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The challenging role of life cycle monitoring: evidence from bisphenol A on the copepod Tigriopus japonicus

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Abstract

We used the marine model copepod taxon T. japonicus Mori, 1938 for a first short sublethal life cycle assay of the endocrine-disrupting chemical bisphenol A (BphA) where we studied life cycle and reproductive success. Individual copepodid-I-stages were reared in 96-well microplates to adulthood in as short as 6 days in only 200 μl of 0.1 mg bisphenol (BphA/L) or seawater solution as a control (CON). Males and females were then mated in one well and checked daily for the following endpoints: postmating days to female brood sac extrusion, days from brood sac extrusion to naupliar hatching, first clutch brood size, hatching success, and reproductive success. Mean naupliar hatching times ranged from 1.3 days for CON-reared mating pairs to 2.7 days for BphA-reared mating pairs; mean brood size was significantly lower for CON females mated with BphA males than for all other mating combinations; reproductive success of CON females mated with BphA males and BphA females mated with BphA males showed significant differences between females and males. In conclusion, T. japonicus complete life cycle exposures to BphA at an environmentally realistic concentration resulted generally in reproductive depression with effect values depending on the exposure history of the different gender.

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References

  • Coull, B. C. & G. T. Chandler, 1992. Pollution and meiofauna: field, laboratory, and mesocosm studies. Oceanography and Marine Biology – An Annual Review 30: 191–271.

    Google Scholar 

  • Dahms, H.-U. & C. Hellio, 2009. Chapter 12: Laboratory based assays for antifouling compounds. In Yebra, S. & C. Hellio (eds), Advances in antifouling coatings and technologies. Woodhead Publishers, Oxford: 275–307.

    Chapter  Google Scholar 

  • Dahms, H.-U., T. Jin & P.-Y. Qian, 2004. Adrenoceptor compounds prevent the settlement of marine invertebrate larvae. Biofouling 20: 313–321.

    Article  CAS  PubMed  Google Scholar 

  • Dahms, H.-U., Y. Xu & C. Pfeiffer, 2006a. Antifouling substances from cyanobacteria. Biofouling 22: 317–327.

    Article  CAS  PubMed  Google Scholar 

  • Dahms, H.-U., T. Harder & P.-Y. Qian, 2006b. Selective attraction and reproductive performance of a harpacticoid copepod in a response to biofilms. Journal of Experimental Marine Biology and Ecology 341: 228–238.

    Article  Google Scholar 

  • Dahms, H.-U., Q.-F. Gao & J.-S. Hwang, 2007. Optimized maintenance and larval production of the bryozoan Bugula neritina (Bryozoa) in the laboratory. Aquaculture 265: 169–175.

    Article  Google Scholar 

  • DiPinto, L. M., B. C. Coull & G. T. Chandler, 1993. Lethal and sublethal effects of the sediment associate PCB aroclor 1254 on a meiobenthic copepod. Environmental Toxicology and Chemistry 12: 1909–1918.

    Article  CAS  Google Scholar 

  • Flint, S., T. Markle, S. Thompson & E. Wallace, 2012. Bisphenol A exposure, effects, and policy: a wildlife perspective. Journal of Environmental Management 104: 19–34.

    Article  CAS  PubMed  Google Scholar 

  • Forbes, V. E., A. Palmqvist & L. Bach, 2006. The use and misuse of biomarkers in ecotoxicology. Environmental Toxicology and Chemistry 25: 272–280.

    Article  CAS  PubMed  Google Scholar 

  • Hicks, G. R. F. & B. C. Coull, 1983. The ecology of marine meiobenthic harpacticoid copepods. Oceanography and Marine Biology – An Annual Review 21: 67–175.

    Google Scholar 

  • Hu, X.-L., J.-F. Peng, J.-F. Liu, G.-B. Jiang & J. Å. Jönsson, 2006. Evaluating the impacts of some environmentally relevant factors on the availability of bisphenol A with negligible-depletion of SPME. Chemosphere 65: 1935–1941.

    Article  CAS  PubMed  Google Scholar 

  • Jung, S.-O., Y.-M. Lee, T.-J. Park, H. G. Park, A. Hagiwara, K. M. Y. Leung, H.-U. Dahms, W. Lee & J.-S. Lee, 2006. The complete mitochondrial genome of the intertidal copepod Tigriopus sp. (Copepoda, Harpacticidae) from Korea and phylogenetic considerations. Journal of Experimental Marine Biology and Ecology 333: 251–262.

    Article  CAS  Google Scholar 

  • Ki, J.-S., K.-W. Lee, H. G. Park, S. Chullasorn, H.-U. Dahms & J.-S. Lee, 2009. Phylogeography of the copepod Tigriopus japonicus along the Northwest Pacific rim. Journal of Plankton Research 31: 209–221.

    Article  CAS  Google Scholar 

  • Kwok, K. W. H. & K. M. Y. Leung, 2005. Toxicity of antifouling biocides to the intertidal harpacticoid copepod Tigriopus japonicus (Crustacea, Copepoda): effects of temperature and salinity. Marine Pollution Bulletin 51: 830–837.

    Article  CAS  PubMed  Google Scholar 

  • Kwok, K. W. H., K. M. Y. Leung, V. W. W. Bao & J.-S. Lee, 2008. Copper toxicity in the marine copepod Tigropus japonicus: low variability and high reproducibility of repeated acute and life-cycle tests. Marin Pollution Bulletin 57: 632–636.

    Article  CAS  Google Scholar 

  • Lee, Y.-M., I.-C. Kim, S.-O. Jung & J.-S. Lee, 2005. Analysis of 686 expressed sequence tags (ESTs) from the intertidal harpacticoid copepod Tigriopus japonicus (Crustacea, Copepoda). Marine Pollution Bulletin 51: 757–768.

    Article  CAS  PubMed  Google Scholar 

  • Lee, Y.-M., J. S. Seo, I.-C. Kim, Y.-D. Yoon & J.-S. Lee, 2006. Endocrine disrupting chemicals (bisphenol A, 4-nonylphenol, 4-tert-octylphenol) modulate expression of two distinct cytochrome P450 aromatase genes differently in gender types of the hermaphroditic fish Rivulus marmoratus. Biochemical and Biophysical Research Communications 345: 894–903.

    Article  CAS  PubMed  Google Scholar 

  • Lee, Y. M., M. J. Seong, J. W. Lee, Y. K. Lee, T. M. Kim, S. Y. Nam, D. J. Kim, Y. W. Yun, T. S. Kim, S. Y. Han & J. T. Hong, 2007. Estrogen receptor independent neurotoxic mechanism of bisphenol A, an environmental estrogen. Journal of Veterinary Science 8: 27–38.

    Article  PubMed  PubMed Central  Google Scholar 

  • Marcial, H. S., A. Hagiwara & T. W. Snell, 2003. Estrogenic compounds affect development of the harpacticoid copepod Tigriopus japonicus. Environmental Toxicology and Chemistry 22: 3025–3030.

    Article  CAS  PubMed  Google Scholar 

  • McManus, G. B., K. D. Wyman, W. T. Peterson & C. F. Wurster, 1983. Factors affecting the elimination of PCBs in the marine copepod Acartia tonsa. Estuarine, Coastal and Shelf Science 17: 421–430.

    Article  CAS  Google Scholar 

  • NIER, 2005. The report for the 6th annual survey of endocrine-disrupting chemicals in Korea. The Ministry of Environment, Seoul, Korea. http://www.nier.go.kr/nierdepart/eds/03status/status01.html.

  • Oberdörster, E., M. Brouwer, T. Hoexum-Brouwer, S. Manning & J. A. McLachlan, 2000. Long-term pyrene exposure of grass shrimp, Palaemonetes pugio, affects molting and reproduction of exposed males and offspring exposed females. Environmental Health Perspectives 108: 641–646.

    Article  PubMed  PubMed Central  Google Scholar 

  • Oehlmann, J., U. Schulte-Oehlmann, W. Kloas, O. Jagnytsch, I. Lutz, K. O. Kusk, L. Wollenberger, E. M. Santos, G. C. Paull, K. J. Van Look & C. R. Tyler, 2009. A critical analysis of the biological impacts of plasticizers on wildlife. Philosophical Transactions of the Royal Society B 364: 2047–2062.

    Article  CAS  Google Scholar 

  • Okada, H., T. Tokunaga, X. Liu, S. Takayanagi, A. Matsushima & Y. Shimohigashi, 2008. Direct evidence revealing structural elements essential for the high binding ability of bisphenol A to human estrogen-related receptor-gamma. Environmental Health Perspectives 116: 32–38.

    Article  CAS  PubMed  Google Scholar 

  • Raisuddin, S., K. W. H. Kwok, K. M. Y. Leung, D. Schlenk & J.-S. Lee, 2007. The copepod Tigriopus: a promising marine model organism for ecotoxicology and environmental genomics. Aquatic Toxicology 83: 161–173.

    Article  CAS  PubMed  Google Scholar 

  • Seo, J. S., T.-J. Park, Y.-M. Lee, H. G. Park, Y.-D. Yoon & J.-S. Lee, 2006a. Small heat shock protein 20 gene (Hsp20) of the intertidal copepod Tigriopus japonicus as a possible biomarker for exposure to endocrine disruptors. Bulletin of Environmental Contamination and Toxicology 76: 566–572.

    Article  CAS  PubMed  Google Scholar 

  • Seo, J. S., Y.-M. Lee, H. G. Park & J.-S. Lee, 2006b. The intertidal copepod Tigriopus japonicus small heat shock protein 20 gene (Hsp20) enhances thermotolerance of transformed Escherichia coli. Biochemical and Biophysical Research Communications 340: 901–908.

    Article  CAS  PubMed  Google Scholar 

  • Seo, J. S., Y.-M. Lee, S.-O. Jung, I.-C. Kim, Y.-D. Yoon & J.-S. Lee, 2006c. Nonylphenol modulates expression of androgen receptor and estrogen receptor genes differently in gender types of the hermaphroditic fish Rivulus marmoratus. Biochemical and Biophysical Research Communications 346: 213–223.

    Article  CAS  PubMed  Google Scholar 

  • U.S. Environmental Protection Agency, 1996. New pesticide fact sheet. EPA 737-F-96-005. Office of Pesticide Programs, Washington DC.

    Google Scholar 

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Acknowledgements

This research was supported by “Long-Term Change of Structure and Function in Marine Ecosystems of Korea” and “Development of Korea Operational Oceanographic System (KOOS)” funded by the Ministry of Oceans and Fisheries, Korea.” H.U.D further acknowledges the funding by MOST 104-2621-M-037-001 to T.H. SHIH. This work was partly supported by the grant from Research Center for Environmental Medicine, Kaohsiung Medical University (KMU-TP105A27) to H.U.D. We also thank the Asia-Pacific Ocean Research Center of the Department of Oceanography [No. 76211194] in the frame of KMU/NSYSU cooperation to H.U.D. and K.S. We are grateful for useful comments on an earlier draft of the MS by Profs. J.S. Lee and J.S. Rhee.

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Correspondence to Jiang-Shiou Hwang.

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Handling editor: Juan Carlos Molinero

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Dahms, HU., Lee, S.H., Huang, DJ. et al. The challenging role of life cycle monitoring: evidence from bisphenol A on the copepod Tigriopus japonicus . Hydrobiologia 784, 81–91 (2017). https://doi.org/10.1007/s10750-016-2859-7

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  • DOI: https://doi.org/10.1007/s10750-016-2859-7

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