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A Preliminary Survey of Estrogenic Effects in Cultured Adult Male Nile Tilapia (Oreochromis niloticus) in the Seven Lakes of San Pablo City, Philippines

Abstract

This study aimed to investigate the impact of estrogenic endocrine disruptors in adult male Nile Tilapia (Oreochromis niloticus) from the Seven Lakes (Bunot, Calibato, Mohicap, Palakpakin, Pandin, Sampaloc and Yambo) of San Pablo City in Laguna, Philippines. Fish were collected from aquaculture operations in each lake from July to September 2017 and examined for plasma vitellogenin (VTG) levels, hepatosomatic index (HSI) and gonadosomatic index (GSI). In comparison to the reference group (Pandin Lake), fish from Mohicap, Sampaloc and Yambo had higher levels of plasma VTG. HSI was increased in fish from Bunot Lake while it was markedly reduced in fish from Sampaloc Lake. Comparable GSI were obtained in all samples. While most examined fish are in active spermatogenesis, fish from Sampaloc Lake had immature gonads with no spermatozoa, and with minimal to moderate Leydig cell vacuolation and hyperplasia. The results suggest that cultured Nile tilapia from Sampaloc Lake is most adversely affected by endocrine-active compounds. The identification and quantification of these chemicals are recommended in future studies.

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References

  1. Al-Ghais SM (2013) Acetylcholinesterase, glutathione and hepatosomatic index as potential biomarkers of sewage pollution and depuration in fish. Mar Pollut Bull 74(1):183–186

    Article  CAS  Google Scholar 

  2. Araujo FG, Morado CN, Parente TTE, Paumgartten FJR, Gomes ID (2018) Biomarkers and bioindicators of the environmental condition using a fish species (Pimelodus maculatus Lacepède, 1803) in a tropical reservoir in Southeastern Brazil. Braz J Biol 78(2):351–359

    Article  CAS  Google Scholar 

  3. Asem-Hiablie S, Church CD, Elliott HA, Shappell NW, Schoenfuss HL, Drechsel P, Williams CF, Knopf AL, Dabie MY (2013) Serum estrogenicity and biological responses in African catfish raised in wastewater ponds in Ghana. Sci Total Environ 463–464:1182–1191. https://doi.org/10.1016/j.scitotenv.2013.06.032

    Article  CAS  Google Scholar 

  4. Berg H, Modig C, Olsson P-E (2004) 17beta-estradiol induced vitellogenesis is inhibited by cortisol at the post-transcriptional level in Arctic char (Salvelinus alpinus). Reprod Biol Endocrinol. 2:62. https://doi.org/10.1186/1477-7827-2-62

    Article  CAS  Google Scholar 

  5. Brillo BBC (2017) The governance of the Seven Crater Lakes, San Pablo City, Philippines. Asian J Water Environ Pollut 14(2):13–25

    Article  Google Scholar 

  6. Brillo BBC (2016) Developing a small lake: the case of Palakpakin Lake, San Pablo City. Philippines. Water Resources 43(4):611–620

    Article  CAS  Google Scholar 

  7. Brillo BBC (2015) Developing Mohicap Lake, San Pablo City, Philippines. Soc Sci J 11(3):283–290

    Google Scholar 

  8. Brillo BBC (2015) Development issues regarding Bunot Lake: the lesser lake among the seven lakes of San Pablo City, Philippines. Lakes Reservoirs: Sci Policy Manage Sustain Use 20:155–165

    Article  Google Scholar 

  9. Creasy DM, Maronpot RR, Giri DK (n.d.) Testis, interstitial cell—vacuolation. NTP Nonneoplastic Lesion Atlas. National Toxicology program US Department of Health and Human Services https://ntp.niehs.nih.gov/nnl/male_reproductive/testis/intcvac/testis_interstitial_cell-vacuolation_508.pdf. Accessed 3 May 2018

  10. El-Sayed Ali T, Abdel-Aziz SH, El-Sayed AFM, Zeid S (2014) Structural and functional effects of early exposure to 4-nonylphenol on gonadal development of Nile Tilapia (Oreochromis niloticus): b-histological alterations in testes. Fish Physiol Biochem 40:1495–1507

    Article  CAS  Google Scholar 

  11. Filby AL, Thorpe KL, Tyler CR (2006) Multiple molecular effect pathways of an environmental oestrogen in fish. J Mol Endocrinol 37:121–134

    Article  CAS  Google Scholar 

  12. Herman RL, Kincaid HL (1988) Pathological effects of orally administered estradiol to rainbow trout. Aquaculture 72:165–172

    Article  CAS  Google Scholar 

  13. Kavanagh RJ, Balch GC, Kiparissis Y, Niimi AJ, Sherry J, Tinson C, Metcalfe CD (2004) Endocrine Disruption and Altered Gonadal Development in White Perch (Morone americana) from the Lower Great Lakes Region. Environ Health Perspect 112:898–902. https://doi.org/10.1289/ehp.6514

    Article  CAS  Google Scholar 

  14. Kidd KA, Blanchfield PJ, Mills KH, Palace VP, Evans RE, Lazorchak JM, Flick RW (2007) Collapse of a fish population after exposure to a synthetic estrogen. Proc Natl Acad Sci USA 104(21):8897–8901. https://doi.org/10.1073/pnas.0609568104

    Article  CAS  Google Scholar 

  15. Jobling S, Sumpter JP, Sheahan D, Osborne JA, Matthiesen P (1996) Inhibition of testicular growth in rainbow trout (Oncorhynchus mykiss) exposed to estrogenic alkylphenolic chemicals. Environ Toxicol Chem 15(2):194–202

    Article  CAS  Google Scholar 

  16. Leaños-Castañeda O, Van Der Kraak G, Lister A, Sima-Alvarez R, Gold-Bouchot G (2002) O, p’-DDT induction of Vitellogenesis and its inhibition by tamoxifen in Nile tilapia (Oreochromis niloticus). Mar Environ Res 54:703–707

    Article  Google Scholar 

  17. LLDA (2008) Water Quality Report of the Seven Crater Lakes. www.llda.gov.ph.

  18. LLDA ( 2016) Water Quality Report of The Seven Crater Lakes. Unpublished raw data.

  19. Ma T, Wan X, Huang O, Wang Z (2005) Biomarker responses and reproductive toxicity of the effluent from a Chinese large sewage treatment plant in Japanese medaka (Oryzias latipes). Chemosphere 59(2):281–288

    Article  CAS  Google Scholar 

  20. Mandich A, Bottero S, Benfenati E, Cevasco A, Erratico C, Maggioni S, Massari A, Pedemonte F, Viganò L, (2007) In vivo exposure of carp to graded concentrations of bisphenol A. Gen Comp Endocrinol 153(2007):15–24

    Article  CAS  Google Scholar 

  21. Matsumoto T, Kobayashi M, Moriwaki T, Kawai S, Watabe A (2004) Survey of estrogenic activity in fish feed by yeast estrogen-screen assay. Comp Biochem Physiol C Toxicol Pharmacol 139(1–3):147–152

    Article  CAS  Google Scholar 

  22. Meng SL, Qiu LP, Hu GD, Fan LM, Song C, Zheng Y, Wu W, Qu JH, Li DD, Chen JZ, Xu P (2017) Effect of methomyl on sex steroid hormone and vitellogenin levels in serum of male tilapia (Oreochromis niloticus). Environ Toxicol 7:1869–1877. https://doi.org/10.1002/tox.22409

    Article  CAS  Google Scholar 

  23. Organisation for Economic Co-operation and Development (2010) OECD Guidance Document for the Diagnosis of Endocrine-Related Histopathology of Fish Gonads. OECD. OECD series on testing and assessment no. 123. Organisation for Economic Cooperation and Development, Paris, p 182

  24. Örn S, Yamani S, Norrgren L (2006) Comparison of vitellogenin induction, sex ratio, and gonad morphology between zebrafish and Japanese medaka after exposure to 17a-ethinylestradiol and 17b-trenbolone. Arch Environ Contam Toxicol 51:237–243

    Article  CAS  Google Scholar 

  25. Paller VGV, Corpuz MNC, Bandal MJRZ (2017) Freshwater fish assemblages and water quality parameters in Seven Lakes of San Pablo, Laguna, Philippines. Asian Sci J. https://doi.org/10.7828/ajob.v8i1.995

    Article  Google Scholar 

  26. Park CB, Aoki JY, Lee JS, Nagae M, Lee YD, Sakakura Y, Hagiwara A, Soyano K (2010) The effects of 17beta-estradiol on various reproductive parameters in the hermaphrodite fish Kryptolebias marmoratus. Aquat Toxicol 96(4):273–279. https://doi.org/10.1016/j.aquatox.2009.11.006

    Article  CAS  Google Scholar 

  27. Rodas-Ortiz JP (2008) Vitellogenin induction and increased plasma 17β-estradiol concentrations in male Nile Tilapia, Oreochromis niloticus. Bull Environ Contam Toxicol. 81:543–547. https://doi.org/10.1007/s00128-008-9556-9

    Article  CAS  Google Scholar 

  28. Schulz RW, Vischer HF, Cavaco JE, Santos EM, Tyler CR, Goos HJ, Bogerd J (2001) Gonadotropins, their receptors, and the regulation of testicular functions in fish. Comp Biochem. Physiol B Biochem. Mol. Biol. 129:407–417

    Article  CAS  Google Scholar 

  29. Teta C, Holbech BF, Norrgren L, Naik YS (2018) Occurrence of oestrogenic pollutants and widespread feminisation of male tilapia in peri-urban dams in Bulawayo, Zimbabwe. Afr J Aquat Sci. https://doi.org/10.2989/16085914.2017.1423269

    Article  Google Scholar 

  30. Water Quality Report of the Seven Crater Lakes (2008) https://www.llda.gov.ph/dox/7lakes/7craterlakes.pdf. Accessed 16 March 2017.

  31. Zafaralla MT (2010) Plankton biodiversity, water quality and environmental status Los Banos’ Crocodile Lake and San Pablo City’s Seven Lakes (Lake Sampaloc and Pandin). [Term Report]. https://agris.fao.org/agris-search/search.do?recordID=PH2012000144. Accessed 16 March 2017

  32. Zaghloul KH, Hasheesh WS, Zahran IA, Mohmed-Assem S. Marie MS (2007) Ecological and biological studies on the Nile tilapia Oreochromis niloticus along different sites of lake Burullus, Egypt. J Aquat Biol Fish 11(3): 57–88 (2007) ISSN 1110 – 6131

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Acknowledgements

The authors would like to thank the UP Enhanced Creative Work and Research Grant (ECWRG-2016-2-074) for funding this study and the Laguna Lake Development Authority (LLDA) for the water quality data.

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Correspondence to Michelle Grace V. Paraso.

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Mabansag, C.J.A., Paraso, M.G.V., Marcelino, R.T. et al. A Preliminary Survey of Estrogenic Effects in Cultured Adult Male Nile Tilapia (Oreochromis niloticus) in the Seven Lakes of San Pablo City, Philippines. Bull Environ Contam Toxicol 103, 400–404 (2019). https://doi.org/10.1007/s00128-019-02685-z

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Keywords

  • Endocrine disruption
  • Estrogenic
  • Fish
  • Lake
  • Vitellogenin