farnesoate is a sex determinant in the crustacean Daphnia magna. J Exp Zool 293:736–739

    Article  CAS  Google Scholar 

  • Pascoe D, Karntanut W, Muller CT (2003) Do pharmaceuticals affect freshwater invertebrates? A study with the cnidarian Hydra vulgaris. Chemosphere 51:521–528

    Article  CAS  Google Scholar 

  • Rowley AF, Vogan CL, Taylor GW, Clare AS (2005) Prostaglandins in non-insectan invertebrates: recent insights and unsolved problems. J Exp Biol 208:3–14

    Article  CAS  Google Scholar 

  • Sagi A, Silkovsky J, Fleisher-Berkovich S, Danon A, Chayoth R (1995) Prostaglandin E2 in previtellogenic ovaries of the prawn Macrobrachium rosenbergii: synthesis and effect on the level of cAMP. Gen Comp Endocrinol 100:308–313

    Article  CAS  Google Scholar 

  • Sibly RM, Calow P (1986) Physiological ecology of animals. An evolutionary approach. Blackwell Scientific Publications, Oxford, UK

    Google Scholar 

  • Sibly RM, Hansen FT, Forbes VE (2000) Confidence intervals for population growth rate of organisms with two-stage life histories. Oikos 88:335–340

    Article  Google Scholar 

  • Spaziani EP, Hinsch GW, Edwards SC (1993) Changes in prostaglandin E(2) and F2-alpha during vitellogenesis in the Florida cayfish Procambarus paeninsulanus. J Comp Physiol B: Biochem Syst Environ Physiol 163:541–545

    Article  CAS  Google Scholar 

  • Stanley D (2006) Prostaglandins and other eicosanoids in insects: biological significance. Annu Rev Entomol 51:25–44

    Article  CAS  Google Scholar 

  • Stanley DW (2000) Eicosanoids in invertebrate signal transduction systems. Princeton University Press, USA

    Google Scholar 

  • Stebbing ARD (1981) The kinetics of growth control in a colonial hydroid. J Mar Biol Ass UK 61:35–63

    Article  Google Scholar 

  • Tahara D, Suitoh K, Hattori H (2005) Hemolymph vitellogenin levels during final maturation and post-spawning in the female kuruma prawn, Marsupenaeus japonicus. Aquaculture 245:311–319

    Article  CAS  Google Scholar 

  • Tatarazako N, Oda S, Watanabe H, Morita M, Iguchi T (2003) Juvenile hormone agonists affect the occurrence of male Daphnia. Chemosphere 53:827–833

    Article  CAS  Google Scholar 

  • Ye XQ, Hama K, Contos JJA, Anliker B, Inoue A, Skinner MK, Suzuki H, Amano T, Kennedy G, Arai H, Aoki J, Chun J (2005) LPA(3)-mediated lysophosphatidic acid signalling in embryo implantation and spacing. Nature 435:104–108

    Article  CAS  Google Scholar 

  • Yokomizo T, Izumi T, Shimizu T (2001) Leukotriene B4: metabolism and signal transduction. Arch Biochem Biophys 385:231–241

    Article  CAS  Google Scholar 

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Acknowledgements

We are grateful to Prof. Taisen Iguchi (Okazaki Institute for Integrative Biosciences, National Institutes of Natural Sciences, Japan) for critically reading the manuscript. This work was supported financially by The Research Endowment Trust Fund of the University of Reading, AstraZeneca and Syngenta. We thank Nikoletta Antoniou and Michaelis Proteriotis for providing additional information on the chronic toxicity of ibuprofen, and two anonymous reviewers for their valuable comments on the manuscript.

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Correspondence to Lars-Henrik Heckmann.

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Hayashi, Y., Heckmann, LH., Callaghan, A. et al. Reproduction recovery of the crustacean Daphnia magna after chronic exposure to ibuprofen. Ecotoxicology 17, 246–251 (2008). https://doi.org/10.1007/s10646-008-0191-3

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  • DOI: https://doi.org/10.1007/s10646-008-0191-3

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