DOI QR코드

DOI QR Code

Mercury Concentrations of Black-tailed Gull Eggs Depending on the Egg-Laying Order for Marine Environmental Monitoring

연안환경 수은 모니터링용 괭이갈매기 알의 산란순서별 농도 차이

  • Lee, Jangho (Natural Environment Research Division, National Institute of Environmental Research) ;
  • Lee, Jongchun (Natural Environment Research Division, National Institute of Environmental Research) ;
  • Jang, Heeyeon (Natural Environment Research Division, National Institute of Environmental Research) ;
  • Park, Jong-Hyouk (Saemangeum Regional Environmental Office) ;
  • Choi, Jeong-Heui (Natural Environment Research Division, National Institute of Environmental Research) ;
  • Lee, Soo Yong (Natural Environment Research Division, National Institute of Environmental Research) ;
  • Shim, Kyuyoung (Natural Environment Research Division, National Institute of Environmental Research)
  • 이장호 (국립환경과학원 자연환경연구과) ;
  • 이종천 (국립환경과학원 자연환경연구과) ;
  • 장희연 (국립환경과학원 자연환경연구과) ;
  • 박종혁 (새만금유역환경청) ;
  • 최정희 (국립환경과학원 자연환경연구과) ;
  • 이수용 (국립환경과학원 자연환경연구과) ;
  • 심규영 (국립환경과학원 자연환경연구과)
  • Received : 2017.09.25
  • Accepted : 2017.12.26
  • Published : 2017.12.31

Abstract

In this study, total mercury (THg) of Black-tailed Gull (Larus crassirostris) eggs laid on Baengnyeongdo, West Sea of Korea was analyzed in order to compare the THg concentrations of eggs depending on egg-laying order. The first-laid eggs ($mean{\pm}standard$ error, $234.4{\pm}11.2ng/g\;wet$, n=18, t=8.4, p<0.01) significantly had higher THg concentrations than the second-laid eggs ($182.8{\pm}9.1ng/g\;wet$, n=18). Also, the first-laid eggs had higher values in biometrics (length $63.10{\pm}0.49mm$, t=2.4, p<0.05; width $44.51{\pm}0.19mm$, t=4.3, p<0.01; weight $65.53{\pm}0.87g$, t=4.2, p<0.01) than the second-laid eggs (length $62.37{\pm}0.40mm$, width $43.55{\pm}0.17mm$, and weight $62.48{\pm}0.72g$). These differences might be attributed to the amount of food eaten by females relating to males' courtship feeding pattern (males increase courtship feeding rate before the first eggs are laid, and decrease the rate following the laying of the first eggs). Moreover, the lower food intake of females could diminish the quantities of egg albumen that contains a protein binds to most of methylmercury during the period of egg production. Therefore, it is necessary to consistently apply one of egg selection methods (targeted selection (the first-laid egg or the second-laid egg), random selection, and etc.) in one nest for ensuring comparability of mercury concentrations among monitoring sites and monitoring years.

본 연구에서는 연안환경 오염물질 중 수은의 생물축적 모니터링 지표종인 괭이갈매기(Larus crassirostris) 알의 산란순서 간 수은 농도차이를 서해 백령도 번식지를 대상으로 분석하였다. 첫 번째(평균${\pm}$표준오차, $234.4{\pm}11.2ng/g\;wet$) 산란한 알의 총수은 농도는 두 번째($182.8{\pm}9.1ng/g\;wet$) 산란한 알에 비해 통계적으로 유의하게 높게 나타났다(각 n=18, t=8.4, p<0.01). 또한 생체특성치에서도 장경, 단경, 중량 모두 첫 번째 알(길이: $63.10{\pm}0.49mm$, 단경: $44.51{\pm}0.19mm$, 중량 $65.53{\pm}0.87g$) 이 두 번째 알(장경: $62.37{\pm}0.40mm$, 단경: $43.55{\pm}0.17mm$, $62.48{\pm}0.72g$)보다 통계적으로 유의하게 높게 나타났다(각 n=18, 장경 t=2.4, p<0.05; 단경 t=4.3, p<0.01; 중량 t=4.2, p<0.01). 이러한 차이는 알 생성기에 암컷이 섭취하는 먹이량과 관련이 있으며, 이는 수컷이 암컷에게 먹이를 공급하다가 첫 번째 알을 낳으면 급이 빈도와 양을 줄이는 구애급이 행동패턴 변화와 관련이 있는 것으로 추측된다. 특히, 암컷의 섭취량 감소는 메틸수은이 주로 존재하는 알 속 흰자(albumen)의 감소에 영향을 미치는 것으로 판단된다. 따라서 수은의 경우, 산란순서에 따라 축적농도가 감소하는 경향이 뚜렷하기 때문에 지역 간 그리고 시기별 비교 모니터링을 수행할 때는 목적과 조사여건(번식경과를 고려한 채취 시기, 입도(入島) 체류가능기간 등) 등을 고려하여 둥지 내 알 선택방법(첫 번째 알만 선택 또는 두 번째 알만 선택 또는 랜덤선택 등)을 일관되게 적용하는 것이 중요하다고 판단된다.

Keywords

References

  1. Ackerman JT, Herzog MP, Schwarzbach SE. 2013. Methylmercury is the predominant form of mercury in bird eggs: a synthesis. Environ Tech. 47: 2052-2060. https://doi.org/10.1021/es304385y
  2. Ackerman JT, Eagles-Smith CA, Herzog MP, Yee JL, Hartman CA. 2016. Egg-laying sequence influences egg mercury concentrations and egg size in three bird species: Implications for contaminant monitoring programs. Environ Toxicol. 35(6): 1458-1469. https://doi.org/10.1002/etc.3291
  3. Becker PH. 1992. Egg mercury levels decline with the laying sequence in Charadriiformes. Bull Environ Contam Toxicol. 48: 762-767.
  4. Burger J, Gochfeld M, Jeitner C, Burke S, Volz CD, Snigaroff R, Snigaroff D, Shukla T, Shukla S. 2009. Mercury and other metals in eggs and feathers of glaucous-winged gulls (Larus glaucescens) in the Aleutians. Environ Monit Assess. 152(0): 179-194. https://doi.org/10.1007/s10661-008-0306-6
  5. Burgess NM, Bond AL, Hebert CE, Neugebauer E, Champoux L. 2013. Mercury trends in herring gull (Larus argentatus) eggs from Atlantic Canada, 1972-2008: temporal change or dietary shift? Environ Pollut. 172: 216-222. https://doi.org/10.1016/j.envpol.2012.09.001
  6. Choi HG, Park JS, Lee PY. 1992. Study on the heavy metal concentration in mussels and oysters from the Korean coastal waters. Bull Korean Fish Soc. 15(6): 485-494.
  7. Choi JW, Matsuda M, Kawano M, Wakimoto T, Iseki N, Masunaga S, Hayama SI, Watanuki Y. 2001a. Chlorinated persistent organic pollutants in black-tailed gulls (Larus crassirostris) from Hokkaido, Japan. Chemoshpere. 44: 1375-1382. https://doi.org/10.1016/S0045-6535(00)00358-1
  8. Choi JW, Matsuda M, Kawano M, Min BY, Wakimoto T. 2001b. Accumulation profiles of persistent organochlorines in waterbirds from an estuary in Korea. Arch Environ Contam Toxicol. 41: 353-363. https://doi.org/10.1007/s002440010259
  9. Dauwe T, Bervoets L, Blust R, Pinxten R, Eens M. 1999. Are eggshell and egg contents of great and blue tits suitable as indicators of heavy metal pollution?. Belg J Zool. 129(2): 439-447.
  10. Ewins PJ, Postupalsky S, Hughes KD, Weseloh DV. 1999. Organochlorine contaminant residues and shell thickness of eggs from known-age female ospreys (Pandion haliaetus) in Michigan during the 1980s. Environ Pollut. 104: 295-304. https://doi.org/10.1016/S0269-7491(98)00159-6
  11. Honda K., Min BY, Tatsukawa, R. 1986. Distribution of heavy metals and their agerelated changes in the Eastern Great White Egret, Egretta alba modesta, in Korea. Arch Environ Contam Toxicol. 15: 185-197. https://doi.org/10.1007/BF01059967
  12. Hong SH, Shim WJ, Han GM, Ha SY, Jang M, Rani M, Hong S, Yeo GY. 2014. Levels and profiles of persistent organic pollutants in resident and migratory birds from an urbanized coastal region of South Korea. Sci of the Total Environ. 470-471:1463-1470. https://doi.org/10.1016/j.scitotenv.2013.07.089
  13. Heinz GH, Hoffman DJ. 2004. Mercury accumulation and loss in mallard eggs. Environ Toxicol Chem. 23(1): 222-224. https://doi.org/10.1897/03-111
  14. Hwang DW, Kim SG, Choi MK, Lee IS, Kim SS, Choi HG. 2016. Monitoring of trace metals in coastal sediments around Korean Peninsula. Marine Pollut Bull. 102: 230-239. https://doi.org/10.1016/j.marpolbul.2015.09.045
  15. Islam MM, Bang S, Kim KW, Ahmed MK, Jannat M. 2010. Heavy metals in frozen and canned marine fish of Korea. J Sci Res. 2(3): 549-557.
  16. Kim JS, Han SH, Lee DP, Koo TH. 2001. Heavy metal contamination of feral pigeons Columba livia by habitat in Seoul. Korean J Ecol. 24(5): 303-307.
  17. Kim JS, Koo TH. 2008. Heavy metal concentrations in feathers of Korean shorebirds. Arch Environ Contam Toxicol 55: 122-128. https://doi.org/10.1007/s00244-007-9089-y
  18. Kim JS, Lee DP, Koo TH. 2003. Monitoring of heavy metal contaminations using feathers of feral pigeons Columba livia in Seoul, Korean J Ecol. 26(3): 91-96. https://doi.org/10.5141/JEFB.2003.26.3.091
  19. Kim SJ, Lee JN, Lee DP. 2006. Cadmium and lead levels of loons wintering in Korea. J Ecol Field Biol. 29(6): 539-543. https://doi.org/10.5141/JEFB.2006.29.6.539
  20. Kim JS, Oh JM. 2012. Monitoring of heavy metal contaminants using feathers of shorebirds, Korea. J Environ Monit. 14: 651-656. https://doi.org/10.1039/c2em10729e
  21. Kim JS, Oh JM. 2014. Heavy metal concentrations in Black-tailed Gull (Larus crassirostris) chicks, Korea. Chemosphere. 112: 370-376. https://doi.org/10.1016/j.chemosphere.2014.04.059
  22. Kim JS, Oh JM. 2015. Comparison of trace element concentrations between chick and adult Black-tailed Gull (Larus crassirostris). Bull Environ Contam Toxicol. 94: 727-731. https://doi.org/10.1007/s00128-015-1536-2
  23. Kim JS, Shin JR, Koo TH. 2009. Heavy metal distribution in some wild birds from Korea. Arch Environ Contam Toxicol. 56:317-324. https://doi.org/10.1007/s00244-008-9180-z
  24. Klein R, Bartel-Steinbach M, Koschorreck J, Paulus M, Tarricone K, Teubner D, Wagner G, Weimann T, Veith M. 2012. Standardization of egg collection from aquatic birds for biomonitoring - a critical review, Envrion Sci & Tech. 1-40.
  25. Koster MD, Ryckman DP, Weseloh DVC, Struger J. 1996. Mercury levels in great lakes herring gull (Larus argentatus) eggs, 1972-1992. Environ Pollut. 93(3): 261-270. https://doi.org/10.1016/S0269-7491(96)00043-7
  26. Kwon YS, Lee WS, Yoo JC. 2006. Clutch size and breeding success of Black-tailed Gull (Larus crassirostris) at Hongdo Island, southeast coast of South Korea. Ocean and Polar Res. 28(2):2 01-207. https://doi.org/10.4217/OPR.2006.28.2.201
  27. Lee DP, Honda K, Tatsukawa R. 1987. Comparison of tissue distributions of heavy metals in birds in Japan and Korea. Yamashina Inst Ornith. 19: 103-116. https://doi.org/10.3312/jyio1952.19.103
  28. Lee WS, Koo TH, Park JY. 2000. A field guide to the birds of Korea. LG Evergreen Foundation, Korea.
  29. Lee J, Lee J, Lee SH, Kim M, Lee E, Han A, Shim K. 2014. The characteristics of heavy metal accumulations in feral pigeon (Columba livia) feathers for environmental monitoring, J Environ Impact Assess. 23(6): 492-504. https://doi.org/10.14249/eia.2014.23.6.492
  30. Lewis SA, Becker PH, Furness RW. 1993. Mercury levels in eggs, tissues, and feathers of Herring Gulls Larus argentatua from the German Wadden sea coast. Environ Pollut. 80: 293-299. https://doi.org/10.1016/0269-7491(93)90051-O
  31. Luo W, Lu Y, Wang T. 2010. Ecological risk assessment of arsenic and metal in sediments of coastal areas of northern Bohai and Yellow Seas, China. AMBIO. 39: 367-375. https://doi.org/10.1007/s13280-010-0077-5
  32. Morera M. Sanpera C. Crespo S. Jover L. Ruiz X. 1997. Inter- and intra clutch variability in heavy metals and selenium levels in Audouin's Gull eggs from the Ebro Delta, Spain. Arch Environ Contam Toxicol. 33:71-75. https://doi.org/10.1007/s002449900225
  33. Morales L, Martrat MG, Olmos J, Parera J, Vicente J, Bertolero A, Abalos M, Lacorte S, Santos FJ, Abad E. 2012. Persistent organic pollutants in gull eggs of two species (Larus michahellis and Larus audouinii) from the Ebro delta Natural Park. Chemosphere. 88: 1306-1316. https://doi.org/10.1016/j.chemosphere.2012.03.106
  34. Nagel P, Smrekar G, Haag-Wackernagel D. 2001. Use of feral pigeon eggs for urban biomonitoring. Fresenius Environ Bul. 10(1): 18-25.
  35. Nam DH, Lee DP, Koo TH. 2001. Factors causing variations of lead and cadmium accumulation of feral pigeons (Columba livia). Korean J Orni. 8(2): 107-115.
  36. Nam DH, Lee DP, Koo TH. 2002. The use of feral pigeon's (Columba livia) feathers as a monitor for lead pollution in Korea. Korean J Environ Ecol. 16(3): 233-238.
  37. Nam DH, Lee DP, Koo TH. 2003. Comparison of lead and cadmium accumulations in feral pigeons (Columba livia) with different developmental stages from urban and industrial complex areas, Korean J Environ Biol. 21(2), 142-148.
  38. Nisianakis P, Giannenas I, Gavriil A, Kontopidis G, Kyriazakis I. 2009. Variation in trace element contents among chicken, turkey, duck, goose, and pigeon eggs analyzed by Inductively Coupled Plasma Mass Spectrometry (ICP-MS). Biol Trace Elem Res. 128: 62-71. https://doi.org/10.1007/s12011-008-8249-x
  39. Park JS, Jung SY, Son YJ, Choi SJ, Kim MS, Kim JG, Park SH, Lee SM, Chae YZ, Kim MY. 2017. Total mercury, methylmercury and ethylmercury in marine fish and marine fishery products sold in Seoul, Korea. Food Additives & Contaminants: Part B. 4(4): 268-274. https://doi.org/10.1080/19393210.2011.638087
  40. Parsons J. 1970. Relationship between egg size and post-hatching chick mortality in the Herring Gull (Larus argentatus). Nature. 228: 1221-1222. https://doi.org/10.1038/2281221a0
  41. Parsons J. 1976. Factors determining the number and size of eggs laid by the Herring Gull. The Condor. 78:481-492. https://doi.org/10.2307/1367097
  42. Paulus M, Bartel M, Klein R, Quack M, Tarricone K, Teubner D, Wagner G. 2010. Guideline for sampling and sample treatment, Herring Gull (Larus argentatus). version 2.0.3. Unweltprobenbank.
  43. Rajaei F, Esmaili SA, Bahramifar N, Ghasempouri SM, Savabieasfahani M. 2010. Mercury concentration in 3 species of gull Larus ridibundus, Larus minutus, Larus canus from south coast of the Caspian Sea, Iran. Bull Environ Contam Toxicol. 84(6): 716-719. https://doi.org/10.1007/s00128-010-9973-4
  44. Royle NJ, Surai PF, McCartney RJ, Speake BK. 1999. Parental investment and egg yolk lipid composition in gulls. Funct Ecol. 13:298-306. https://doi.org/10.1046/j.1365-2435.1999.00306.x
  45. Rudel H, Uhlig S, Weingartner M. 2008. Pulverisation and homogenisation of environmental samples by cryomilling. Fraunhofer Institute, Germany.
  46. Rudel H, Fliedner A, Kosters Jan. 2010. Twenty years of elemental analysis of marine biota within the German Environmental Specimen Bank-a thorough look at the data. Environ Sci Pollut Res. 17:1025-1034. https://doi.org/10.1007/s11356-009-0280-8
  47. Ruiz X, Jover L, Pedrocchi V, Oro D, Gonzalez-Solis J. 2000. How costly is clutch formation in the audouin's gull Larus audouinii? J of Avian Biol. 31: 567-575. https://doi.org/10.1034/j.1600-048X.2000.310416.x
  48. Sagerup K, Helgason LB, Polder A, Strom H, Josefsen TD, Skare JU, Gabrielsen GW. 2009. Persistent organic pollutants and mercury in dead and dying glaucous gulls (Larus hyperboreus) at Bjornoya (Svalbard). Sci of the Total Environ. 407: 6009-6016. https://doi.org/10.1016/j.scitotenv.2009.08.020
  49. Saino N, Romano M, Rubolini D, Caprioli M, Ambrosini R, Fasola M. 2010. Food supplementation affects egg albumen content and body size asymmetry among yellow-legged gull siblings. Behav Ecol Sociobiol. 64:1813-1812. https://doi.org/10.1007/s00265-010-0993-1
  50. Sanpera C, Morera M, Crespo S, Ruiz X, Jover L. 1997. Trace elements in clutches of Yellow-legged Gulls, Larus cachinnans, from the Medes Islands, Spain. Bull Environ Contam. Toxicol. 59:757-762. https://doi.org/10.1007/s001289900545
  51. Sanpera C, Morera M, Ruiz X, Jover L. 2000. Variability of mercury and selenium levels in clutches of Audouin's Gulls (Larus audouinii) breeding at the Chafarinas Islands, Southwest Mediterranean. Arch Environ Contam Toxicol. 39: 119-123.
  52. Salzer DW, Larkin GJ. 1990. Impact of courtship feeding on clutch and third-egg size in glaucous-winged gulls. Anim Behav. 39(6):1149-1162. https://doi.org/10.1016/S0003-3472(05)80787-0
  53. Shin JR, Kim JS, Koo TH. 2008. Lead and cadmium concentrations in Korean wild birds. Korean J Environ Biol. 26(1): 8-14.
  54. Szumilo E, Fila G, Szubska M, Meissner W, Beldowska M, Falkowska L. 2010. Distribution of total mercury in Herring Gull (Larus argentatus) from the vicinity of the Gulf of Gdansk, Poland. Oceanol and Hydrobiol Stud. 105-114.
  55. Won BO. 1981. Illustrated flora & fauna of Korea, vol. 25, avifauna. Ministry of Education.
  56. Yu JP, Chun BS, Kim IK, Kang JH. 2006. Hatching and livability of the Black-tailed Gull (Larus crassirostris) in relation to the egg size in Hongdo Island. Kor J Orni. 13(1): 21-26.
  57. Yoo JC, Kwon YS. 1997. Some aspects of laying, incubation and hatching in the Black-tailed Gull, Larus crassirostris. Kor J Orni. 4(1): 1-5.