J. ENVIRON. TOXICOL. Vol. 21, No. 3, 267~273 (2006) 유류에오염된아비류 (Loons) 의체내조직중필수원소농도 김상진, 이종남 1, 이두표 * 호남대학교생명과학과, 1 경성대학교조류관 Concentrations of Essential Metals in Tissues of Oiled Loons Sang-Jin Kim, Jong-Nam Lee 1 and Doo-Pyo Lee* Department of Biological Science, Honam University, Gwangju 506-714, Korea 1 Institute of Wild Bird, Kyungsung University, Busan 608-736, Korea ABSTRACT Concentrations of four essential metals (Fe, Cu, Mn and Zn) were determined in apparently oil-polluted dead or near-dead three loon species collected in the Busan coast, Korea. Fe, Cu, Mn and Zn concentrations were generally high in liver, and also, Mn and Zn were high in bone. There were significant differences in some tissue concentrations of Fe, Cu, Mn and Zn among three species, but did not show any consistent evidence of species-specific accumulation. Mean concentration of Fe was 11,635±4010 µg/g, Cu 64.3±30.7 µg/g, Mn 13.1±2.32 µg/g, and Zn 121±24.8 µg/g in liver of all three species examined. Mn and Zn levels in this study were similar to those of normal loons and other seabirds reported from different countries. However, Fe and Cu liver levels were extraordinarily higher than those of reported. This result suggests that unusual accumulations of essential metals such as Fe and Cu may partially arise from long-term starvation due to oil pollution. Key words : seabirds, essential metals, oil pollution, heavy metals 서 론 유류오염 (oil pollution) 은많은해양조류들에게악영향을미치는데특히아비류 (loons) 를포함한논병아리류 (grebes), 사다새류 (pelecaniforms), 바다오리류 (alcids) 등과같은잠수성해양조류들은생활사중많은시간을해수면과접하고있기때문에더큰피해를입고있다 (Piatt et al., 1990). 유류는다양한영향으로해양조류를사망케하는데, 그주요영향은깃털의방수능력을파괴시키 To whom correspondence should be addressed. Tel: +82-62-940-5434, Fax: +82-62-940-5434 E-mail: dplee@honam.ac.kr 는것이다. 유류가묻은해양조류는깃털의방수능력을회복시키기위해즉시깃다듬기를실시하지만, 이로인해유류의독성물질을흡입하게되어발달, 생식, 면역, 삼투조절및영양상태등의생리적인과정에서다양한병리적상태에놓이게된다 (Briggs et al., 1996). 유류가묻은조류의경우신장, 간및소화관에서의유류독성이주요사망원인이될수있다는보고가있다 (Leighton, 1991). 또한유류에오염된잠수성해양조류는잠수능력이약화되어먹이섭취부족으로인한굶주림으로사망할수있다. 조류에서중금속축적은노출된강도및기간, 그리고물질대사및생리기능과관련된여러요소들에의해좌우될뿐만아니라연령, 성별, 질병의 267
268 J. ENVIRON. TOXICOL. Vol. 21, No. 3 진행상태, 유류오염의유무등에의해서도영향을받는다고알려져있다 (Debacker et al., 2000). 특히필수원소는번식, 절식 (fasting), 성장단계및털갈이등의다양한생리작용에따라특이적인분포경향을나타낸다 (Honda et al., 1986a, b; 이두표, 1996). 또한단기간의절식또는기아 (starvation) 는미량필수무기질뿐만아니라특히 Zn 과 Cu 같은필수원소의운용 (mobilization) 및물질대사에영향을준다고알려져있으며이는바다오리류 Somateria mollissima (Norheim and Borch-Iohnsen, 1990), 흰눈썹바다오리 Uria aalge (Wenzel and Adelung, 1996) 등의야생조류에서입증되었다. 현재유류에오염된해양조류의중금속축적연구는여러나라에서많이진행되어왔지만유류오염과필수원소축적간의관계를이해하기위한활용가능한자료는미미한실정이다. 따라서본연구는부산연안지역에서수집한유류에오염된아비류를대상으로체내조직중필수원소농도를측정하고이들원소의축적과유류오염과의관계를파악하고자한다. 1. 연구대상 재료및방법 본연구대상조류는아비목 (Gaviformes) 아비과 (Gaviidae) 의아비 Gavia stellata, 회색머리아비 G. pacifica, 큰회색머리아비 G. arctica 의 3 종으로이들의생태학적특성은유사한편이다. 한국에도래하는아비류는주로시베리아북동부, 북극주변습지, 늪, 호수등지에서번식하며동해안과남해안일대연안및강하구등지에서월동한다 ( 원병오, 1981; Carboneras, 1992). 아비류는주로어식성으 로민물 ( 번식지 ) 에서는송어류 (Salmo trutta), 연어류 (Salmo salaris), 잉어과어류 (Rutilus rutilus) 등을먹으며, 바다 ( 월동지 ) 에서는대구류 (Gadus morhua, Melanogrammus aeglefinus), 청어류 (Clupea harengus, Sprattus sprattus), 민어과어류 (Merlangius merlangus) 등을먹는다. 또한수생무척추동물, 개구리, 갑각류 ( 새우류및게류 ) 및식물질을먹기도한다 (Carboneras, 1992). 분석한아비류는 1999 년부터 2003 년겨울동안부산근처해안가, 만 (bay) 및강하구에서수집하였다 (Table 1). 수집된개체는모두깃털에약간의유류가묻어있었으며사망직전이거나사망한상태였다. 사망직전의개체는수집후 2 일이내에모두사망하였다. 육안관찰결과수집된개체는모두가슴근육이위축된상태였고외상의흔적은발견되지않았으며사망원인은알수없었다. 시료는수집즉시폴리에틸린봉투에넣어중금속분석전까지 -20 C 에냉동보관하였다. 2. 중금속분석 필수원소인 Fe, Cu, Mn 및 Zn 분석을위해냉동된시료는상온에서해동시킨후해부하여간, 근육 ( 가슴근육 ), 신장그리고뼈 ( 대퇴부 ) 등의조직을추출하였다. 추출한조직은건조기에 80 C 로 12 시간동안항량이될때까지건조시켰다. 각조직을균질화하여시료 1~3g 를취하여황산, 질산, 과염소산을가하여가열분해한후분해액을 100 ml 로희석하여원자흡광광도계 (Shimadzu AA-6400) 로필수원소를측정하였다 (Lee et al., 1989). 3. 통계처리 모든통계처리는 SPSS-WIN version 12.0 프로그 Table 1. Basic data on loon samples analyzed Sampling date Species Winter Winter Winter Winter Total Sampling site 1999~00 2000~01 2001~02 2002~03 Red-throated loon Gavia stellata - 2 1 1 4 Pacific loon Busan (beach, 6 1 2-9 G. pacifica breakwater, estuary) Arctic loon G. arctica 1 3 2 6 12
September 2006 Kim et al. : 아비류의필수원소농도 269 램을이용하여일원배치분산분석 (one-way ANOVA) 을실시하였다. 통계학적유의성은 p=0.05 수준에서판정하였다. 조직의모든원소농도는 (µg/g) 건중량으로나타내었다. 결과및고찰 아비류체내조직중필수원소분석결과는 Table 2 에나타냈다. 아비류 3 종의 Fe 과 Cu 농도는간에서높고뼈에서낮았으며, Mn 과 Zn 은간과뼈에서높고근육에서낮아이들필수원소들은체내조직간축적특이성을보였다. 또한분석한체내조직중필수원소농도는 Fe 이가장높고, Zn, Cu, Mn 순으로나타났다. 아비류 3 종에서 Fe, Cu, Mn, Zn 의농도는일부조직에서통계학적으로종간에유의차가나타났지만 (Table 2) 그차이는개체의연령, 성별, 몸크기등에의한생물학적변동폭이내로 ( 이두표, 1995) 필수원소의종특이적축적현상은보이지않았다. 1. Fe 농도 아비류의체내조직중평균 Fe 농도는 393~ 12,914 µg/g 의범위로, 간조직 ( 평균 11,166~12,914 µg/g) 에서가장높고뼈조직 ( 평균 393~593 µg/g) 에서가장낮았다 (p 0.05, Table 2). 이러한경향은 Kim 등 (1996) 이보고한아비류및다른해양조류에서의조직분포패턴과비슷하였다. 일반적으로간조직중높은 Fe 농도는연령에따른미오글로빈 (myoglobin), 헤모글로빈 (hemoglobin) 의증가와페리틴 (ferritin) 또는헤모시데린 (hemosiderin) 같은 Fe 저장단백질에기인한다 (Underwood, 1971). 아비류 3 종의간조직중평균 Fe 농도는 11,653 ±4,010 µg/g 로번식지인러시아지역에서채집된아비및큰회색머리아비 ( 정상개체 ) 보다약 5 배이상높았고, 다른잠수성해양조류인바다오리과 (Alcidae) 및가마우지과 (Phalacrocoracidae) 조류의농도보다약 10 배이상높게나타났다. 그러나미국 Michigan 지역에서수집한사망하거나또는병들거나사망직전인북방아비 (Gavia immer) 의평균농도보다는약 4 배높았으나농도범위를보면그중일부시료는본연구의농도에필적하는높은농도를보였다 (Table 3). 이와같이약간의유류에오염되어사망직전인본연구의시료와질병으로사망직전인 Michigan 지역의일부시료에서모두간조직중 Fe 농도가특이하게높은것을알 Table 2. Concentrations (mean±sd and range in parenthesis, µg/g dry wt) of essential metals in the liver, muscle, kidney and bone of loons Tissues Liver Muscle Kidney Bone Metals Red-throated loon Pacific loon Arctic loon Gavia stellata (n=4) Gavia pacifica (n=9) Gavia arctica (n=12) Fe 12,914±4,587 (9,232~18,907) 11,691±4,764 (5,296~19,881) 11,166±3,463 (4,663~15,729) Cu 60.4±13.1 (47.3~75.3) 62.1±29.8 (15.6~115) 67.3±36.3 (28.4~139) Mn 11.6±1.70 (9.10~12.7) 12.9±2.75 (9.35~17.2) 13.7±2.05 (10.5~17.3) Zn 106±21.1 (82.8~133) 112±20.6 (74.8~137) 134±24.2 (111~186) Fe 1,591±373 (1,052~1,892) 1,177±484 (596~1,877) 1,508±689 (811~3,246) Cu 55.6±10.1 a (42.4~65.7) 32.7±15.9 b (11.9~65.1) 36.7±10.7 ab (19.2~51.9) Mn 1.50±0.54 ab (0.77~2.07) 1.25±0.23 b (0.89~1.57) 2.54±1.36 a (1.28~6.43) Zn 85.4±8.81 (73.6~92.4) 73.1±20.8 (35.0~98.8) 81.6±27.5 (44.6~132) Fe 1,274±324 (946~1,171) 1,264±431 (628~1,911) 1,187±234 (853~1,592) Cu 30.0±6.71 (21.1~37.3) 25.2±10.1 (8.48~39.7) 19.5±12.6 (10.4~55.2) Mn 9.85±1.13 (9.03~11.4) 8.53±6.64 (3.68~21.5) 5.74±1.13 (4.49~8.12) Zn 93.8±13.3 (74.2~103) 96.5±26.9 (65.6~148) 93.0±29.1 (65.5~155) Fe 593±143 a (474~799) 393±67.4 b (291~487) 437±107 b (307~619) Cu 3.10±0.64 ab (2.30~3.85) 3.89±0.72 a (2.75~4.67) 2.43±0.57 b (1.46~3.15) Mn 9.46±1.21 b (9.03~11.5) 11.4±2.54 ab (8.08~15.9) 14.5±2.95 a (7.70~18.6) Zn 137±9.13 a (128~146) 96.5±26.9 b (64.8~130) 108±15.6 b (77.5~133) ab For each species, means followed by different letters are significantly different (p 0.05)
Table 3. Concentrations (mean±sd and range in parenthesis, µg/g dry wt) of essential metals in the liver of loons and seabirds in different areas Family Species N Fe Cu Mn Zn Sampling area, year References Gaviidae Three species of loons 25 O 11,635±4,010 64.3±30.7 13.1±2.32 121±24.8 (4,663~19,881) (15.6~139) (9.10~17.3) (74.8~186) Busan coast, Korea, 1999~2003 This study Red-throated loon Gavia stellata 1 NO 2,203 18.9 17.9 123 Northeast Siberia, Russia, 1993 Kim et al., 1996 Arctic loon G. arctica 1 NO 627 12 20.9 133 Northeast Siberia, Russia, 1993 Kim et al., 1996 Common loon 1) 2,947 60.3 40.8 154 54 U G. immer (192~20,923) (36.9~1,042) (30.2~57.9) (72.9~577) Michigan, USA, 1988~1993 O Brien et al., 1995 Alcidae Ancient murrelet Elliott and 9 NO 519±205 25.4±4.21 9.76±1.58 120±48.2 Canadian Pacific coast, 1990 Synthliboramphus antiquus Scheuhammer, 1997 Ancient murrelet 1) S. antiquus 7 NO 801±176.1 18.0±1.98 9.03±1.14 86.7±11.5 North Pacific Ocean, 1986 Honda et al., 1990 Rhinoceros auklet Elliott and Scheuhammer, 9 NO 1,033±266 22.2±2.57 11.6±1.35 111±16.6 Canadian Pacific coast, 1990 Cerorhinca monocerata 1997 Common guilemot 1) Uria aalge 6 NO 846±238 16.2±1.44 8.25±1.29 68.4±4.74 North Pacific Ocean, 1986 Honda et al., 1990 Common guilemot 1.54±0.87 73.3±12.7) 30 O U. aalge (0.26~4.12) (26.7~100 Galician coast, 2002~2003 Pérez-López et al., 2006 Atlantic puffin 1.01±0.63 27.0±8.2 24 O Fratercula arctica (0.29~2.15) (14.9~40.2) Galician coast, 2002~2003 Pérez-López et al., 2006 Razorbill 0.99±0.69 39.4±15.5 43 O Alca torda (ND~3.23) (17.2~48.6) Galician coast, 2002~2003 Pérez-López et al., 2006 Phalacrocoracidae Olivaceous cormorant Southeast gulf of california, Ruelas-Inzunza and 6 NO 1,098±311 20.3±3.0 11±1.8 98±18 Phalacrocorax olivaceus 2000 Péez-Oóuna, 2004 Great cormorant Lake Biwa and Mie, Japan, 4 NO 36.5±1.1 19.0±0.48 166±4 P. carbo 2003 Nam et al., 2005 Temminck s cormorant 1) P. capillatus 2 NO 993 16.47 15.4 76.8 Sea of East, 1987 Honda et al., 1990 O: oiled, NO: non-oiled, U: unknown. 1) Originally reported as ppm on a wet weight basis and converted as dry weight basis with conversion factor 3.0. 270 J. ENVIRON. TOXICOL. Vol. 21, No. 3
September 2006 Kim et al. : 아비류의필수원소농도 271 수있다. 이두경우모두수집전까지기아가장기간지속되었다는공통점이있는것으로보아장기간의기아가체내에서의 Fe 대사및축적에영향을미칠수있다는사실을암시해준다. 2. Cu 농도 아비류 3 종의체내조직중평균 Cu 농도는 2.43~67.3 µg/g 의범위로, 연조직인간조직 ( 평균 60.4~67.3 µg/g) 에서가장높고경조직인뼈조직 ( 평균 2.43~3.89 µg/g) 에서가장낮게나타났다 (p 0.05, Table 2). 간은 Fe 와마찬가지로 Cu 의저장고로서역할을하는데본연구의조직분포경향은다른해양조류의경향과비슷하였다 (Kim et al., 1998). 아비류 3 종의간조직중평균 Cu 농도는 64.3± 30.7 µg/g (15.6~139 µg/g) 로미국 Michigan 지역에서사망하거나또는병들거나사망직전인북방아비의농도와큰차이가없었으나정상적인러시아의아비와큰회색머리아비농도보다는약 3~5 배정도높게나타났다. 그리고잠수성해양조류인바다오리과및가마우지과조류의평균농도보다약 2~3 배정도높은경향을보였다 (Table 3). 이와같이간조직중높은 Cu 농도는 Fe 와마찬가지로장기간에걸친기아로인한체내 Cu 대사이상에의한것으로사료된다. 3. Mn 농도 아비류의체내조직중평균 Mn 농도는 1.25~ 67.3 µg/g 의범위로, 간 ( 평균 11.6~13.7 µg/g) 과뼈조직 ( 평균 9.46~14.5 µg/g) 에서높고근육조직 ( 평균 1.25~2.54 µg/g) 에서가장낮은경향을보였다 (p 0.05, Table 2). 이러한경향은 Kim 등 (1996) 이보고한아비류의분포패턴과비슷하며, Klasing (1998) 의조류에서 Mn 은뼈, 간, 췌장및신장조직이가장활동적으로흡수하는조직으로높은축적이일어난다는보고와도일치하였다. 아비류 3 종의간조직중평균 Mn 농도는 13.1 ±2.32 µg/g 로미국 Michigan 지역에서수집한북방아비의농도보다는낮았지만큰차이는보이지않았다. 또한러시아에서수집한정상적인아비와큰회색머리아비의농도와비슷하였으며, 다른해양조류인바다오리과및가마우지과조류들의농도와 도큰차이가없었다 (Table 3). 해양조류에서활용할수있는 Mn 의농도에대한정보는부족한편이다. 현재 Mn 은미국및캐나다등의나라에서휘발류 (gasoline) 에 Pb 대신에첨가제로사용되고있으며 (Cooper, 1984), 멕시코 Culiacán 계곡의집약적인농경지에서살균제로서이용되고있는데 (Páez-Osuna et al., 1993) 이러한이유로환경중의 Mn 농도는주의깊게고려되고있다. 따라서다른국가들로이들의사용이확장되기전에기초자료를확보하는면에서본아비류의 Mn 농도는중요할것이라고사료된다. 4. Zn 농도 아비류의조직중평균 Zn 농도는 73.1~137 µg/g 의범위로, 간 ( 평균 106~134 µg/g), 뼈 ( 평균 96.5~137 µg/g), 신장 ( 평균 93.0~96.5 µg/g) 이근육조직 ( 평균 73.1~85.4 µg/g) 보다높은경향을보였다 (p 0.05, Table 2). 이러한경향은 Kim 등 (1996) 의러시아지역아비류의간에서가장높고근육에서가장낮은축적경향과일치하였다. 일반적으로 Zn 은연조직인근육, 간장, 신장보다경조직인뼈나깃털등에높게축적되는조직특이성을보인다고알려져있으나본연구에서 Zn 농도는연조직과경조직간의축적차이는없었다. 아비류간조직중평균 Zn 농도는 121±24.8 µg/g 로러시아및미국 Michigan 지역에서수집한아비류의농도와비슷한수준이었다. 또한해양조류인바다오리과및가마우지과조류들의농도와도큰차이를보이지않았다 (Table 3). 5. 유류오염과필수원소축적과의관계 분석한유류에오염된아비류의간조직중필수원소농도는보고된정상적인아비류와잠수성해양조류의농도보다 Fe 농도는약 5~10 배, Cu 농도는약 2~5 배정도높게나타났으나, Mn 과 Zn 의농도는큰차이를보이지않았다. 간조직중의 Fe 농도는조류의성장단계와절식에의해변동하며, 그생물학적변동폭은약 2 배정도로알려져있다 ( 이두표, 1995). 그예로중대백로 (Egretta alba modesta) 성조의간조직중 Fe 축적레벨은유조에비해낮고 (Honda et al., 1986a), 남극의펭귄 (Pygoscelis adeliae) 에서는절식의진
272 J. ENVIRON. TOXICOL. Vol. 21, No. 3 행과함께농도가상승한다는보고가있다 (Honda et al., 1986b). 또한 Hunt 등 (1981) 은잠수성해양조류인바다오리류의경우산소를저장해야하기때문에 Fe 결합단백질인미오글로빈을많이함유하고있을것으로보았다. 간조직중 Cu 농도는메탈로티오네인 (metallothionein) 에의해물질대사적으로제어된다고알려져있다 (Anan et al., 2001). 그러나 Parker 와 Holm (1990) 은산란기간동안바다오리류 (Somateria mollissima) 의간무게는 63% 감소하며, 산란초기에서부화기까지체중의 46%, 간무게의 27% 가더감소한다고하였는데, Savinov 등 (2003) 은이러한절식으로인해바다오리류의간조직중농도가증가할수도있다고하였다. 그러나본연구의 Fe 과 Cu 농도는이러한생물학적변동에의한축적보다는유류오염으로인한취식행동감소로장기간의절식및기아, 질병등의불리한생리적조건으로고농도축적이일어난것으로사료된다. Pérez-López 등 (2005) 은해양조류의조직내 Cu, Zn 의농도는유류에오염된개체와그렇지않은같은개체를비교했을때농도는비슷하거나낮은것으로유류오염으로인한농도차이는크지않다고하였다. Nybø 등 (1996) 의보고에의하면 Zn 은항상성에의해조절되는데, 그메커니즘은초과된 Zn 의유입은내장 (gut) 으로배출을증가시키거나흡수를감소시켜 Zn 의축적이더이상증가하지않는다고하였다. 또한대부분수생무척추동물 ( 아비류의먹이 ) 의 Zn 농도는환경중의농도에의존하는데수생무척추동물도체내 Zn 농도를조절할수있다고하였다 (White and Rainbow, 1982; Devineau and Amiard-triquet, 1985). 따라서보고된농도와큰차이를보이지않은아비류의 Zn 농도는항상성에의해조절되는것으로보이며, 또한환경중에서 Zn 의양이증가하여도먹이생물과아비류개체양쪽에서조절되어일정농도이상으로 Zn 이축적되지않는것으로사료된다. 그러나 Saeki 등 (1999) 은유류에함유된 vanadium 이물범류에있어서 Fe, Cu 같은원소와양의상관관계가있다고하였다. 또한 Wenzel 와 Adelung (1996) 은유류가묻은동물의영양상태는특히 Cu, Zn 같은중금속농도에영향을준다고하였으며, Debacker 등 (2000) 은간과신장조직중필수원소농도는질병의진행상태와직접적인관 련이있다고하였는데, 유류의유무는 Fe 의축적에영향을주지만 Cu, Zn 은큰영향이없다고하였다. 이와같이대부분의연구결과는유류오염은필수원소의농도에큰영향을미치지않는다고하였으나이는대형유조선사고등으로인한다량의유류에해양조류가노출되어곧바로사망했을경우에해당되며, 본연구의시료처럼약간의유류가깃털에묻어있어장기간경과후기아로사망하는경우와는차이가있는것으로판단된다. 따라서본연구의조직중 Fe 및 Cu 의특이적으로높은농도는약간의유류오염으로인한장기간에걸친기아의영향으로생각되지만, 정확한원인을파악하기위해서는앞으로유류오염과필수원소축적간의관계에대한연구가더필요할것으로사료된다. 참고문헌 원병오. 한국동식물도감제 25 권동물편 ( 조류생태 ), 삼화서적주식회사 1981; 684-686. 이두표. 조류의조직중중금속축적레벨의종간차에관한연구, 호남대학교산업기술연구논문집 1995; 2: 165-176. 이두표. 조류의조직중중금속레벨의상관관계에관한연구, 경희대학교조연보 1996; 5(1): 59-67. Anan Y, Kunito T, Watanabe I, Sakai H and Tanabe S. Trace element accumulation in hawksbill turtle (Eretmochelys imbricate) and green turtle (Chelonia mydas) from Yaeyama Islands, Japan, Environ Toxicol Chem 2001; 20: 2802-2817. Briggs KT, Yoshida SH and Gershwin ME. The influence of petrochemicals and stress on the immune system of seabirds, Reg Toxicol Pharmacol 1996; 23: 145-155. Carboneras C. Family Gaviidae (Loons). In: Hoyo J, Elliott A and Sargatal J (eds), Handbook of the birds of the world, Vol. 1. Lynx Edicions, Barcelona 1992; 162-172. Cooper WC. The health implications of increased manganes in the environment resulting from the combustion of fuel additives: a review of the literature, J Toxicol Environ Health 1984; 14: 23-46. Debacker V, Jauniaux T, Coignoul F and Bouquegneau JM. Heavy metals contamination and body condition of wintering guillemots (Uria aalge) at the Belgian coast from 1993 to 1998, Environ Res Section A 2000; 84: 310-317. Devineau J. and Amiard-triquet C. Patterns of bioaccumulation of an essential trace element (zinc) and a pollutant
September 2006 Kim et al. : 아비류의필수원소농도 273 (cadmium) in larvae of the prawn Palaemon serratus, Mar Biol 1985; 86: 139-143. Elliott JE and Scheuhammer AM. Heavy metal and metallothionein concentrations in seabirds from the pacific coast of Canada, Marine Pollution Bulletin 1997; 34(10): 794-801. Honda K, Marcovecchio JE, Kan S, Tatsukawa R and Ogi H. Metal concentrations in pelagic seabirds from the north pacific ocean, Arch Environ Contam Toxicol 1990; 19: 704-711. Honda K, Nin BY and Tatsukawa R. Organ and tissue distribution of heavy metals, and age-related changes in the eastern great white great, Egretta alba modesta, in Korea, Arch Environ Contam Toxicol 1986a; 15: 185-197. Honda K, Yamamoto Y, Hidaka H and Tatsukawa R. Heavy metal accumulation in adelie penguin, Pygoscelis adaliae, and their variations with the reproduction processes, Mem Natl Inst Polar Res Spec Issue 1986b; 40: 443-453. Hunt Jr GL, Burgeson B and Sanger GA. Feeding ecology of seabirds in the eastern Bering Sea. In: Hood DW and Calderv JA (eds), The eastern Bering Sea shelf: Oceanography and Resources (Vol. 2), University of Washington Press, Seattle, WA, 1981; 629-648. Kim EY, Goto R, Tanabe S, Tanaka H and Tatsukawa R. Distribution of 14 elements in tissues and organs of oceanic seabirds, Arch Environ Contam Toxicol 1998; 35: 638-645. Kim EY, Ichihashi H, Saeki K, Atrashevich G, Tanabe S and Tatsukawa R. Metal accumulation in tissues of seabirds from Chaun, northeast Siberia, Russia, Environ Pollut 1996; 92: 247-252. Klasing KC. Comparative avian nutrition, Cambridge University Press 1998; 234-276. Lee DP, Honda K, Tatsukawa R and Woo PO. Distribution and residue level of mercury, cadmium and lead in Korean birds, Bull Environ Contam Toxical 1989; 43: 550-555. Leighton FA. The toxicity of petroleum oils to birds: an overview. In: White J and Frink L (eds), The effects of oil on wildlife: research, rehabilitation and general concerns, The Effets of Oil on Wildlife 1991; 43-57. Nam DH, Anan Y, Ikemoto T, Okabe Y, Kim EY, Subramanian A, Saeki K and Tanabe S. Specific accumulation of 20 trace elements in great cormorants (Phalacrocorax carbo) from Japan, Environ Pollut 2005; 134: 503-514. Norheim G. and Borch-Iohnsen B. Svalbard: trace elements in liver from eider. In: Låg J (eds), Excess and deficiency of trace elements in relation to human and animal health in arctic and subarctic regions, The Norwegian Academy of Sciences and Letters 1990; 217-219. Nybø S, Fjeld PE, Jerstad K and Nissen A. Long-range air pollution and its impact on heavy metal accumulation in dippers Cinclus cinclus in Norway, Environ Pollut 1996; 94(1): 31-38. O Brien DJ, Poppenga RH and Ramm CW. An exploratory analysis of liver element relationships in a case series of common loons (Gavia immer), Prev Vet Med 1995; 25: 37-49. Páez-Osuna F, Osuna-López JI, Izaguirre-Fierro G, Zazueta- Padilla H. Heavy metals in oysters from a subtropical coastal lagoon associated with an agricultural drainage basin, Bull Environ Contam Toxicol 1993; 50: 696-702. Parker H and Holm H. Patterns of nutrient and energy expenditure female common eiders nesting in the High Arctic, The Auk 1990; 107: 660-668. Pérez-López M, Cid F, Orpesa AL, Fidalgo LE, Beceiro AL and Soler F. Heavy metal and arsenic content in seabirds affected by the Prestige oil spill on the Galician coast (NW Spain), Sci Total 2006; 209-220. Piatt JF, Carter HR and Nettleship DN. Effects of oil pollution on marine bird population, The oil symposium Herndon Virginia 1990; 125-141. Ruelas-Inzunza J and Páez-Osuna F. Trace metals in tissues of resident and migratory birds from a lagoon associated with an agricultural drainage basin (SE Gulf of California), Arch Environ Contam Toxicol 2004; 47: 117-125. Saeki K, Nakajima M, Noda K, Loughlin TR, Baba N, Kiyata M, Tatsukawa R and Calkins DG. Vanadium accumulation in pinnipeds, Arch Environ Contam Toxicol 1999; 36: 81-86. Savinov VM, Gabrielsen GW and Savinova TN. Cadmium, zinc, copper, arsenic, selenium and mercury in seabirds from the Barents Sea: levels, inter-specific and geographical differences, Sci Total Environ 2003; 306: 133-158. Underwood EJ. Trace elements in human and animal nutrition (3rd ed.), Academic press Inc 1971. Wenzel C. and Adelung D. The suitability of oiled guillemots (Uria aalga) as monitoring organisms geographical comparisons of trace element contaminants, Arch Environ Contam Toxicol 1996; 31(3): 358-377. White SL. and Rainbow PS. Regulation and accumulation of copper, zinc and cadmium by the shrimp Palaemon elegans, Mar Ecol Prog Ser 1982; 8: 95-101.