Advertisement

Ecotoxicology

, Volume 23, Issue 9, pp 1764–1773 | Cite as

Effects of dietborne cadmium on life history and secondary production of a tropical freshwater cladoceran

  • J. P. Souza
  • D. C. Melo
  • A. T. Lombardi
  • M. G. G. Melão
Article

Abstract

The presence of metals in aquatic environments has increased worldwide. Environmental assessments of metals in freshwater ecosystems presume that toxicity is mainly caused by aqueous exposure, but dietborne exposure (contaminated food) in zooplankton may occur because microalgae carry metal ions through adsorption/absorption of dissolved metal species, resulting in toxic effects once ingested by the animals. However, official regulations for ecotoxicological assays in most countries do not consider the toxic effects caused by dietborne exposure. Here, we provide life history parameters and secondary production of Simocephalus serrulatus (Koch 1841) (Cladocera: Daphniidae) fed with cadmium (Cd) contaminated algae during a 21-day bioassay. The microalgae Chlorophyceae Scenedesmus quadricauda was exposed for 96 h to dissolved Cd concentrations of 0.03; 5.87; 12.27 and 22.27 µg Cd l−1 (equivalent to 1.6 × 10−10; 3.2 × 10−8; 6.7 × 10−8; 1.2 × 10−7 mol l−1) that resulted in algae internal Cd burdens of 0.004; 0.032; 0.270 and 0.280 pg Cd cell−1, respectively. Significant toxic effects on life history parameters of S. serrulatus were observed. Time of embryonic development, generation time and age at first reproduction (primipara) showed significant delay. Length at first reproduction, number of eggs and clutches produced per female, hatching percentage, body length, survival and feeding rates were significantly reduced. Secondary production, that is, accumulated biomass for growth and reproduction, decreased significantly with dietborne Cd concentrations. Our results emphasize that food can be an important source of metals to zooplankton in aquatic ecosystems. Environmental regulations should consider the diet in ecotoxicological assessments. Furthermore, secondary production may be considered as a suitable endpoint in ecotoxicity tests.

Keywords

Ecotoxicity Food Metal Microalgae Zooplankton 

Notes

Acknowledgments

This work was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo - FAPESP (Proc. No. 2008/03487-0; 2008/02078-9; 2008/05464-7) and Conselho Nacional de Desenvolvimento Científico e Tecnológico - CNPq (Proc. No. 305183/2008-7; 556588/2009-6). The authors thank Dr. Hugo Sarmento for your assistance in the paper review.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Amiard JC, Amiard-Trquet C, Barka S, Pellerin J, Rainbow PS (2006) Metallothioneins in aquatic invertebrates: their role in metal detoxification and their use as biomakers. Aquat Toxicol 76:160–202CrossRefGoogle Scholar
  2. Associação Brasileira de Normas Técnicas (ABNT) (2005) Avaliação da toxicidade crônica utilizando Ceriodaphnia spp., (Cladocera, Crustacea). NBR13373Google Scholar
  3. Association Française Normalisation (AFNOR) (1980) Essais deseaux Determination de I’inhibition de Scenesdesmus subspicatus par une substance. Norme experimentale T90-304Google Scholar
  4. Baillieul M, Smolders R, Blust R (2005) The effect of environmental stress on absolute and mass-specific scope for growth in Daphnia magna Strauss. Comp Biochem Physiol C 140:364–373Google Scholar
  5. Barata C, Baird DJ (2000) Determining the ecotoxicological mode of action of chemicals from measurements made on individuals: results from instar-based tests with Daphnia magna Straus. Aquat Toxicol 48:195–209CrossRefGoogle Scholar
  6. Barata C, Markich SJ, Baird DJ, Soares AMVM (2002) The relative importance of water food as cadmium sources to Daphnia magna Straus. Aquat Toxicol 61:143–154CrossRefGoogle Scholar
  7. Barber I, Baird DJ, Calow P (1994) Effect of cadmium and ration level on oxygen consumption, RNA concentration and RNA-DNA ratio in two clones of Daphnia magna Straus. Aquat Toxicol 30:249–258CrossRefGoogle Scholar
  8. Bossuyt BTA, Janssen CR (2005) Copper toxicity to different field-collected cladoceran species: intra- and inter-species sensitivity. Environ Pollut 136:145–154CrossRefGoogle Scholar
  9. Bottrell HH, Duncan A, Gliwicz ZM, Grygierek E, Herzig A, Hillbricht-Ilkowska A, Kurasaua H, Larsson P, Weglenska T (1976) A review of some problems in zooplankton production studies. Norw J Zool 24:419–456Google Scholar
  10. Conselho Nacional do Meio Ambiente (CONAMA) (2005). Resolução nº 357 de 17 de março. Ministério do Meio Ambiente http://www.mma.gov.br/pot/conama. Accessed June 2014
  11. De Schamphelaere KAC, Forrez I, Dierckens K, Sorgeloos P, Janssen CR (2007) Chronic toxicity of dietary copper to Daphnia magna. Aquat Toxicol 81:409–418CrossRefGoogle Scholar
  12. Debelius B, Forja JM, DelValls A, Lubián LM (2009) Toxicity and bioaccumulation of copper and lead in five marine microalgae. Ecotoxicol Environ Saf 72:1503–1513CrossRefGoogle Scholar
  13. Downing JA, Rigler FH (1984) A manual of methods for the assessment of secondary productivity in freshwater. Blackwell Scientific, Oxford and Edinburgh, OxfordGoogle Scholar
  14. Edmondson WT, Winberg GG (1971) A manual on methods for the assessment of secondary productivity in freshwaters. Blackwell Scientific, Oxford and Edinburgh, OxfordGoogle Scholar
  15. El-Moor-Loureiro LMA (1997) Manual para a identificação dos Cladocera límnicos brasileiros. Universa: Universidade Católica de Brasília, BrasíliaGoogle Scholar
  16. Emsley J (1998) The elements. Clarendon Press Oxford, LondonGoogle Scholar
  17. Faupel M, Traunspurger W (2012) Secondary production of zoobenthic community under metal stress. Water Res 46:3345–3352CrossRefGoogle Scholar
  18. Faupel M, Ristau K, Traunspurger W (2011) Biomass estimation across the benthic community in polluted freshwater sediment: a promising endpoint in microcosm studies? Ecotoxicol Environ Saf 74:1942–1950CrossRefGoogle Scholar
  19. Faupel M, Ristau K, Traunspurger W (2012) The functional response of a freshwater benthic community to cadmium pollution. Environ Pollut 162:104–109CrossRefGoogle Scholar
  20. Gauld DT (1951) The grazing rate of planktonic copepods. J Mar Biol Assoc UK 29:695–705CrossRefGoogle Scholar
  21. Geffard O, Geffard A, Chaumot A, Vollat B, Alvarez C, Tusseau-Vuillemin MH, Garric J (2008) Effects of chronic dietary and waterborne cadmium exposures on the contamination level and reproduction of Daphnia magna. Environ Toxicol Chem 27:1128–1134CrossRefGoogle Scholar
  22. Goulet RR, Krack S, Doyle PJ, Hare L, Vigneault B, McGeer JC (2007) Dynamic multipathway modeling of Cd bioaccumulation in Daphnia magna using waterborne and dietborne exposure. Aquat Toxicol 81:117–125CrossRefGoogle Scholar
  23. Gusso-Choueri PK, Choueri RB, Lombardi AT, Melão MGG (2012) Effects of dietary cadmium on life-history traits of a tropical freshwater cladoceran. Arch Environ Contam Toxicol 62:589–598CrossRefGoogle Scholar
  24. Hickey CW (1989) Sensitivity of four New Zealand cladoceran species and Daphnia magna to aquatic toxicants. N Z J Mar Freshw Res 23:131–137CrossRefGoogle Scholar
  25. Hook SE, Fisher NS (2000) Exposure to silver via food reduces egg production and viability in herbivorous copepods and cladocerans. Mar Environ Res 50:545–552CrossRefGoogle Scholar
  26. Khoshmanesh A, Lawson F, Pince IG (1996) Cadmium uptake by unicellular green microalgae. The Chem Eng J 62:81–88Google Scholar
  27. Knops M, Altenburger R, Seger H (2001) Alterations of physiological energetics, growth and reproduction of Daphnia magna under toxicant stress. Aquat Toxicol 53:79–90CrossRefGoogle Scholar
  28. Kooijman SALM (2000) Dynamic energy and mass budgets in biological systems. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  29. Lombardi AT, Vieira AAH, Sartori LA (2002) Muscilaginous capsule adsorption and intracellular uptake of copper by Kircheriella aperta (Chlorococcales). J Phycol 38:332–337CrossRefGoogle Scholar
  30. Lores EM, Pennock JR (1999) Bioavailability and trophic transfer of humic-bound copper from bacteria to zooplankton. Mar Ecol Progr Ser 187:67–75CrossRefGoogle Scholar
  31. Munger C, Hare L, Craig A, Charest PM (1999) Influence of exposure time on the distribution of cadmium within the cladoceran Ceriodaphnia dubia. Aquat Toxicol 44:195–200CrossRefGoogle Scholar
  32. Muyssen BTA, Bossuyt BTA, Janssen CR (2005) Inter- and intra-species variation in acute zinc tolerance of field-collected cladoceran populations. Chemosphere 61:1159–1167CrossRefGoogle Scholar
  33. Nogueira AJA, Baird DJ, Soares AMVM (2004) Testing physiologically based resource allocation rules in laboratory experiments with Daphnia magna Straus. Ann Limnol Int J Limnol 40:257–267CrossRefGoogle Scholar
  34. Nogueira PFM, Melão MGG, Lombardi AT, Vieira AAH (2005) The effects of Anabaena spiroides (Cyanophyceae) exopolysaccharide on copper toxicity to Simocephalus serrulatus (Cladocera, Daphnidae). Freshw Biol 50:1560–1567CrossRefGoogle Scholar
  35. Organization for Economic Cooperation and Development (OECD) (1998) Test Guideline Nº. 211: Daphnia magna reproduction test. OECD 211Google Scholar
  36. Organization for Economic Cooperation and Development (OECD) (2006) Guidelines for the testing of chemicals. Nº. 211: Freshwater Alga and Cyanobacteria. Growth Inhibition Test. OECD 211Google Scholar
  37. Organization for Economic Cooperation and Development (OECD) (2007) Guidelines for the testing of chemicals. Nº. 225: Sediment-Water Lumbriculus Toxicity Test Using Spiked Sediment. OECD 225Google Scholar
  38. Rodgher S, Espíndola ELG (2008) Effects of interactions between algal densities and cadmium concentrations on Ceriodaphnia dubia fecundity and survival. Ecotoxicol Environ Saf 71:765–773CrossRefGoogle Scholar
  39. Rodgher S, Lombardi AT, Melão MGG (2009) Evaluation onto life cycle parameters of Ceriodaphnia silvestrii submitted to 36 days dietary copper exposure. Ecotoxicol Environ Saf 72:1748–1753CrossRefGoogle Scholar
  40. Ruangsomboon S, Wongrat L (2006) Bioaccumulation of cadmium in an experimental aquatic food chain involving phytoplankton (Chlorella vulgaris), zooplankton (Moina macrocopa), and the predatory catfish Clarias macrocephalus × C. gariepinus. Aquat Toxicol 78:15–20CrossRefGoogle Scholar
  41. Smolders R, Baillieul M, Blust R (2005) Relationship between the energy status of Daphnia magna and its sensitivity to environmental stress. Aquat Toxicol 73:155–170CrossRefGoogle Scholar
  42. Sofyan A, Price DJ, Wesley JB (2007) Effects of aqueous, dietary and combined exposure of cadmium to Ceriodaphnia dubia. Sci Total Environ 385:108–116CrossRefGoogle Scholar
  43. Taylor G, Baird DJ, Soares AMVM (1998) Surface binding of contaminants by algae: consequences for lethal toxicity and feeding to Daphnia magna Straus. Environ Toxicol Chem 17:412–419CrossRefGoogle Scholar
  44. United States Environmental Protection Agency (USEPA) (1996) Ecological effects test guidelines. Daphinid Chronic Toxicity Test. EPA/OPPTS 850.1300/1996Google Scholar
  45. Wang ZS, Kong HN, Wu DY (2009) Acute and chronic copper toxicity to a saltwater cladoceran Moina monogolica Daday. Arch Environ Contam Toxicol 53:50–56CrossRefGoogle Scholar
  46. Wang Z, Yan C, Hynez RV (2010) Effects of dietary cadmium exposure on reproduction of saltwater cladoceran Moina monogolica Daday: implications in Water Quality Criteria. Environ Toxicol Chem 29:365–372CrossRefGoogle Scholar
  47. Winberg GG (1971) Methods for the estimation of production of aquatic animals. Academic Press, Inc., London Ltd and New YorkGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • J. P. Souza
    • 1
  • D. C. Melo
    • 1
  • A. T. Lombardi
    • 2
  • M. G. G. Melão
    • 1
  1. 1.Plankton Laboratory, Hydrobiology DepartmentFederal University of São CarlosSão CarlosBrazil
  2. 2.Algae Biotechnology Laboratory, Botany DepartmentFederal University of São CarlosSão CarlosBrazil

Personalised recommendations