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Intersexuality of Oyster, Crassostrea gigas in Uninhabited Island Waters Near Yeosu, Korea

한국 여수 인근 무인도 해역에서 굴 Crassostrea gigas의 인터섹스 출현율

  • Park, Jung Jun (Aquaculture Management Division, National Institute of Fisheries Science (NIFS)) ;
  • Shin, So Ryung (Department of Aqualife Medicine, Chonnam National University) ;
  • Kim, Hyeon Jin (Department of Aqualife Medicine, Chonnam National University) ;
  • Oh, Han Young (Department of Aqualife Medicine, Chonnam National University) ;
  • Lee, Dong-Geun (JeollaNamdo Institute of Ocean&Fisheries Science) ;
  • Lee, Jung Sick (Department of Aqualife Medicine, Chonnam National University)
  • 박정준 (국립수산과학원 양식연구과) ;
  • 신소령 (전남대학교 수산생명의학과) ;
  • 김현진 (전남대학교 수산생명의학과) ;
  • 오한영 (전남대학교 수산생명의학과) ;
  • 이동근 (전라남도 해양수산과학원) ;
  • 이정식 (전남대학교 수산생명의학과)
  • Received : 2021.11.05
  • Accepted : 2021.11.16
  • Published : 2021.12.15

Abstract

The purpose of this study was to report the intersex identified in the oyster Crassostrea gigas (n=410, SH 43.3±11.4 mm) in the waters around 13 uninhabited islands near Yeosu. The overall sex ratio (male: female) was 1:1.1, but there was a difference between the sampling areas. In Gajangdo, Sogyeongdo, and Jungsamdo, females showed a high ratio of 65% or more, and in Songdo, Chodo, and Buseodo, males showed a high ratio of 65% or more. The overall intersexuality was about 12.8%, which was high in males, about 34.7% in females and 64.3% in males. Intersexuality was the highest with about 43.8% in Chodo of Gamak Bay. Histologically, intersex could be divided into three types: intrafollicular type, interfollicular type and mixed type. Among these three types, the intrafollicular type was the most dominant with about 81.6%. The intersex cause of oysters reported in this study is considered to require detailed research in the future.

본 연구는 여수 인근 13개 무인도 주변 해역의 굴 Crassostrea gigas (n=410, SH 43.3±11.4 mm)에서 확인된 인터섹스 현상을 보고하고자 하였다. 전체 성비(암:수)는 1:1.1이었으나 채집 정점별로 성비의 차이를 보였다. 가장도, 소경도, 중삼도에서는 암컷이 65% 이상의 높은 비율을 보였으며, 송도, 초도, 부서도에서는 수컷이 65% 이상의 높은 비율을 나타냈다. 전체 intersexuality 는 약 12.8%로 암컷에서 약 34.7%, 수컷에서 약 64.3%로 수컷에서 높았다. Intersexuality는 가막만의 초도에서 약 43.8%로 가장 높았다. 조직학적으로 인터섹스는 intrafollicular type, interfollicular type, mixed type의 세 가지 형태로 나눌 수 있었다. 이들 세 가지 형태 가운데 intrafollicular type이 약 81.6%로 가장 우세하였다. 본 연구에서 보고된 굴의 인터섹스 원인에 관해서는 추후 세부적인 연구가 필요할 것으로 생각된다.

Keywords

Acknowledgement

본 연구는 2021년도 국립수산과학원 수산과학연구사업(R2021003)의 지원으로 수행되었습니다.

References

  1. Ackermann GE, Schwaiger J, Negele RD, Fent K. 2002. Effects of long-term nonylphenol exposure on gonadal development and biomarkers of estrogenicity in juvenile rainbow trout, Oncorhynchus mykiss. Aquat Toxicol 60: 203-221. https://doi.org/10.1016/S0166-445X(02)00003-6
  2. Andrew MN, Dunstan RH, O'Connor WA, Van Zwieten L, Nixon B, MacFarlane GR. 2008. Effects of 4-nonylphenol and 17-ethynylestradiol exposure in the Sydney rock oyster, Saccostrea glomerata: Vitellogenin induction and gonadal development. Aquat Toxicol 88: 39-47. https://doi.org/10.1016/j.aquatox.2008.03.003
  3. Baralla E, Pasciu V, Varoni MV, Nieddub M, Demuro R, Demontis MP. 2021. Bisphenols' occurrence in bivalves as sentinel of environmental contamination. Sci Total Environ 785: 147263. https://doi.org/10.1016/j.scitotenv.2021.147263
  4. Bortone SA, Davis WP. 1994. Fish intersexuality as indicator of environmental stress: Monitoring fish reproductive systems can serve to alert humans to potential harm. Bioscience 44: 165-172. https://doi.org/10.2307/1312253
  5. Byrne PA, O'Halloran J. 2001. The role of bivalve molluscs as tools in estuarine sediment toxicity testing: a review. Hydrobiologia 465: 209-217. https://doi.org/10.1023/A:1014584607501
  6. Chesman BS, Langston WJ. 2006. Intersex in the clam Scrobicularia plana: a sign of endocrine disruption in estuaries? Biol Lett 2: 420-422. https://doi.org/10.1098/rsbl.2006.0482
  7. Drysdale DT, Bortone SA. 1989. Laboratory induction of intersexuality in the mosquitofish, Gambusia affinis, using paper mill effluent. Bull Environ Contam Toxicol 43: 611-617. https://doi.org/10.1007/BF01701943
  8. Dublinowska M, Smolarz K, Zabrzanska S, Larsson J, Czerniawska N. 2016. Intersexuality in the blue mussel Mytilus edulis complex (Mytilidae) from the Baltic Sea and the Danish Strait. Am Malacol Bull 34: 28-39. https://doi.org/10.4003/006.034.0105
  9. Gagne F, Blaise C, Pellerin J, Pelletier E, Douville M, Gauthier-Clerc S, Viglino L. 2003. Sex alteration in soft-shell clams, Mya arenaria in an intertidal zone of the Saint Lawrence River (Quebec, Canada). Comp Biochem Physiol C 134: 189-198. https://doi.org/10.1016/S1096-4959(02)00250-6
  10. Gauthier-Clerc S, Pellerin J, Blaise C, Gagne F. 2002. Delayed gametogenesis of Mya arenaria in the Saguenay fjord (Canada): a consequence of endocrine disruptors? Comp Biochem Physiol C 131: 457-467. https://doi.org/10.1016/S1095-6433(01)00485-8
  11. Gibbs PE, Pascoe PL, Burt GR. 1988. Sex change in the female dog-whelk, Nucella lapillus, induced by tributyltin from antifouling paints. J Mar Biol Assoc UK 68: 715-731. https://doi.org/10.1017/S0025315400028824
  12. Gimeno S, Komen H, Venderbosch PWM, Bowmer T. 1997. Disruption of sexual differentiation in genetic male common carp (Cyprinus carpio) exposed to an alkylphenol during different life stages. Environ Sci Technol 31: 2884-2890. https://doi.org/10.1021/es970215h
  13. Gomes T, Gonzalez-Rey M, Bebianno MJ. 2009. Incidence of intersex in male clams Scrobicularia plana in the Guadiana Estuary (Portugal). Ecotoxicology 18: 1104-1109. https://doi.org/10.1007/s10646-009-0359-5
  14. Graca B, Rychter A, Staniszewska M, Smolarz K, Sokolowski A, Bodziach K. 2021. Bioaccumulation of phenolic endocrine disruptors in the clam Rangia cuneata: Storage in shells and influence of size and sex. Environ Res 197: 111181. https://doi.org/10.1016/j.envres.2021.111181
  15. Gray MA, Metcalfe CD. 1997. Induction of testis-ova in Japanese medaka, Oryzias latipes exposed to p-nonylphenol. Environ Toxicol Chem 16: 1082-1086. https://doi.org/10.1897/1551-5028(1997)016<1082:IOTOIJ>2.3.CO;2
  16. Guo X, Hedgecock D, Hershberger WK, Cooper K, Allen SK Jr. 1998. Genetic determinants of protandric sex in the Pacific oyster, Crassostrea gigas Thunberg. Evolution 52: 394-402. https://doi.org/10.2307/2411076
  17. Holm G, Norrgren L, Linden O. 1991. Reproductive and histopathological effects of long-term experimental exposure to bis(tributyltin)oxide (TBTO) on the three-spined stickleback, Gasterosteus aculeatus Linnaeus. J Fish Biol 38: 373-386. https://doi.org/10.1111/j.1095-8649.1991.tb03127.x
  18. Horiguchi T, Shiraishi H, Shimizu M, Morita M. 1994. Imposex and organotin compounds in Thais clavigera and T. bronniin Japan. J Mar Biol Ass UK 74: 651-669. https://doi.org/10.1017/S002531540004772X
  19. Huggett RJ, Kimerle RA, Mehrle PM Jr, Bergman HL (eds.). 1992. Biomarkers: biochemical, physiological, and histological markers of anthropogenic stress. Lewis Publishers, London, pp 347.
  20. Iguchi T. 1998. Environmental endocrine disruptors. Jap J Clin Med 56: 2953-2962.
  21. Jeon MA, Kang JC, Lee JS. 2013. Concentration of heavy metal and alteration of reproductive and histological biomarker of Mytilus galloprovincialis in Gamak Bay of the Southern coast of Korea. Korean J Malacol 29: 33-41. https://doi.org/10.9710/kjm.2013.29.1.33
  22. Jobling S, Coey S, Whitmore JG, Kime DE, Van Look KJW, McAllister BG, Beresford N, Henshaw AC, Brisghty G, Tyler CR, Sumpter JP. 2002. Wild intersex roach, Rutilus rutilus have reduced fertility. Biol Reprod 67: 515-524. https://doi.org/10.1095/biolreprod67.2.515
  23. Jobling S, Nolan M, Tyler CR, Brighty G, Sumpter JP. 1998. Widespread sexual disruption in wild fish. Environ Sci Technol 32: 2498-2506. https://doi.org/10.1021/es9710870
  24. Ju SM, Lee JW, Jin YG, Yu J, Lee JS. 2006. Effect of zinc bioaccumulation on survival rate, activity, growth and organ structure of the equilateral venus, Gomphina veneriformis (Bivalvia: Veneridae). Environ Health Toxicol 21: 115-126.
  25. Ju SM, Park JJ, Lee JS. 2009. Induction of intersex and masculinization of the equilateral venus, Gomphina veneriformis (Bivalvia: Veneridae) by Zinc. Anim Cells Syst 13: 339-344. https://doi.org/10.1080/19768354.2009.9647227
  26. Kim HJ, Shin SR, Kim H, Park JJ, Shin YK, Lee JS. 2021. Induction of sex ratio change and intersex in Tegillarca granosa (Bivalvia: Arcidae) by waterborne zinc exposure. Aquacult Rep 21: 1000794.
  27. Lee JS, Cho HS, Jin YG, Park JJ, Shin YK. 2009. Reproductive disrupting effect of organotin compound in the ark shell, Scapharca broughtonii (Bivalvia: Arcidae). Anim Cells Syst 13: 223-227. https://doi.org/10.1080/19768354.2009.9647214
  28. Lee JS, Lee YG, Kang SW, Park JS, Lee DG, Jeon MA, Ju SM. 2010. Intersexuality of Crassostrea gigas and Ruditapes philippinarum in Southern coastal waters of Korea. Environ Anal Health Toxicol 25: 287-294.
  29. Lee JS, Park JJ. 2007. Risk assessment of nonylphenol using the sex ratio, sexual maturation, intersex and lipofuscin accumulation of the equilateral venus, Gomphina veneriformis (Bivalvia: Veneridae). Korean J Fish Aquat Sci 40: 16-23. https://doi.org/10.5657/KFAS.2007.40.1.016
  30. Lee JS, Park JJ, Shin YK, Kim H, Jeon MA. 2014. Sex change and sequential hermaphroditism in Tegillarca granosa (Bivalvia: Arcidae). Invertebr Reprod Dev 58: 314-318. https://doi.org/10.1080/07924259.2014.949014
  31. Lee JS, Park JS, Shin YK, Lee YG, Park JJ. 2013. Sequential hermaphroditism in Manila clam Ruditapes philippinarum (Bivalvia: Veneridae). Invertebr Reprod Dev 57: 185-188. https://doi.org/10.1080/07924259.2012.717109
  32. Marin MG, Boscolo R, Cella A, Degetto S, Ros LD. 2006. Field validation of autometallographical black silver deposit (BSD) extent in three bivalve species from the Lagoon of Venice, Italy (Mytilus galloprovincialis, Tapes philippinarum, Scapharca inaequivalvis) for metal bioavailability assessment. Sci Total Environ 371: 156-167. https://doi.org/10.1016/j.scitotenv.2006.09.003
  33. Matozzo V, Marin MG. 2005. Can 4-nonylphenol induce vitellogenin-like proteins in the clam, Tapes philippinarum? Environ Res 97: 43-49. https://doi.org/10.1016/j.envres.2004.03.002
  34. Nimrod AC, Benson WH. 1996. Environmental estrogenic effects of alkylphenol ethoxylates. Crit Rev Toxicol 26: 335-364. https://doi.org/10.3109/10408449609012527
  35. NRC (National Research Council). 1983. Risk assessment in the federal government: managing the process. National Academy Press, Washington DC, pp 192.
  36. Park JJ. 2008. Study on the bioindicator of the equilateral venus, Gomphina veneriformis (Bivalvia: Veneridae) chronically exposed to TBT (tributytin chloride). Yeosu: Chonnam National University, pp 222.
  37. Park JJ, Kim H, Kang SW, An CM, Lee S, Gye MC, Lee JS. 2012. Sex ratio and sex reversal in two-year-old class of oyster, Crassostrea gigas (Bivalvia: Ostreidae). Dev Reprod 16: 385-388. https://doi.org/10.12717/DR.2012.16.4.385
  38. Park JS, Lee JS. 2011. Change of reproductive and histological biomarkers of Ruditapes philippinarum (Bivalvia: Veneridae) exposed to nonylphenol. Korean J Malacol 27: 181-190. https://doi.org/10.9710/kjm.2011.27.3.181
  39. Quinn B, Gagne F, Blaise C, Costello MJ, Wilson JG, Mothersill C. 2006. Evaluation of the lethal the sub-lethal toxicity and potential endocrine distupting effect of nonylphenol on the zebra mussel, Dreissena polymorpha. Comp Biochem Physiol C 142: 118-127.
  40. Quinn B, Gagne F, Costello M, McKenzie C, Wilson J, Mothersill C. 2004. The endocrine disrupting effect of municipal effluent on the zebra mussel (Dreissena polymorpha). Aquat Toxicol 66: 297-292.
  41. Reinboth R. 1975. Intersexuality in the animal kingdom. Springer-Verlag, New York, pp 449.
  42. Sadovy Y, Shapiro DY. 1987. Criteria for the diagnosis of hermaphroditism in fishes. Copeia 1987: 136-156. https://doi.org/10.2307/1446046
  43. Schintu M, Durante L, Maccioni A, Meloni P, Degetto S, Contu A. 2008. Measurement of environmental trace-metal levels in Mediterranean coastal areas with transplanted mussels and DGT techniques. Mar Pollut Bull 57: 832-837. https://doi.org/10.1016/j.marpolbul.2008.02.038
  44. Siah A, Pellerin J, Amiard JC, Pelletier E, Viglino L. 2003. Delayed gametogenesis and progesterone levels in soft-shell clams, Mya arenaria in relation to in situ contamination to organotins and heavy metals in the St. Lawrence River (Canada). Comp Biochem Physiol C 135: 145-156.
  45. Trevor PRG, Susan J, Carole K, Steven M, Geoff B, Michael JW, John PS, Charles RT. 2001. Exposure of juvenile roach, Rutilus rutilus to treated sewage effluent induces dose-dependent and persistent disruption in gonadal duct development. Environ Sci Techol 35: 462-470. https://doi.org/10.1021/es001225c
  46. Tyler CR, Routledge EJ. 1998. Natural and anthropogenic environmental oestrogens: the scientific basis for risk assessment, oestrogenic effects in fish in English rivers with evidence of their causation. Pure Appl Chem 70: 1795-1804. https://doi.org/10.1351/pac199870091795
  47. WWF (World Wide Fund for Nature). 2006. Reducing your risk from EDCs. WWF, Switzerland, pp 20.