이사천에서채집된피라미, Zacco platypus 의생식과기관계구조이상 진영국, 신순호 1, 이제봉, 이재우, 안철민 2, 이정식 J. ENVIRON. TOXICOL. Vol. 21, No. 1, 35~43 (2006) 전남대학교수산해양대학수산생명의학과, 1 진남여자중학교, 2 국립수산과학원 Abnormality of Reproduction and Organ Structure of the Pale Chub, Zacco platypus from Isa Stream Young Guk Jin, Soon Ho Shin 1, Jae Bong Lee, Jae Woo Lee, Cheul Min An 2 and Jung Sick Lee Department of Aqualife Medicine, College of Fisheries and Ocean Science, Chonnam National University, Yeosu 550-749, Korea 1 Jinnam Girls Middle School, Yeosu 550-240, Korea 2 National Fisheries Research and Development Institute, Busan 619-900, Korea Reproduction and organ structure of the pale chub, Zacco platypus in Isa stream were investigated by means of histological methods. The results of the study confirmed reproductive abnormality and histopathological features in the pale chub. The gonadosomatic index (GSI) of the fish showed two peak in April and August. In summer season, GSI of the male was about two times of the female s GSI. Monthly variation of the gonadal development was very irregular. From the histological analysis of the organ structure, epidermal atrophy, necrosis and hyperplasia of pigment cell were observed in the skin. Epithelial layer lifting and clubbing of the lamella and bifurcation of the filament were observed in the gill. Also histological changes as congestion, cytoplasmic degeneration of hepatic cell, degeneration of bile duct, glomerular dilatation, degeneration of renal tubule and pycnosis of interstitial cell were identified in the liver and kidney, respectively. Key words : Zacco platypus, reproductive abnormality, histological degenerations, Isa stream 서 론 하천과바다로유입되는생활하수를비롯한각종오염물질들은비록저농도일지라도그곳에서식하는많은생물들에게치명적인영향을주고있으며 (Capel et al., 1988; Crisp, 1989; Paalman and Van der Weijden, 1992; Kim and Lee, 2000), 이로 Corresponding author. Tel: +82-61-659-3172, E-mail: ljs@chonnam.ac.kr 인해받는스트레스는다른생물학적요인에보다쉽게감염될수있는위험성을제공한다 (Kim et al., 2002). 특히, 담수생태계의상당부분차지하는하천은어류의생활에필요한모든요소들을포함하고있기때문에유해물질의노출시직접적인영향을받는다. 담수생태계의오염에의한서식생물체의생식과기관계구조의이상에관해서는 Filand 4 곳의호수에서식하는 perch, Perca fluviatilis 와 roach, Rutilus rurilus 의아가미구조의이상 (Haaparanta et al., 1997), Mississippi river 에서식하는 shovelnose 35
36 J. ENVIRON. TOXICOL. Vol. 21, No. 1 sturgeon, Scaphirhynchus platyorynchus 의 intersex (Harshbarger et al., 2000) 그리고국내만경강오염수에서식하는붕어, Carassius auratus 아가미와신장의비정상적인조직 (Kim et al., 2002) 을비롯하여최근에다수의연구들이보고되고있다. 피라미, Zacco platypus 는몸이옆으로납작하고길며, 주둥이는짧고끝은뾰족하다. 하천중류의여울에서주로서식하며부착조류를주먹이로하고있다. 산란기는 5~7 월로이시기의수컷은눈의아래쪽에추성이나타나며, 뒷지느러미의앞쪽몇개의기조가다른기조보다현저히길어지고, 주로붉은색의체색을나타낸다 (Kim and Kang, 1993). 본연구는전라남도순천시상사댐의지류인이사천에서식하는피라미에서생식과기관계구조의이상이확인되어이결과를보고하고자한다. Table 1. Number of specimens and sex ratio of the pale chub, Zacco platypus Collection date Number of Sex ratio specimens (female/male) (female/male) Dec. 7, 2001 38 (23/15) 1 : 0.65 Jan. 7, 2002 34 (20/14) 1 : 0.70 Feb. 3, 2002 35 (16/19) 1 : 1.19 Mar. 4, 2002 38 (19/19) 1 : 1.00 Apr. 8, 2002 27 (17/10) 1 : 0.59 May 5, 2002 37 (12/25) 1 : 0.95 June 9, 2002 26 (9/17) 1 : 1.89 July 10, 2002 37 (12/25) 1 : 2.08 Aug. 6, 2002 40 (17/23) 1 : 1.35 Sep. 8, 2002 29 (14/15) 1 : 1.07 Oct. 6, 2002 20 (5/15) 1 : 3.00 Nov. 10, 2002 10 (3/7) 1 : 2.33 Total 371 (174/197) 1 : 1.13 2. 방법 1. 재료 재료및방법 본연구에사용된피라미, Zacco platypus 는 2001 년 12 월부터 2002 년 11 월까지전남순천시상사호하류이사천의역조정지댐하류에서통발등을사용하여매월채집하였다 (Fig. 1). 분석에사용된개체수는 Table 1 에나타낸바와같이 371 개체였다. 1) 측정및조직학적방법채집된재료는현장에서 10% 중성포르말린에고정후실험실로옮겨전장및체중을각각 0.1 mm, 0.1 g 까지측정하였다. 그후생식소와간의무게를 0.01 g 까지측정한다음, Bouin 용액에고정후파라핀절편법에의해 4~6 µm 두께로연속절편을제작하였다. 표본은 Mayer s hematoxylin-0.5% eosin (H-E) 비교염색, Mallory 삼중염색, PAS 반응과 AB-PAS(pH 2.5) 반응을실시하였다. 2) 생식지수생식소중량지수 (gonadosomatic index: GSI) 는성어를대상으로 생식소무게 100/ 순체중 의식으로구하였다. 간중량지수 (hepatosomatic index: HSI) 는성어를대상으로 간무게 100/ 순체중 의식으로구하였다. Fig. 1. Sampling area of the pale chub, Zacco platypus. 3) 생식소발달단계생식소발달단계는 Fig. 2 와 3 에나타낸바와같이암 수각각의생식세포발달단계를기준으로암컷은성장기 (growing stage), 성숙및완숙기 (maturation and ripe stage), 산란및회복기 (spent and recovery stage) 그리고휴지기 (resting stage) 의 4 단계로나누었고, 수컷은 5 단계로성장기 (growing stage), 성숙기 (maturation stage), 완숙기 (ripe stage),
March 2006 Jin et al. : 피라미의생식과기관계구조이상 37 100 µm A B C 100 µm 100 µm D E F 250 µm 250 µm 100 µm Fig. 2. Ovarian development of the pale chub, Zacco platypus. A: Oogonial and previtellogenic stage. H-E stain. B: Early vitellogenic stage. Note the small yolk vesicle and follicle layer (Fl). H-E stain. C: Early active vitellogenic stage. H- E stain. D: Late active vitellogenic stage. Note the eosinophilic yolk globules. H-E stain. E: Mature and ripe stage. Note the germinal vesicle breakdown, numerous eosinophilic yolk globules and well developed zona radiata (Zr). H- E stain. F: Section of after spawning showing the degenerating oocytes and atretic follicles. H-E stain. N: nucleus, No: nucleolus, Og: oogonium, Op: ooplasm. A B C 100 µm 50µm 100 µm D E F 100 µm 50µm 100 µm Fig. 3. Testicular development of the pale chub, Zacco platypus. A: Section of testicular tissue showing the testicular lobules (Tl) and testicular cysts (Tc). H-E stain. B: Section of the resting stage showing the spermatogonia (Sg). H-E stain. C: Growing stage. Note the spermatocytes (Sc). H-E stain. D: Mature stage. Note the numerous spermatids (Sd) and spermatozoa (Sz). H-E stain. E: Ripe stage. Note the basophilic spermatozoa. H-E stain. F: Spent and recovery stage. Note the undischarged spermatozoa (Uds). H-E stain.
38 J. ENVIRON. TOXICOL. Vol. 21, No. 1 방정및회복기 (spent and recovery stage) 그리고휴지기 (resting stage) 로구분하였다. 1. 생식 결 과 1) 생식소의형태및내부구조난소는한쌍의둥근삼각형의낭상형으로난소내부는다수의난소소엽으로구성되어있었다 (Fig. 2, A). 정소는한쌍의긴둥근삼각형으로정소내부의조직상은다수의정소소엽으로구성되며, 각소엽은다수의정소소낭을가지고있었다 (Fig. 3, A). 2) 성비채집된개체들의암 수성비는채집시기별로다소차이는있었으나, 전체개체수에서는 1 : 1.13 으로나타났다 (Table 1). GSI 3) 생식소중량지수 (GSI) 의월변화 2001 년 12 월부터 2002 년 11 월까지조사된 GSI 5.0 4.0 3.0 2.0 1.0 0.0 Dec. Jan. Feb. Mar. Apr. May Month Female Male June July Aug. Sep. Oct. Nov. Fig. 4. Monthly variation of gonadosomatic index (GSI) of the pale chub, Zacco platypus. 의월변화는 Fig. 4 에서보는바와같다. 암컷의 GSI 는 4 월과 8 월에각각 2.83 과 2.05 로두번의정점을나타냈으며, 그이외에는약 1.5 내외로낮은값을나타냈다. 수컷의 GSI 는 8 월에 4.35 로가장높은값을나타냈는데, 7 월부터 9 월까지의수컷의 GSI 는같은시기의암컷 GSI 에비해약두배에해당하는수치였다. 이시기를제외한다른시기에수컷 GSI 는약 0.7 내외의낮은값을보였다. 4) 간중량지수 (HSI) 의월변화 Fig. 5 에나타낸것과같이암 수의 HSI 는약 2.0 내외로증가와감소를반복하는불규칙한양상을보였다. 5) 계절별생식소발달단계의변화암 수계절별생식소발달단계는생식소조직상의월변화를기초로암컷은 4 단계 (Fig. 2), 수컷은 5 단계 (Fig. 3) 로구분하여 Fig. 6 과 7 에월별출현빈도를나타내었다. Frequency (%) 100 80 60 40 20 0 Dec. Jan. Feb. Mar. Apr. May Growing Spent and recovery Month June July Aug. Sep. Mature and ripe Resting Oct. Nov. Fig. 6. Monthly variation of frequency of ovarian development stage of the pale chub, Zacco platypus. HSI 5.0 4.0 3.0 2.0 1.0 0.0 Dec. Jan. Feb. Mar. Apr. May Month Female Male June July Aug. Sep. Oct. Nov. Fig. 5. Monthly variation of hepatosomatic index (HSI) of the pale chub, Zacco platypus. Frequency (%) 100 80 60 40 20 0 Dec. Jan. Feb. Mar. Apr. May Month June July Aug. Sep. Oct. Growing Mature Ripe Spent and recovery Resting Nov. Fig. 7. Monthly variation of frequency of testicular development stage of the pale chub, Zacco platypus.
March 2006 Jin et al. : 피라미의생식과기관계구조이상 39 (1) 봄 2002 년 3 월부터 5 월사이로암컷은 GSI 가 1.32~2.83 이었다. 난소의발달단계는 3 월에휴지기로주로난원세포및난황형성전단계의난모세포들이관찰되었으며, 일부에서는성숙및완숙기의조직상이관찰되었다. 4 월에는성장기가약 65%, 휴지기와성숙및완숙기의조직상을가지는개체들이약 17.5% 를나타냈다. 5 월에는성장기의조직상을가지는개체들이 50%, 휴지기 33.3%, 방출및회복기가 16.7% 로나타났으며, 성숙및완숙기의조직상을가지는개체는나타나지않았다. 수컷은 GSI 가 0.61~1.45 로나타났다. 이시기에정소조직상은주로간기의정원세포들과간충조직이풍부한휴지기를나타냈으며 (Fig. 3, B), 성숙기와완숙기의발달단계를가지는개체들은관찰되지않았다. (2) 여름 2002 년 6 월부터 8 월사이로암컷의 GSI 는 1.13~2.05 였다. 6 월과 7 월의난소조직상은성장기가주를이루었다. 8 월에는산란및회복기가 41.18% 로이때난소조직상에서는산란전단계의난모세포들과폐쇄여포및난황형성개시기이후난모세포들의퇴화 흡수가관찰되었다 (Fig. 2, F). 수컷의 GSI 는 0.89~4.35 로연중가장높은값을나타냈다. 6 월에는휴지기의정소조직상을가지는개체들의비율이 81.25% 를차지하였다. 7 월에는휴지기가 40% 로나타났으며, 8 월에는완숙기 (35%) 를비롯한모든발달단계가관찰되었다. (3) 가을 2002 년 9 월부터 11 월사이로암컷은 GSI 가 1.27~1.87 이었다. 9 월에는주로성장기가나타났고, 10 월에는휴지기와성장기가각각 40% 를차지하였으며, 성숙및완숙기의난소를가지는개체들이 20% 로나타났다. 11 월에는방출및회복기가 33.3%, 휴지기의난소를가지는개체들은 66.7% 로조사되었다. 수컷의 GSI 는 2.70~1.35 이었다. 9 월은방정및회복기의정소를가지는개체들이약 70% 였으며, 10 월과 11 월에는휴지기의정소를가지는개체들의비율이높았다. (4) 겨울 2001 년 12 월부터 2002 년 2 월사이로암컷의 GSI 는 1.02~1.51 이었다. 이시기에는휴지기의난소를가지는개체들의비율이높았으나 2003 년 2 월에는성장기와성숙및완숙기의난소를가지는개체들이각각 12.50% 로나타났다. 수컷의 GSI 는 0.39~0.82 로가장낮은값을나타냈다. 2001 년에 12 월과 2002 년 1 월에는조사된모든개체들이휴지기의정소를가지고있었으며, 2002 년 2 월은휴지기 (82%) 와분열증식중인정원세포들과정모세포들이주를이루고있는성장기 (17%) 의정소를가지는개체들이관찰되었다. 2. 기관계 피라미의피부계는일반경골어류와같이외부로부터상피층과진피층으로이루어져있었다. 상피층은지지세포와선세포들로구성되어있었고, 진피층은기저막에인접한소수의색소세포와결합조직층으로구성되어있었다. 선세포는타원형의점액세포와곤봉상세포로구성되었다. 2002 년 1 월에채집한개체들의피부에서는상피층의괴사및분비세포의붕괴그리고선세포들의위축이나타났으며 (Fig. 8, A), 상피층의표면세포들의탈락과상피층에색소세포의증식이관찰되었다 (Fig. 8, B). 그리고 2002 년 4 월에채집한개체중일부에서점액세포의위축과곤봉상세포의변형이관찰되었으며, 일부개체의피부상피층에서는점액세포의활성과곤봉상세포의위축이발견되었다. 아가미는빗모양으로줄지어있는많은수의새엽과각각의새엽에서발달된새판으로구성되며, 각새판은상피세포, 점액세포, 염세포그리고벽주세포등으로구성되어있었다. 2001 년 12 월에서 2002 년 11 월까지채집된대부분의개체들의아가미에서새판상피층의박리와심각한새판의곤봉화가관찰되었으며 (Fig. 8, C), 2002 년 9 월에채집한개체중일부에서는벽주세포가붕괴된새판들과새엽들의융합과분지에의한형태학적이상이관찰되었다 (Fig. 8, D). 간은분지형태로되어있었고, 간세포는둥근다각형으로뚜렷한인을가지고있었으며, 모세혈관과담관이존재하고있었다. 2001 년 12 월부터 2002 년 11 월에걸쳐채집한개체가운데대부분의간조직에서흑색대식세포가출현하였고, 일부간세포의핵응축과담관내강의자유면이 AB-PAS (ph 2.5) 반응에서청색으로반응하였다 (Fig. 8, E). 흑색대식세포의출현은저수온기 (2001 년 11 월 ~2002
40 J. ENVIRON. TOXICOL. Vol. 21, No. 1 50 µm 50µm A B 100 µm 100 µm C D 50 µm 100 µm E F 100 µm 50 µm G H Fig. 8. Histological changes of skin, gill, liver and kidney in the pale chub, Zacco platypus. A: Note the epidermal layer necrosis of the skin. H-E stain. B: Epidermal layer of the skin showing the excoriation of the superficial layer and increased pigment cells (Pc). AB-PAS (ph 2.5) reaction. C: Section of the gill showing the clavate lamellae and epithelial lifting (El). H-E stain. D: Gill deformation with fusion and bifurcation of the filaments. AB-PAS (ph 2.5) reaction. E: Hepatocyte pycnosis and epithelial degeneration of bile duct (Bd) in the liver. AB-PAS (ph 2.5) reaction. F: Section of the liver showing the melano-macrophagocytes (Mp), cytoplasmic degeneration of hepatocytes and increment of hemocytes. AB-PAS (ph 2.5) reaction. G: Section of the kidney showing the glomerular dilatation (Gl) and hyaline droplet degeneration of the renal tubules. AB-PAS (ph 2.5) reaction. H: Note the pycnosis in the interstitial tissue and degeneration of the renal tubule (Rt) in the kidney. AB-PAS (ph 2.5) reaction. Cc: club cell, Ch: chloride cell, Dl: dermal layer, El: epidermal layer, Mc: mucous cell, S: scale.
March 2006 Jin et al. : 피라미의생식과기관계구조이상 41 년 3 월 ) 보다고수온기 (2002 년 6 월 ~2002 년 9 월 ) 에증가하는양상이나타났다. 그리고 2002 년 8 월에채집한개체중일부는간세포의세포질변성과간정맥내의혈구증가그리고담관의변성을나타냈다 (Fig. 8, F). 피라미의신장은앞부분이두갈래로분지되어있었고, 나머지부분은융합된형태를하고있었다. 2001 년 12 월과 2002 년 4 월에채집한개체들의신장에서는흑색대식세포의출현, 사구체의활성, 세뇨관상피층의초자성과립변성과비후가관찰되었고 (Fig. 8, G), 일부에서는세뇨관의폐쇄와간질조직의핵응축이관찰되었다 (Fig. 8, H). 고 찰 어류의성성숙과생식주기의변화는수온, 광, 영양분, 밀도등여러가지의생물 물리학적요인들에의하여영향을받지만 (Davies and Hanyu, 1986), 이외에도중금속과화학물질등의오염원에의해서도영향을받게된다 (Segner, 2005). 일반적으로온대지역에서식하는담수어류는큰납자루, Acheilognathus rhombea (Shimizu et al., 1985), 각시붕어, Rhodeus uyekii (An, 1995), 묵납자루, Acheilognathus signifer (Baek et al., 2003) 그리고감돌고기, Pseudopungtungia nigra (Lee et al., 2004) 등과마찬가지로연중 1 회의생식소중량지수 (GSI) 정점을가지며, 1 회의산란기를가진다. 어류의성숙과생식주기는 GSI 와간중량지수 (HSI) 의변화, 생식소의조직학적관찰을이용한생식소발달단계그리고어류의특정부위에나타나는체색의변화및이차성징의변화등을통해서도알수있는데, 이러한생식관련형질들은일정한변화경향과함께주기성을나타낸다 (Song and Kwon, 1989; Kim et al., 1999; Baek et al., 2003). 어류의 GSI 는주둥치, Leiognathus nuchalis (Lee and Huh, 2000) 의경우수컷에서높은것으로보고된경우도있으나점망둑, Chasmichthya dolichignathus (Baek and Lee, 1985), pike, Esox lucius (Treasurer, 1990), Siganus sutor (Ntiba and Jaccarini, 1990), Salmo trutta (Maisse et al., 1991), 연준모치, Phoxinus phoxinus (Song and Son, 2002) 그리고감 돌고기, Pseudopungtungia nigra (Lee et al., 2004) 등많은보고에서수컷에비해암컷이높은것으로보고되고있다. 본연구에서피라미암컷의 GSI 는연중 4 월과 8 월두번의정점을나타냈으며, 수컷의 GSI 도 5 월과 8 월에두번의정점을나타냈다. 그리고 7 월부터 9 월까지의수컷의 GSI 는같은시기의암컷 GSI 에비해약두배높게나타났다. 그리고생식소를조직학적으로조사한결과, 성장기, 성숙및완숙기, 방출및회복기, 휴지기의조직상을나타내는개체들의출현이계절에관계없이불규칙하게분포하였다. 또한피라미는납지리, Paracheilognathus rhombea 와줄납자루, Acheilognathus yamatsutae (Kweon and Ha, 1996) 그리고각시붕어, Rhodeus uyekii (An, 1995; Kim et al., 1999) 등과마찬가지로수컷의경우성숙및완숙시기에체색의변화가나타난다고알려져있으나 (Kim and Kang, 1993), 본조사결과피라미의계절별뚜렷한체색변화는관찰되지않았다. 이러한본연구의결과는어류의생식과관련한기존의많은보고들과는매우다른결과로서피라미는불안정한생식주기를가지는것으로판단되는데, 이러한결과를나타나게한원인에대해서는추후세부적인연구가필요할것으로생각된다. 물리 화학적인환경요인에의한어류의기관계변화가운데피부계의구조적변화에관한보고에서 Pleuronectes platessa 에자외선을조사하였을때, 이들어류의피부상피층에호산성과립세포들의출현과표면상피층의탈락이관찰된다 (Roberts and Bullock, 1981). 그리고내분비계장애물질과스트레스에의해서 Cyprinus carpio 와 Silurus glanis 의피부에서는점액세포와표면세포가증가되고결합조직층에서상피세포층으로혈구의침투가확인되며 (Iger et al., 1991), 송어류인 Oncorhynchus mykiss 의피부에서는표면세포와색소세포가증가되었다가소실된다 (Iger et al., 1994). 어류의아가미상피층은가스교환, 이온조절, 산 염기조절그리고질소배설등을조절하는기관으로여러가지환경오염원은어류아가미의형태및생리적기능을변화시킨다 (Evans, 1986). 중금속에노출된어류의아가미에서는상피세포의세포질공포, 미세융모손실, 미토콘드리아의이상, 비대및괴사와상피층의박리가관찰된다 (Mallatt,
42 J. ENVIRON. TOXICOL. Vol. 21, No. 1 1985). 그리고롱아일랜드의오염된곳에서채집된 winter flounder, Pleuronectes americanus 의아가미에서는새판의분지가관찰되었다 (Pereira et al., 1992). 어류의간은다양한물질대사와독성물질해독작용뿐만아니라난황전구체인비텔로제닌합성등중요한기능을수행한다. 비소에노출된 green sunfish, Lepomis cyanellus 의간은소엽구조가불규칙하고, 간세포핵의변형과담관의변성이나타난다 (Sorensen et al., 1980). 세제에지속적으로노출된 Heteropneustes fossilis 의간에서는퇴행성병변과염증성괴사가나타났으며 (Narain and Nath, 1986), 오염된엘베강하류에서채집된 Gymnocephalus cernua, Platichthys flesus 그리고 Osmerus eperlanus 의간에서는간세포감소와퇴행성병변을보였다 (Peters et al., 1987). 화학물질이유출된나일강의뱀장어, Anguilla anguilla 간에서는간세포크기가감소하고, 비특이적면역반응으로간조직내에식세포가나타났다 (Braunbect et al., 1990). Microcystin-LR (MC-LR) 을경구투여한무지개송어, Oncorhynchus mykiss 의간에서는종창과괴사가확인되었다 (Kotak et al., 1996). 경골어류의신장은중요한조혈및배설기관으로 monocrotophos 에노출된 Puntius conchonius 의신장에서는조혈조직의변성, 사구체의위축및세뇨관의변성이나타났다 (Kumar and Pant, 1985). Puntius conchonius 를 methoxy ethyl mercuric chloride (MEMC) 에노출시켰을때세뇨관상피세포의핵응축과내강표면의붕괴가나타났고 (Gill et al., 1988), 카드뮴에노출되었을때주로원위곡세관에상피세포의핵이응축되고붕괴되는퇴행성병변을나타냈다 (Gill et al., 1989). Microcystin-LR (MC-LR) 을먹인무지개송어, Oncorhynchus mykiss 는보우먼주머니의팽창과세뇨관괴사가나타났다 (Kotak et al., 1996). 본연구에서관찰된피라미의피부, 아가미, 간, 신장에서관찰된여러가지의병리조직학적특징들은외부환경요인에의한기존의보고들과비교할수있는현상으로판단되지만, 이러한피라미의병리조직학적인특징의유발요인에관해서는추후세부적인연구가필요할것으로생각된다. 참고문헌 An CM. Reproductive cycle of the spring-spawning bitterling, Rhodeus uyekii (Pisces : Cyprinidae), Kor J Ichthyol 1995; 7: 33-42. (in Korean) Baek HJ and Lee TY. Experimental studies on the mechanism reproductive cycle in the longchin goby, Chasmichthys dolichognathus, Bull Korean Fish Soc 1985; 18(3): 243-252. (in Korean) Baek HM, Song HB and Kwon OK. Sexual maturation and the spawning season of the Korean bitterling, Acheilognathus signifer in upper reachs of the Hongcheon river, Kor J Ichthyol 2003; 15(4): 278-288. (in Korean) Braunbeck T, Burkhardt-Holm P and Storch V. Liver pathology in eels, Anguilla anguilla L. from the Rhin river exposed to the chemical spill at Basle in November 1986. Biology of the river Rhine, Limnol Akt 1990; 1: 371-392. Capel PD, Eisenreich SJ, Baker JE and Looney BB. Chemical limnology of PCBs in lack superior-a case study, Toxic cont Lar 1988; 3: 291-318. Crisp DT. Comparison of the physical properties of real and artificial salmonid eggs and of their performance when drifting in an experimental stream channel, Hydrobiologia 1989; 178: 143-153. Davies PR and Hanyu I. Effect of temperature and photoperiod on sexual maturation and spawning of the common carp- I. Under conditions of high temperature, Aquaculture 1986; 51: 277-288. Evans DH. The fish gill: Site of action and model for toxic effects on environmental pollutants. Mechanisms of pollutant action in aquatic organisms, Research Triangle park NC (USA) 1986; 21-23. Gill TS, Pant JC and Texari H. Branchial and renal pathology in the fish exposed chronically to methoxy ethyl mercuric chloride, Bull Environ Contam Toxicol BECTA 6. 1988; 41: 241-246. Gill TS, Pant JC and Tewari H. Cadmium nephropathy in a freshwater fish, Puntius conchonius Hamilton, Ecotoxicol and Environ Safety EESADV 1989; 18: 165-172. Haaparanta A, Valtonen ET and Hoffmann RW. Gill anomalies of perch and roach from four lakes differing in water quality, J Fish Biol 1997; 50: 575-591. Harshbarger JC, Coffey MJ and Young MY. Intersex in Mississippi river shovelnose sturgeon sampled below Saint Louis, Missouri, USA, Mar Environ Res 2000; 50:
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