Ecotoxicology

, Volume 19, Issue 5, pp 901–910 | Cite as

Effects of 4-nonylphenol, fish predation and food availability on survival and life history traits of Daphnia magna straus

  • Meryem Beklioglu
  • S. Banu Akkas
  • H. Elif Ozcan
  • Gizem Bezirci
  • Inci Togan
Article

Abstract

This study aimed to investigate the compound effect of environmentally relevant 4-nonylphenol (NP) concentrations and natural stressors—namely fish predation and food availability—on Daphnia magna, which were exposed to four NP concentrations (0, 1, 5 and 10 μg l−1) under optimum or low food concentrations (1.00 and 0.075 mg C l−1, respectively) in water (un)conditioned by a fish predator (Alburnus alburnus). A(n) “environmentally relevant” and “no observable effect” concentration (NOEC) of NP (10 μg l−1) resulted in a significant reduction (P < 0.01**) in daphnids’ survival when it was encountered concurrently with conditions of low food availability and presence of fish predation. The significance of the results lies in the observation that not only environmentally relevant concentrations of NP but also NP concentrations reported to have no observable effect on daphnids may in reality have unexpected critical effects on D. magna survival under conditions more parallel to natural ecosystems. The deterioration of the life-history traits—namely, NP-induced delay in the age at first reproduction (P < 0.001***) and fish kairomone-induced reduction in the size at first reproduction (P < 0.001***)—of the D. magna individuals is also crucial, as such alterations could significantly influence future generations and result in ultimate adverse effects at the community level because large-bodied daphnids are key-stone species in freshwater ecosystems. The results of this study demonstrate the importance of taking into account environmentally realistic conditions while investigating the effects of NOEC levels of toxicants on non-target aquatic species.

Keywords

First clutch Clutch size Ecotoxicology Multiple stressors Toxicity tests 

References

  1. Ahel M, Giger W, Koch M (1994a) Behaviour of alkylphenol polyethoxyrate surfactants in the aquatic environment—I. Occurrence and transformation in sewage treatment. Water Res 28:1131–1142CrossRefGoogle Scholar
  2. Ahel M, Giger W, Schaffner C (1994b) Behaviour of alkylphenol polyethoxyrate surfactants in the aquatic environment—II. Occurrence and transformation in rivers. Water Res 28:1143–1152CrossRefGoogle Scholar
  3. Akkas SB, Kepenek AO, Beklioglu M, Severcan F (2010) Molecular approach to the chemical characterization of fish-exuded kairomone: a Fourier transform infrared spectroscopic study. Aquat Sci 72:71–83CrossRefGoogle Scholar
  4. Andersen HR, Wollenberger L, Halling-Sorensen B, Kusk KO (2001) Development of copepod nauplii to copepodites—a parameter for chronic toxicity including endocrine disruption. Environ Toxicol Chem 20:2821–2829Google Scholar
  5. Baer KN, Owens KD (1999) Evaluation of selected endocrine disrupting compounds on sex determination in Daphnia magna using reduced photoperiod and different feeding rates. B Environ Contam Tox 62:214–221CrossRefGoogle Scholar
  6. Baldwin WS, Milam DL, LeBlanc GA (1995) Physiological and biochemical perturbation in Daphnia magna following exposure to the model environmental estrogen diethylstilbestrol. Environ Toxicol Chem 14:945–952Google Scholar
  7. Baldwin WS, Graham SE, Shea D, LeBlanc GA (1997) Metabolic androgenization of female Daphnia magna by the xenoestrogen 4-nonylphenol. Environ Toxicol Chem 16:1905–1911Google Scholar
  8. Barry MJ, Meehan BJ (2000) The acute and chronic toxicity of lanthanum to Daphnia carinata. Chemosphere 41:1669–1674CrossRefGoogle Scholar
  9. Beklioglu M, Ince O, Tuzun I (2003) Restoration of the eutrophic Lake Eymir, Turkey, by biomanipulation after a major external nutrient control. Hydrobiologia 490:93–105CrossRefGoogle Scholar
  10. Beklioglu M, Cetin AG, Zorlu P, Ay-Zog D (2006a) Role of planktonic bacteria in biodegradation of fish-exuded kairomone in laboratory bioassays of diel vertical migration. Arch Hydrobiol 165:89–104CrossRefGoogle Scholar
  11. Beklioglu M, Telli M, Cetin AG (2006b) Fish and mucus-dwelling bacteria interact to produce a kairomone that induces diel vertical migration in Daphnia. Freshw Biol 51:2200–2206CrossRefGoogle Scholar
  12. Blackburn MA, Waldock MJ (1995) Concentrations of alkylphenols in rivers and estuaries in England and Wales. Water Res 29:1623–1629CrossRefGoogle Scholar
  13. Blom A, Ekman E, Johannisson A, Norrgren L, Pesonen M (1998) Effects of xenoestrogenic environmental pollutants on the proliferation of a human breast cancer cell line (MCF-7). Arch Environ Con Tox 34:306–310CrossRefGoogle Scholar
  14. Boersma M, De Meester L, Spaak P (1999) Environmental stress and local adaptation in Daphnia magna. Limnol Oceanogr 44:393–402Google Scholar
  15. Burkhardt-Holm P, Wahli T, Meier W (2000) Nonylphenol affects the granulation pattern of epidermal mucous cells in rainbow trout Oncorhynchus mykiss. Ecotox Environ Saf 46:34–40CrossRefGoogle Scholar
  16. Cairns J Jr (1983) Are single species toxicity tests alone adequate for estimating environmental hazard? Hydrobiologia 100:47–57CrossRefGoogle Scholar
  17. Cakmak G, Togan I, Severcan F (2003) FT-IR spectroscopic analysis of rainbow trout liver exposed to nonylphenol. Appl Spectrosc 57:835–841CrossRefGoogle Scholar
  18. Cakmak G, Togan I, Severcan F (2006) 17β-Estradiol induced compositional, structural and functional changes in rainbow trout liver, revealed by FT-IR spectroscopy: A comparative study with nonylphenol. Aquat Toxicol 77:53–63CrossRefGoogle Scholar
  19. Christiansen T, Korsgaard B, Jespersen A (1998) Induction of vitellogenin synthesis by nonylphenol and 17 beta -estradiol and effects on the testicular structure in the eelpout Zoarces viviparus. Mar Environ Res 46:141–144CrossRefGoogle Scholar
  20. De Meester L, Weider LJ (1999) Depth-selection behavior, fish kairomones, and the life histories of Daphnia hyalina x galeata hybrid clones. Limnol Oceanogr 44:1248–1258CrossRefGoogle Scholar
  21. DeMott WR (1983) Seasonal succession in a natural Daphnia assemblage. Ecol Monogr 53:321–340CrossRefGoogle Scholar
  22. Dinan L, Bourne P, Whiting P, Dhadialia TS, Hutchinson TH (2001) Screening of environmental contaminants for ecdysteroid agonist and antagonist activity using the Drosophila melanogaster B11 cell in vitro assay. Environ Toxicol Chem 20:2038–2046Google Scholar
  23. Doksæter A, Vijverberg J (2001) The effects of food and temperature regimes on life-history responses to fish kairomones in Daphnia hyalina galeata. Hydrobiologia 442:207–214CrossRefGoogle Scholar
  24. Ferrao-Filho AS, Azevedo S (2003) Effects of unicellular and colonial forms of toxic Microcystis aeruginosa from laboratory cultures and natural populations on tropical cladocerans. Aquat Ecol 37:23–35CrossRefGoogle Scholar
  25. Fliedner A (1993) Daphnia magna, Reproduction test (OECD No. 202). FraunhoferBInstitute fur Umweltchemie und Okotoxikologie, Postfach 1260, WB5948 Schmallenberg B Grafschaft, Germany. Report No. UBAB002/4B22 FebruaryGoogle Scholar
  26. Folt CL, Chen CY, Moore MV, Burnaford J (1999) Synergism and antagonism among multiple stressors. Limnol Oceanogr 44:864–877CrossRefGoogle Scholar
  27. Gerritsen J, Porter KG, Strickler JR (1988) Not by sieving alone: observations on suspension feeding in Daphnia. Bull Mar Sci 43:366–376Google Scholar
  28. Ghekiere A, Verslycke T, Janssen CR (2006) Effects of methoprene, nonylphenol and estrone on the vitellogenesis of the mysid Neomysis integer. Gen Comp Endocr 147:190–195CrossRefGoogle Scholar
  29. Gibble R, Baer KN (2003) Effects of 4-nonylphenol on sexual maturation in Daphnia magna. B Environ Contam Tox 70:315–321CrossRefGoogle Scholar
  30. Giger W, Brunner PH (1984) 4-Nonyl phenol in sewage sludge: accumulation of toxic metabolites from nonionic surfactants. Science 225:623–625CrossRefGoogle Scholar
  31. Gourmelon A, Ahtiainen J (2007) Developing test guidelines on invertebrate development and reproduction for the assessment of chemicals, including potential endocrine active substances—The OECD perspective. Ecotoxicology 16:161–167CrossRefGoogle Scholar
  32. Hanazato T (1995) Combined effect of the insecticide carbaryl and the Chaoborus kairomone on helmet development in Daphnia ambigua. Hydrobiologia 310:95–100CrossRefGoogle Scholar
  33. Hanazato T (1998a) Predator kairomones reduce tolerance of Daphnia to environmental stress and control their population dynamics: an indirect effect of predators. Verhandlungen Internationale Vereingungen Limnologie 26:1941–1944Google Scholar
  34. Hanazato T (1998b) Response of a zooplankton community to insecticide application in experimental ponds: a review and the implications of the effects of chemicals on the structure and functioning of freshwater communities. Environ Pollut 101:361–373CrossRefGoogle Scholar
  35. Hanazato T (1999) Anthropogenic chemicals (insecticides) disturb natural organic chemical communication in the plankton community. Environ Pollut 105:137–142CrossRefGoogle Scholar
  36. Hanazato T, Dodson SI (1992) Complex effects of a kairomone of Chaoborus and an insecticide on Daphnia pulex. J Plankton Res 14:1743–1755CrossRefGoogle Scholar
  37. Hanazato T, Dodson SI (1995) Synergistic effects of low oxygen concentration, predator kairomone, and a pesticide on the cladoceran Daphnia pulex. Limnol Oceanogr 40:700–709CrossRefGoogle Scholar
  38. Harvell CD (1990) The ecology and evolution of inducible defenses. Q Rev Biol 65:323–340CrossRefGoogle Scholar
  39. Hense BA, Jüttner I, Welzl G, Severin GF, Pfister G, Behechti A, Schramm KW (2003) Effects of 4-nonylphenol on phytoplankton and periphyton in aquatic microcosms. Environ Toxicol Chem 22:2727–2732CrossRefGoogle Scholar
  40. Hense BA, Severin GF, Pfister G, Welzl G, Jaser W, Schramm KW (2005) Effects of anthropogenic estrogens nonylphenol and 17α-ethinylestradiol in aquatic model ecosystems. Acta Hydrochim Hydrobiol 33:27–37CrossRefGoogle Scholar
  41. Hu SS, Tessier AJ (1995) Seasonal succession and the strength of intra- and interspecific competition in a Daphnia assemblage. Ecology 76:2278–2294CrossRefGoogle Scholar
  42. Hughes PJ, McLellan H, Lowes DA, Khan SZ, Bilmen JG, Tovey SC, Godfrey RE, Michell RH, Kirk CJ, Michelangeli F (2000) Estrogenic alkylphenols induce cell death by inhibiting testis endoplasmic reticulum Ca2+ pumps. Biochem Biophys Res Commun 277:568–574CrossRefGoogle Scholar
  43. Jobling S, Sheahan D, Osborne JA, Methiessen P, Sumpter JP (1996) Inhibition of testicular growth in rainbow trout (Oncorhynchus mykiss) exposed to estrogenic alkylphenolic chemicals. Environ Toxicol Chem 15:194–202Google Scholar
  44. Kvestak R, Ahel M (1994) Occurrence of toxic metabolites from nonionic surfactants in the Krka River estuary. Ecotox Environ Saf 28:25–34CrossRefGoogle Scholar
  45. Lampert W (1978) A field study on the dependence of the fecundity of Daphnia spcc. on food concentration. Oecologia 36:363–369CrossRefGoogle Scholar
  46. Lampert W (1987) Feeding and nutrition in Daphnia. Memorie dell Istituto Italiano di Idrobiologia 45:143–192Google Scholar
  47. Lampert W, Fleckner W, Rai H, Taylor BE (1986) Phytoplankton control by grazing zooplankton: a study on the spring clear-water phase. Limnol Oceanogr 31:478–490CrossRefGoogle Scholar
  48. Larsson P, Dodson SI (1993) Chemical communication in planktonic animals. Arch Hydrobiol 129:129–155Google Scholar
  49. Lass S, Spaak P (2003) Chemically induced anti-predator defenses in plankton: a review. Hydrobiologia 491:221–239CrossRefGoogle Scholar
  50. LeBlanc GA (2007) Crustacean endocrine toxicology: a review. Ecotoxicology 16:61–81CrossRefGoogle Scholar
  51. LeBlanc GA, Mu X, Rider CV (2000) Embryotoxicity of the alkylphenol degradation product 4-nonylphenol to the crustacean Daphnia magna. Environ Health Perspect 108:1133–1138CrossRefGoogle Scholar
  52. Loose CJ, von Elert E, Dawidowicz P (1993) Chemically induced diel vertical migration in Daphnia—a new bioassay for kairomones exuded by fish. Arch Hydrobiol 126:329–337Google Scholar
  53. Lynch M (1989) The life history consequences of resource depression in Daphnia pulex. Ecology 70:246–256CrossRefGoogle Scholar
  54. Machácěk J (1991) Indirect effect of planktivorous fish on the growth and reproduction of Daphnia galeata. Hydrobiologia 225:193–197CrossRefGoogle Scholar
  55. McCauley E, Murdoch WW, Nisbet RM, Gurney WSC (1990) The physiological ecology of Daphnia: development of a model of growth and reproduction. Ecology 71:703–715CrossRefGoogle Scholar
  56. Michels E, Semsari S, Bin C, De Meester L (2000) Effect of sublethal doses of cadmium on the phototactic behavior of Daphnia magna. Ecotox Environ Saf 47:261–265CrossRefGoogle Scholar
  57. Moss B (1998) Ecology of freshwaters: man and medium, past to future, 3rd edn. Blackwell Science, OxfordGoogle Scholar
  58. Muluk CB, Beklioglu M (2005) Lack of a typical diel vertical migration: varying role of water clarity, food, and dissolved oxygen in Lake Eymir, Turkey. Hydrobiologia 537:139–149CrossRefGoogle Scholar
  59. Naylor CG (1995) Environmental fate and safety of nonylphenol ethoxylates. Text Chem Color 27:29–33Google Scholar
  60. Orcutt JD Jr, Porter KG (1984) The synergistic effects of temperature and food concentration on life history parameters in Daphnia. Oecologia 63:300–306CrossRefGoogle Scholar
  61. Organization for Economic Cooperation and Development (1984) Daphnia sp., acute immobilisation test and reproduction test. OECD Guideline 202. April 4. Paris, FranceGoogle Scholar
  62. Organization for Economic Cooperation and Development (1998) Daphnia magna reproduction test. OECD Guideline 211. September 21. Paris, FranceGoogle Scholar
  63. SAS (2002) SAS System for Windows. Release 8.2. SAS Institute Inc., Cary, NCGoogle Scholar
  64. Segner H, Caroll K, Fenske M, Janssen CR, Maack G, Pascoe D, Schafers C, Vandenberg GF, Watts M, Wenzel A (2003) Identification of endocrine-disrupting effects in aquatic vertebrates and invertebrates: report from the European IDEA project. Ecotox Environ Saf 54:302–314CrossRefGoogle Scholar
  65. Shurin JB, Dodson SI (1997) Effects of cyanobacteria and nonylphenol on environmental sex determination and development in Daphnia. Environ Toxicol Chem 16:1269–1276Google Scholar
  66. Skakkebaek NE, Rajpert-De Meyts R, Jørgensen N, Carlsen E, Peterson PM, Giwercman A, Andersen AG, Jensen TK, Andersson AM, Müller J (1998) Germ cell cancer and disorders of spermatogenesis: an environmental connection? APMIS 106:3–12CrossRefGoogle Scholar
  67. SPSS (2004) SPSS for Windows. Version 13.0. SPSS Inc., ChicagoGoogle Scholar
  68. Stibor H (1992) Predator induced life-history shifts in a freshwater cladoceran. Oecologia 92:162–165CrossRefGoogle Scholar
  69. Stibor H, Lüning J (1994) Predator induced phenotypic variation in the pattern of growth and reproduction in Daphnia hyalina (Crustacea: Cladocera). Funct Ecol 8:97–101CrossRefGoogle Scholar
  70. Sun H, Gu X (2005) Comprehensive toxicity study of nonylphenol and short-chain nonylphenol polyethoxylates on Daphnia magna. B Environ Contam Tox 75:677–683CrossRefGoogle Scholar
  71. Tatarazako N, Oda S (2007) The water flea Daphnia magna (Crustacea, Cladocera) as a test species for screening and evaluation of chemicals with endocrine disrupting effects on crustaceans. Ecotoxicology 16:197–203CrossRefGoogle Scholar
  72. Thornton JW, Need E, Crews D (2003) Resurrecting the ancestral steroid receptor: ancient origin of estrogen signaling. Science 301:1714–1717CrossRefGoogle Scholar
  73. Threlkeld ST (1976) Starvation and the size structure of zooplankton communities. Freshw Biol 6:489–496CrossRefGoogle Scholar
  74. Threlkeld ST (1979) The midsummer dynamics of two Daphnia species in Wintergreen Lake, Michigan. Ecology 60:165–179CrossRefGoogle Scholar
  75. Tollrian R, Dodson SI (1999) Inducible defences in cladocera, constraints, costs, and multi-predator environments. In: Tollrian R, Harvell CD (eds) The ecology and evolution of inducible defenses. Princeton University Press, Princeton, New Jersey, pp 306–321Google Scholar
  76. Uguz C, Togan I, Eroglu Y, Tabak I, Zengin M, Iscan M (2003) Alkylphenol concentrations in two rivers of Turkey. Environ Toxicol Phar 14:87–88CrossRefGoogle Scholar
  77. Urabe J, Clasen J, Sterner RW (1997) Phosphorus limitation of Daphnia: is it real? Limnol Oceanogr 42:1436–1443CrossRefGoogle Scholar
  78. Von Elert E (2002) Determination of limiting polyunsaturated fatty acids in Daphnia galeata using a new method to enrich food algae with single fatty acids. Limnol Oceanogr 47:1764–1773CrossRefGoogle Scholar
  79. von Elert E, Stibor H (2006) Predator-mediated life history shifts in Daphnia: enrichment and preliminary chemical characterisation of a kairomone exuded by fish. Arch Hydrobiol 167:21–35CrossRefGoogle Scholar
  80. Weber A (2001) Interactions between predator kairomone and food level complicate the ecological interpretation of Daphnia laboratory results. J Plankton Res 23:41–46CrossRefGoogle Scholar
  81. Weider LJ, Pijanowska J (1993) Plasticity of Daphnia life history in response to chemical cues from predators. Oikos 67:385–392CrossRefGoogle Scholar
  82. Weltje L, com Saal FS, Oehlmann J (2005) Reproductive stimulation by low doses of xenoestrogens contrasts with the view of hormesis as an adaptive response. Hum Exp Toxicol 24:431–437CrossRefGoogle Scholar
  83. Zhang C, Xie Y, Martignetti JA, Yeo TT, Massa SM, Longo FM (2003) A candidate chimeric mammalian mRNA transcript is derived from distinct chromosomes and is associated with nonconsensus splice junction motifs. DNA Cell Biol 22:303–315CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Meryem Beklioglu
    • 1
  • S. Banu Akkas
    • 1
  • H. Elif Ozcan
    • 1
  • Gizem Bezirci
    • 1
  • Inci Togan
    • 1
  1. 1.Biology DepartmentMiddle East Technical UniversityAnkaraTurkey

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