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Hydrobiologia

, Volume 759, Issue 1, pp 75–84 | Cite as

Effect of neurotoxic compounds on ephyrae of Aurelia aurita jellyfish

  • Elisa Costa
  • Chiara Gambardella
  • Veronica Piazza
  • Giuliano Greco
  • Silvia Lavorano
  • Martina Beltrandi
  • Elisabetta Bongiovanni
  • Guido Gnone
  • Marco Faimali
  • Francesca Garaventa
COELENTERATE BIOLOGY

Abstract

The aim of this study was to analyze the toxicity of two neurotoxic compounds on the ephyra stage of the Scyphozoan jellyfish Aurelia aurita, an innovative and sensitive model organism recently proposed in ecotoxicological bioassays. Indeed, jellyfish play an important role in the marine ecosystem, being a key component of the gelatinous zooplankton and of the marine food web, but are not represented in routine ecotoxicology. In this study, ephyrae were exposed to several concentrations (0, 0.1, 0.5, 1, 5, 10, 50 mg l−1) of eserine (ES) and chlorpyrifos (CPF), a carbamate and an organophosphorous compound, respectively, in order to analyze their toxic effect on this model organism. Acute (% of immobility) and behavioral (% alteration of frequency of pulsations) end-points were investigated after 24 and 48 h of exposure. Exposure to both compounds caused a dose-dependent effect, and for each end-point, it was possible to quantify these effects by means of EC50. Results highlighted how these compounds reported a high toxicity for marine organisms and exerted their toxic effect on this innovative biological model (in particular, CPF resulted to be more toxic than ES), which proved to be more sensitive than other marine invertebrates commonly used for ecotoxicological bioassays.

Keywords

Aurelia aurita Behavior Ecotoxicology Ephyrae Immobility Neurotoxic compounds 

Notes

Acknowledgements

The authors acknowledge RITMARE Flagship Project, a National Research Programme funded by the Italian Ministry of University and Research (MIUR).

References

  1. Anctil, M., 2009. Chemical transmission in the sea anemone Nematostella vectensis: a genomic perspective. Comparative Biochemistry and Physiology D 4: 268–289.Google Scholar
  2. Almeda, R. Z., C. Wambaugh, Z. Chai, Z. Wang & Z. Liu, 2013. Effects of crude oil exposure on bioaccumulation of polycyclic aromatic hydrocarbons and survival of adult and larval stages of gelatinous zooplankton. PLoS ONE 8(10): 74476. doi: 10.1371/journal.pone.0074476.CrossRefGoogle Scholar
  3. Arai, M. N., 2005. Predation on pelagic coelenterates: a review. Journal Marine Biological Association UK 85: 523–536.CrossRefGoogle Scholar
  4. Ashauer, R., A. Boxall & C. Brown, 2006. Uptake and elimination of chlorpyrifos and pentachlorophenol into the freshwater amphipod Gammarus pulex. Archives of Environmental Contamination and Toxicology 51: 542–548.CrossRefPubMedGoogle Scholar
  5. Aydin, M.E., S. Ozcan & F. Beduk, 2011. Acute toxicity of Organophosphorus pesticides and their degradation by-products to Daphnia magna, Lepidium sativum and Vibrio fischeri www.intechopen.com.
  6. Barahona-Gomariz, M. V., F. Sanz-Barrera & S. Sanchez-Forton, 1994. Acute toxicity of organic solvents on Artemia salina. Bullettin of Environmental Contamination and Toxicology 52: 766–771.Google Scholar
  7. Barron, M. G. & K. B. Woodburn, 1995. Ecotoxicology of chlorpyrifos. Reviews of Environmental Contamination and Toxicology 144: 1–93.CrossRefPubMedGoogle Scholar
  8. Bellas, J., R. Beiras, J. C. MarinoBalsa & N. Fernandez, 2005. Toxicity of organic compounds to marine invertebrate embryos and larvae: A comparison between the sea urchin embryogenesis bioassay and alternative test species. Ecotoxicology 14: 337–353.CrossRefPubMedGoogle Scholar
  9. Calabrese, E. J. & L. A. Baldwin, 2001. Hormesis: u-shaped dose responses and their centrality in toxicology. Trends in Pharmacological Sciences 22: 285–291.CrossRefPubMedGoogle Scholar
  10. Calabrese, E. J. & R. Blain, 2005. The occurrence of hormetic responses in toxicological literature, the hormesis database: an overview. Toxicology Application Pharmacology 202: 289–301.CrossRefGoogle Scholar
  11. Cardona, L., A. I. Ivarez de Quevedo, A. Borrell & A. Aguilar, 2012. Massive consumption of gelatinous plankton by Mediterranean apex predators. PLoSONE 7(3): 31329.CrossRefGoogle Scholar
  12. Chapman, P. M., 2001. The implications of hormesis to ecotoxicology and ecological risk assessment. Human & Experimental Toxicology 20: 499.CrossRefGoogle Scholar
  13. Charoy, C. P. & C. R. Janssen, 1999. The swimming behaviour of Brachionus calyciflorus (rotifer) under toxic stress. II. Comparative sensitivity of various behavioural criteria. Chemosphere 38: 3247–3260.CrossRefGoogle Scholar
  14. Costantini, D., N. B. Metcalfe & P. Monaghan, 2010. Ecological processes in a hormetic framework. Ecology Letters 13: 1435–1447.CrossRefPubMedGoogle Scholar
  15. Daly, M., M. Brugler, P. Cartwright, A. Collins, M. N. Dowson, D. G. Fautin, S. C. France, C. S. Mcfadden, D. M. Opresk, E. Rodriguez, S. L. Romano & J. L. Stakeet, 2007. The phylum Cnidaria: a review of phylogenetic patterns and diversity 300 years after Linneus. Zootaxa 1668: 127–182.Google Scholar
  16. Demetrio, P. M., D. Gustavo, D. B. Rossini, C. A. Bonetto & A. E. Ronco, 2012. Effects of pesticide formulations and active ingredients on the Coelenterate Hydra attenuata (Pallas, 1766). Bullettin of Environmental Contaminant and Toxicology 88: 15–19.CrossRefGoogle Scholar
  17. Directives 2000/60/EC and 2008/105/EC as regards priority substances in the field of water policy.Google Scholar
  18. Directive 2013/39/EU of the European Parliament and of the council of 12 August 2013 amending.Google Scholar
  19. Downs, C. A., E. J. Fauth, V. D. Downs & G. K. Ostrander, 2010. In vitro cell-toxicity screening as an alternative animal model for coral toxicology: effects of heat stress, sulfide, rotenone, cyanide, and cuprous oxide on cell viability and mitochondrial function. Ecotoxicology 19: 171–184.CrossRefPubMedGoogle Scholar
  20. Eamkamon, T., S. Klinbunga, K. Thirakhupt, P. Menasveta & N. Puanglarp, 2012. Acute toxicity and neurotoxicity of chlorpyrifos in Black Tiger Shrimp, Penaeus monodon. EnviromentAsia 5(1): 26–31.Google Scholar
  21. Faimali, M., F. Garaventa, V. Piazza, F. Magillo, G. Greco, C. Corrà, E. Giacco, L. Gallus & C. Falugi, 2006. Swimming speed alteration of larvae of Balanus amphitrite as behavioural end-point for laboratory toxicological bioassays. Marine Biology 149: 87–96.CrossRefGoogle Scholar
  22. Faimali, M., F. Garaventa, V. Piazza, E. Costa, G. Greco, V. Mazzola, M. Beltrandi, E. Bongiovanni, S. Lavorano & G. Gnone, 2014. Ephyra Jellyfish as a new model for ecotoxicological bioassays. Marine Environmental Research 93: 93–101.CrossRefPubMedGoogle Scholar
  23. Falugi, C., C. Morri, J. Bouillon & F. Boero, 1994. Localizatione of some neurotransmitters during development in hydroidomedusae. Tissue and Cell 26: 523–538.CrossRefPubMedGoogle Scholar
  24. Finney, D. J., 1978. Statistical Method in Biological Assay, 3rd ed. Charles Griffin & Co. Ltd, London.Google Scholar
  25. Galgani, F. & G. Bocquene, 1990. In vitro inhibition of acetylcholinesterase from four marine species by organophosphates and carbamates. Bullettin of Environmental Contaminant and Toxicology 45: 243–249.CrossRefGoogle Scholar
  26. Garaventa, F., C. Gambardella, A. Di Fino, M. Pittore & M. Faimali, 2010. Swimming Speed alteration of Artemia sp. and Brachionus plicatilis as a sub-lethal behavioural end-point for ecotoxicological surveys. Ecotoxicology 19: 512–519.CrossRefPubMedGoogle Scholar
  27. Getzin, L. W., 1985. Factors influencing the persistence and effectiveness of chlorpyrifos in soil. Journal Enconomic Entomology 78: 412–418.CrossRefGoogle Scholar
  28. Gerstl, Z., 1990. Estimation of organic chemical sorption by soils. Journal of Contaminant Hydrology 6: 357–375.CrossRefGoogle Scholar
  29. Greco, G., C. Corrà, F. Garaventa, E. Chelossi & M. Faimali, 2006. Standardization of laboratory bioassays with Balanus amphitrite larvae for preliminary oil dispersants toxicological characterization. Chemistry and Ecology 22(1): 163–172.CrossRefGoogle Scholar
  30. Guzzella, L., A. Gronda & L. Colombo, 1997. Acute toxicity of organophosphorus insecticides to marine invertebrates. Bullettin Environmental Contamination and Toxicology 59: 313–320.CrossRefGoogle Scholar
  31. Holdaway, S., N. Davidson, J. Dignan, R. Hammersley, J. Hine & P. Marsh, 2001. New strategies to address youth offending: the national evaluation of the pilot youth offending teams. Research, Development and Statistics Directorate Paper No. 69. Home Office, London.Google Scholar
  32. Holst, S., 2012. Morphology and development of benthic and pelagic life stages of North Sea jellyfish (Scyphozoa, Cnidaria) with special emphasis on the identification of ephyra stages. Marine Biology 159: 2707–2722.CrossRefGoogle Scholar
  33. Huang, X., Y. Zeng, B. Hvan & S. Li, 2013. Effect of Alexandrium catenella (Dinophyta) concentration on the behavior and growth of Aurelia sp. Ephyra. Journal Plankton Research 0: 1–5.Google Scholar
  34. Karntanut, W. & D. Pascoe, 2000. The toxicity of copper, cadmium and zinc to four different Hydra (Cnidaria: hydrozoa). Chemosphere 47: 1059–1064.CrossRefGoogle Scholar
  35. Key, P. B., S. E. Simonik, N. Kish, K. W. Chung & M. H. Fulton, 2013. Differences in response of two model estuarine crustaceans after lethal and sublethal exposures to chlorpyrifos. Journal of Environmental Science and Health, Part B: Pesticides, Food Contaminants, and Agricultural Wastes 48(11): 967–973.CrossRefGoogle Scholar
  36. Kramp, P. L., 1961. Synopsis of the medusae of the world. Journal of Marine Biology 40: 1–469.Google Scholar
  37. Kusui, T. & C. Blaise, 1999. Ecotoxicological assessment of Japanese industrial effluents using a battery of small-scale toxicity tests. Impact assessment of hazardous aquatic contaminants: concepts and approaches. Lewis Publishers, Boca Raton, FL: 161–181.Google Scholar
  38. Logan, T.J., J.M. Davidson, J.L. Boker & M.R. Overcosh, 1987. Effects of conservation tillage on grand quality-nitrates and pesticides. Lewis Publishers, Boca Raton, 192: pp.Google Scholar
  39. Lucas, C. H., 2001. Reproduction and life history strategies of the common jellyfish, Aurelia aurita, in relation to its ambient environment. Hydrobiologia 451: 229–246.CrossRefGoogle Scholar
  40. Matanoski, J. C., R. R. Hood, R. L. Owens & J. E. Purcell, 2004. Patterns in swimming by a scyphomedusa: a novel approach to quantifying behavior in individuals. Marine Biology 145: 303–313.CrossRefGoogle Scholar
  41. McHenry, M. J. & J. Jason, 2003. The ontogenetic scaling of hydrodynamics and swimming performance in jellyfish (Aurelia aurita). The Journal of Experimental Biology 206: 4125–4137.CrossRefPubMedGoogle Scholar
  42. Mesarič, T., K. Sepčič, V. Piazza, C. Gambardella, F. Garaventa, D. Drobne & M. Faimali, 2013. Effects of nano carbon black and single-layer graphene oxide on settlement, survival and swimming behaviour of Amphibalanus amphitrite larvae. Chemistry and Ecology 29(7): 643–652.CrossRefGoogle Scholar
  43. Mills, C. E., 1995. Medusae, siphonophores, and ctenophores as planktivorous predators in changing global ecosystems. ICES Journal of Marine Science 52: 575–581.CrossRefGoogle Scholar
  44. Mills, C. E., 2001. Jellyfish blooms: are populations increasing globally in response to changing ocean conditions? Hydrobiologia 451: 55–68.CrossRefGoogle Scholar
  45. Mills, C.E., 2011. Phylum Ctenophora: List of all valid species names. University of Washington. (http://faculty.washington.edu/cemills/Ctenolist.html).
  46. Nawroth, J.C., K. E. Feitl, S. P. Colin, J. H. Costello & J. O. Dabiri, 2014. Phenotypic plasticity in.juvenile jellyfish medusa facilitates effective animal fluid interaction. Biology Letters. doi: 10.1098/rsbl.2010.0068 Published online.
  47. Palma, P., V. L. Palma, R. M. Fernandes, A. M. V. M. Soares & I. R. Barbosa, 2008. Acute toxicity of atrazine, endosulfan sulphate and chlorpyrifos to Vibrio fischeri, Thamnocephalus platyurus and Daphnia magna, relative to their concentrations in surface waters from the alentejo region of Portugal. Bullettin Environmental Contamination and Toxicology 81: 485–489.CrossRefGoogle Scholar
  48. Pascoe, D., W. Karntanut & C. T. Müller, 2003. Do pharmaceuticals affect freshwater invertebrates? A study with the cnidarian Hydra vulgaris. Chemosphere 51: 21–528.CrossRefGoogle Scholar
  49. Pesando, D., P. Huitorelb, V. Dolcinia, C. Angelinic, P. Guidetti & C. Falugi, 2003. Biological targets of neurotoxic pesticides analysed by alteration of developmental events in the Mediterranean sea urchin, Paracentrotus lividus. Marine Environmental Research 55: 39–57.CrossRefPubMedGoogle Scholar
  50. Pierce, J., 2009. Prediction, location, collection and transport of jellyfish (Cnidaria) and their polyps. Journal of Zoology and Biology 28: 163–176.CrossRefGoogle Scholar
  51. Pitt, K. A., K. Koop & D. Rissik, 2005. Contrasting contributions to inorganic nutrient recycling by the co-occurring jellyfishes, Catostylus mosaicus and Phyllorhiza punctuate (Scyphozoa, Rhizostomeae). Journal of Experimental Marine Biology and Ecology 315: 71–86.CrossRefGoogle Scholar
  52. Pollino, C. A. & D. A. Holdway, 1999. Potential of two Hydra species as standard toxicity test animals. Ecotoxicology and Environmental Safety 43: 309–316.CrossRefPubMedGoogle Scholar
  53. Pope, C. N., 1999. Organophosphorus pesticides: do they all have the same mechanism of toxicity? Journal of Toxicology and Environmental Health, Part B: critical reviews 2(2): 161–181.CrossRefGoogle Scholar
  54. Purcell, J. E., 1997. Pelagic cnidarians and ctenophores as predators: selective predation, feeding rates and effects on prey populations. Annales Institute Oceanographique Paris 73: 125–137.Google Scholar
  55. Purcell, J.E., W.M. Graham & H.J. Dumont, 2001. Jellyfish blooms: ecological and societal importance. Developments in hydrobiology 155. Kluwer Academic, Dordrecht.Google Scholar
  56. Purcell, J. E., S. Uye & W. Lo, 2007. Anthropogenic causes of jellyfish blooms and their direct consequences for humans: a review. Marine Ecology Program Service 350: 153–174.CrossRefGoogle Scholar
  57. Rakow, K. C. & W. M. Graham, 2006. Orientation and swimming mechanics by the scyphomedusa Aurelia sp. in shear flow. Limnology and Oceanography 51: 1097–1106.CrossRefGoogle Scholar
  58. Rao, J. V., P. Kavitha, N. M. Jakka, V. Sridhar & P. K. Usman, 2007. Toxicity of organophosphates on morphology and locomotor behaviour in brine shrimp, Artemia salina. Archives of Environmental Contamination and Toxicology 53: 227–232.CrossRefGoogle Scholar
  59. Riisgard, H. U., C. V. Madsen, C. Barth-Jensen & J. E. Purcell, 2011. Population dynamics and zooplankton-predation impact of the indigenous scyphozoan Aurelia aurita and the invasive ctenophore Mnemiopsis leidyi in Limfjorden (Denmark). Aquatic Invasion 7: 147–162.CrossRefGoogle Scholar
  60. Russell, F.S., 1970. The Medusae of the British Isles. II. Pelagic Scyphozoa with a supplement to the first volume on Hydromedusae. Cambridge University Press, London, 284: pp.Google Scholar
  61. Satterlie, R. A., 2002. Neuronal control of swimming in jellyfish: a comparative story. Canadian Journal of Zoology 80: 1654–1669.CrossRefGoogle Scholar
  62. Serrano, R., F. Hermindez, J. B. Pefia, V. Dosda & J. Canales, 1995. Toxicity and bioconcentration of selected organophosphorus pesticides in Mytilus galloprovincialis and Venus gallina. Archives of Environmental Contamintion and Toxicology 29: 284–290.CrossRefGoogle Scholar
  63. Smulders, C. J. G. M., R. G. D. M. Van Kleef, C. Aart de Groot, C. Gotti & H. P. M. Vijverberg, 2004. A noncompetitive, sequential mechanism for inhibition of Rat a4b2 neuronal nicotinic acetylcholine receptors by carbamate pesticides. Toxicological Sciences 82: 219–227.CrossRefPubMedGoogle Scholar
  64. Takahashi, T. & N. Hamaue, 2010. Molecular characterization of Hydra acetylcholinesterase and its catalytic activity. Federation of European Biochemical Societies 584: 511–516.CrossRefGoogle Scholar
  65. Turk, V., D. Lucĭc, V. Flander-Putrle & A. Malej, 2008. Feeding of Aurelia sp. (Scyphozoa) and links to the microbial food web. Marine Ecology 29: 495–505.CrossRefGoogle Scholar
  66. Underwood, A. J., 1997. Experiments in Ecology: Their Logical Design and Interpretation Using Analysis of Variance, 524, Vol. 524. University of Sydney, Sydney.Google Scholar
  67. Van der Oost, R., J. Beyer & N. P. E. Vermulen, 2003. Fish bioaccumulation and biomarker in environmental risk assessment: a review. Environmental Toxicology and Pharmacology 13: 57–149.CrossRefPubMedGoogle Scholar
  68. Varò, I., J. C. Navarro, F. Amat & L. Guilhermino, 2002. Characterisation of cholinesterases and evaluation of the inhibitory potential of chlorpyrifos and dichlorvos to Artemia salina and Artemia parthenogenetica. Chemosphere 48: 563–569.CrossRefPubMedGoogle Scholar
  69. Watanabe, H., T. Fujisawa & T. W. Holstein, 2009. Cnidarians and the evolutionary origin of the nervous system. Development Growth and Differentiation 51: 167–183.CrossRefGoogle Scholar
  70. Wilby, O. K. & J. M. Tesh, 1990. The Hydra assay as an early screen for teratogenic potential. Toxicology in Vitro 4: 582–583.CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Elisa Costa
    • 1
    • 2
  • Chiara Gambardella
    • 2
  • Veronica Piazza
    • 2
  • Giuliano Greco
    • 2
  • Silvia Lavorano
    • 3
  • Martina Beltrandi
    • 3
  • Elisabetta Bongiovanni
    • 3
  • Guido Gnone
    • 3
  • Marco Faimali
    • 2
  • Francesca Garaventa
    • 1
    • 2
  1. 1.National Research Council - Institute of Marine Sciences (CNR - ISMAR)VenetiaItaly
  2. 2.National Research Council - Institute of Marine Sciences (CNR - ISMAR)GenoaItaly
  3. 3.Costa Edutainment S.p.A., Acquario di GenovaGenoaItaly

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