|
|
Cite this paper: |
|
|
WU Qingyang, WANG Shuqi, CHEN Xiaopeng, LI Ping. Reproductive toxicity assessment of benzo[a]pyrene in the marine polychaete Perinereis nuntia[J]. Journal of Oceanology and Limnology, 2017, 35(4): 867-873 |
|
|
|
|
|
|
|
Reproductive toxicity assessment of benzo[a]pyrene in the marine polychaete Perinereis nuntia |
|
| WU Qingyang1, WANG Shuqi1, CHEN Xiaopeng2, LI Ping1 |
|
1 Guangdong Provincial Key Laboratory of Marine Biology, Shantou University, Shantou 515063, China;
2 Administration of Ocean and Fisheries of Shantou, Shantou 515000, China |
|
| Abstract: |
| Benzo[a]pyrene (B[a]P) is an increasingly present marine environmental pollutant, yet our understanding of the long-term consequences of reproductive toxicity in marine benthic polychaetes remains limited. To test the reproductive toxicity of B[a]P on polychaetes, Perinereis nuntia was exposed to B[a]P-contaminated artificial seawater and sexual maturation, the sex ratio, number of eggs spawned, fertilization and hatching rated, as well as vitellogenin (VTG) mRNA expression levels were analyzed. A low concentration of B[a]P (2.5 μg/L) had no effects on the rate of sexual maturation, spawning, or fertilization but significantly increased the sex ratio (female:male) from 1.6±0.15:1 to 2.3±0.18:1, inhibited hatching rate by 27%, and significantly increased VTG mRNA expression level by 3.7-fold following a 60-day exposure, compared with those in the solvent controls. A higher concentration of B[a]P (25 μg/L) caused more serious effects; sexual maturation, fertilization success, and hatching decreased by 31%, 17% and 46%, respectively, and the sex ratio (female:male) and VTG mRNA gene expression level increased by 54% and 7.1-fold, respectively. These results demonstrate that sublethal concentrations of B[a]P negatively affect reproductive performance of the sandworm P. nuntia. |
|
| Key words:
Perinereis nuntia|benzo[a]pyrene|reproductive biology|vitellogenin
|
|
| Received: 2016-01-26 Revised: 2016-04-06 |
|
|
|
|
References:
Banni M, Bouraoui Z, Clerandeau C, Narbonne J F, Boussetta H. 2009. Mixture toxicity assessment of cadmium and benzo[a]pyrene in the sea worm Hediste diversicolor. Chemosphere, 77(7):902-906.
Banni M, Negri A, Dagnino A, Jebali J, Ameur S, Boussetta H. 2010. Acute effects of benzo[a]pyrene on digestive gland enzymatic biomarkers and DNA damage on mussel Mytilus galloprovincialis. Ecotoxicology and Environmental Safety, 73(5):842-848.
Bode M, Marshall D J. 2007. The quick and the dead? Sperm competition and sexual conflict in sea. Evolution, 61(11):2 693-2 700.
Bouraoui Z, Banni M, Ghedira J, Clerandeau C, Narbonne J F, Boussetta H. 2009. Evaluation of enzymatic biomarkers and lipoperoxidation level in Hediste diversicolor exposed to copper and benzo[a]pyrene. Ecotoxicology and Environmental Safety, 72(7):1 893-1 898.
Catalano B, Moltedo G, Martuccio G, Gastaldi L, VirnoLamberti C, Lauria A, Ausili A. 2012. Can Hediste diversicolor (Nereidae, Polychaete) be considered a good candidate in evaluating PAH contamination? A multimarker approach. Chemosphere, 86(9):875-882.
Denslow N D, Chow M C, Kroll K J, Green L. 1999. Vitellogenin as a biomarker of exposure for estrogen or estrogen mimics. Ecotoxicology, 8(5):385-398.
Du R B. 2004. The study on ecological condition and reproductive biology of adult Perinereis nuntia Savigny under artificial culture condition. Ocean University of China, Qingdao, China, p.18-38. (in Chinese)
Fry D M, Toone C K. 1981. DDT-induced feminization of gull embryos. Science, 231(4510):922-924.
García-Alonso J, Hoeger U, Rebscher N. 2006. Regulation of vitellogenesis in Nereis virens (Annelida:Polychaeta):Effect of estradiol-17β on eleocytes. Comparative Biochemistry and Physiology Part A:Molecular & Integrative Physiology, 143(1):55-61.
Gibson R, Smith M D, Spary C J, Tyler C R, Hill E M. 2005. Mixtures of estrogenic contaminants in bile of fish exposed to wastewater treatment works effluents. Environmental Science & Technology, 39(8):2 461-2 471.
Guilette L J, Crain D A. 1996. Endocrine-disrupting contaminants and reproductive abnormalities in reptiles. Communications Toxicology, 5(4):381-399.
Hardege J D, Bartels-Hardege H D. 1995. Spawning behaviour and development of Perinereis nuntia var brevicirrus(Annelida:Polychaeta). Invertebrate Biology, 114(1):39-45.
Jeong W G, Cho S M. 2005. The effects of polycyclic aromatic hydrocarbon exposure on the fertilization and larval development of the Pacific oyster, Crassostrea gigas. Journal of Shellfish Research, 24(1):209-213.
Jobling S, Nolan M, Tyler C R, Brighty G, Sumpter J P. 1998. Widespread sexual disruption in wild fish. Environmental Science & Technology, 32(17):2 498-2 506.
Kanaly R A, Harayama S. 2000. Biodegradation of highmolecular-weight polycyclic aromatic hydrocarbons by bacteria. Journal of Bacteriology, 182(8):2 059-2 067.
Keay J, Thornton J W. 2009. Hormone-activated estrogen receptors in annelid invertebrates:implications for evolution and endocrine disruption. Endocrinology, 150(4):1 731-1 738.
Lee B G, Griscom S B, Lee J S, Choi H J, Koh C H, Luoma S N, Fisher N S. 2000. Influences of dietary uptake and reactive sulfides on metal bioavailability from aquatic sediments. Science, 287(5451):282-284.
Lin J H, Zheng F W. 2007. Preliminary study on ecology of benthic polychaeta in Quanzhou Bay and its adjacent waters. Journal of Oceanography Taiwan Strait, 26(2):281-288. (in Chinese with English abstract)
Livingstone D R. 1994. Recent developments in marine invertebrate organic xenobiotic metabolism. Toxicology and Ecotoxicology News, 1(3):88-94.
Lopes S, Jurisicova A, Sun J G, Casper R F. 1998. Reactive oxygen species:potential cause for DNA fragmentation in human spermatozoa. Human Reproduction, 13(4):896-900.
Matozzo V, Gagné F, Marin M G, Ricciardi F, Blaise C. 2008. Vitellogenin as a biomarker of exposure to estrogenic compounds in aquatic invertebrates:a review. Environment International, 34(4):531-545.
McElroy A, Leitch K, Fay A. 2000. A survey of in vivo benzo[α]pyrene metabolism in small benthic marine invertebrates. Marine Environmental Research, 50(1-5):33-38.
Mearns A J, Reish D J, Oshida P S, Ginn T, Rempel-Hester M A, Arthur C, Rutherford N. 2013. Effects of pollution on marine organisms. Water Environment Research, 85(10):1 828-1 933.
Monteiro P R R, Reis-Henriques M A, Coimbra J. 2000. Plasma steroid levels in female flounder (Platichthys flesus) after chronic dietary exposure to single polycyclic aromatic hydrocarbons. Marine Environmental Research, 49(5):453-467.
Munkittrick K R, Portt C B, Van Der Kraak G J, Smith I R, Rokosh D A. 1991. Impact of bleached kraft mill effluent on population characteristics, liver MFO activity, and serum steroid levels of a Lake Superior white sucker(Catostomus commersoni) Population. Canadian Journal of Fisheries and Aquatic Sciences, 48(8):1 371-1 380.
Oakes K D, Hewitt L M, McMaster M E, Wood C, Munkittrick K R, Van Der Kraak G J. 2005. Oxidative stress and sex steroid levels in fish following short-term exposure to pulp-mill effluents. Journal of Toxicology and Environmental Health, Part A, 68(4):267-286.
Rose J, Holbech H, Lindholst C, Nørum U, Povlsen A, Korsgaard B, Bjerregaard P. 2002. Vitellogenin induction by 17β-estradiol and 17α-ethinylestradiol in male zebrafish (Danio rerio). Comparative Biochemistry and Physiology Part C:Toxicology & Pharmacology, 131(4):531-539.
Rurangwa E, Biegniewska A, Slominska E, Skorkowski E F, Ollevier F. 2002. Effect of tributyltin on adenylate content and enzyme activities of teleost sperm:a biochemical approach to study the mechanisms of toxicant reduced spermatozoa motility. Comparative Biochemistry and Physiology Part C:Toxicology & Pharmacology, 131(3):335-344.
Rust A J, Burgess R M, Brownawell B J, McElroy A E. 2004. Relationship between metabolism and bioaccumulation of benzo[α]pyrene in benthic invertebrates. Environmental Toxicology and Chemistry, 23(11):2 587-2 593.
Sternberg R M, Hotchkiss A K, LeBlanc G A. 2008. The contribution of steroidal androgens and estrogens to reproductive maturation of the eastern mud snail Ilyanassa obsoleta. General and Comparative Endocrinology, 156(1):15-26.
Sumpter J P, Jobling S. 1995. Vitellogenesis as a biomarker for estrogenic contamination of the aquatic environment. Environmental Health Perspectives, 103(Supplement 7):173-178.
Tian S M, Pan L Q, Sun X H. 2013. An investigation of endocrine disrupting effects and toxic mechanisms modulated by benzo[a]pyrene in female scallop Chlamys farreri. Aquatic Toxicology, 144-145:162-171.
Van den Belt K, Verheyen R, Witters H. 2003. Comparison of vitellogenin responses in zebrafish and rainbow trout following exposure to environmental estrogens. Ecotoxicology and Environmental Safety, 56(2):271-281.
Wang C D, Croll R P. 2004. Effects of sex steroids on gonadal development and gender determination in the sea scallop, Placopecten magellanicus. Aquaculture, 238(1-4):483-498.
Wen J M, Pan L Q. 2015. Short-term exposure to benzo[a] pyrene disrupts reproductive endocrine status in the swimming crab Portunus trituberculatus. Comparative Biochemistry and Physiology Part C:Toxicology & Pharmacology, 174-175:13-20.
Weston D P. 1990. Hydrocarbon bioaccumulation from contaminated sediment by the deposit-feeding polychaete Abarenicola pacifica. Marine Biology, 107(1):159-169.
Yund P O. 2000. How severe is sperm limitation in natural populations of marine free-spawners? Trends in Ecology & Evolution, 15(1):10-13.
Zar J H. 1999. Biostatistical Analysis. 5th edn. Prentice Hall Inc., New Jersey, p.189-248.
Zheng J S, Richardson B J, Shouming O, Zheng J H. 2004. Distribution and sources of polycyclic aromatic hydrocarbon (PAH) in marine environment of China. Chinese Journal of Oceanology and Limnology, 22(2):136-145.
Zheng S L, Chen B, Wang Z, Qiu X Y, Yu X, Freestone D, Liu Z H, Huang H, Yu W W, Xu X Z. 2010. Reproductive toxic effects of sublethal cadmium on the marine polychaete Perinereis nuntia. Ecotoxicology and Environmental Safety, 73(6):1 196-1 201.
|
|
|
|