The Science of the Total Environment, 102 (1991) 1-19 Elsevier Science Publishers B.V., Amsterdam

Review THE EEL (ANGUILLA POLLUTANTS

SP) AND ORGANIC CHEMICAL

J. B R U S L E

Laboratoire de Biologie Marine, Universitd de Perpignan, Avenue de Villeneuve. 66025 Perpignan, France

(Received December 12th, 1989; accepted February 20th, 1990) ABSTRACT The effects of pollutants [pesticides, polychlorinated biphenyls (PCB), hydrocarbons and surfactants] on different species of eel are reviewed. Two types of data are analyzed from the existing literature (72 references), namelythose for contaminatedwaters and those for experiments under laboratory conditions. It is concluded that the eel is not as resistant as has generally been suggested.

INTRODUCTION

The eel A n g u i l l a has generally been thought to be a resistant species owing to its apparent robustness in the face of fluctuations in temperature, salinity, food availability, oxygen and temporary emersion. This characteristic has also been studied with respect to the decline in water quality of various contaminated water bodies such as estuaries, lagoons, lakes and streams. However, conflicting hypotheses were developed when eel kills were observed, as in the River Rhine (Basel, in November 1986), due to toxic efltuents (including atrazine, fenitrothion, parathion; Anonymous, 1987a). Another fish kill occurred in western France (Josnin, 1987) and severe mortalities were observed in Canada in m a t u r i n g eels (A. rostrata) migrating to the sea through the St. Lawrence estuary (losses were estimated to have been > 100t in 1972-1973; Dutil, 1984; Dutil and Lallier, 1984; Dutil et al., 1985, 1987). It is now established that the eel is more susceptible to toxicants than has generally been assumed. In addition to the threat to wild eel populations, risks to h u m a n health have been observed, for example in Canada (Turgeon and Beaulieu, 1973) and in Germany (Bimbos and Mau, 1986) where commercial eel fishing was banned because of the toxicity of eel flesh. Thus, it is useful to survey the present knowledge on the acute and chronic effects of chemical pollutants on wild populations and also to consider experimental investigations. The eel, indeed, seems to be particularly suitable as a laboratory animal in ecotoxicology (Brusle, 1990a).

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An early review of the effects of heavy metals on the eel was first presented at the EIFAC Working Party on the Eel, Bristol (Brusle, 1987), and published by Brusle (1990a). This paper deals with the effects of some organic toxicants on American, European and Japanese eels, from the existing literature (72 references). Two main types of toxicological data were considered: (i) observations in the field, for eels taken from contaminated waters; and (ii) experimental investigations under laboratory conditions. A summary of the toxicants for Anguilla anguilla, A. rostrata and A. japonica is given in Tables 1 and 2 and details are discussed below.

LETHALITY In the field, natural eel kills have hardly ever been correlated with a precise chemical factor, because of the complexity of the various contaminant mixtures in some polluted areas (Anonymous, 1987a). In Canada, heavy mortalities since the 1960s have taken place in late summer in the St. Lawrence River and its estuary, with a maximum intensity reached between 1972 and 1974. Three potential causes have been considered: bacterial infection; viral infection; and physiological stress related to the processes of maturation and migration of female eels. However, the authors (Dutil, 1984; Dutil and Lallier, 1984) reached the coi~c!u~ion that mortalities were not associated with bacterial pathogens (Aeromonas, Renibacterium, Vibrio). In addition, moribund eels showed a lower serum osmola!ity (270mOsM kg-') than the controls (328mOsM kg-~). This variation resulted from low sodium and low chloride contents. Maturing eels failed to maintain their mineral balance in freshwater and suffered from an excessive mineral 10ss resulting in mortality through physiological disorders in the particular conditions, which included mixed pollutan;s present in the St. Lawrence (Dutil, 1984; Dutil et al., 1985, 19~7). The impoverishment of eel communities and a reduction in the frequencies of occurrence of eels in some Dutch soft waters were reported to be caused by acidification (Leuven and Oyen, 1987). Osmoregulatory stress, impaired gas exchange and changes in the predator-prey relationships are considered to be the main causes for the mortality, or the avoidance, of eels in waters with a low pH ( < 5.5). Unfortunately, no clear-cut cause was identified and further data are required. Under laboratory conditions, available data deal with acute toxicity using LCs0, MATC (maximum acceptable toxicant concentration) and MTL (median tolerance limit) criteria.

Phenols Acute. toxicity of phenols to the eel is characterized first by an exciting phase, then by ataxia, followed by death (Grauby et al.,1973). Lethality is high (in a few hours) following exposure to 20ng I-~ phenol (Caries, 1973). Toxicity

Yellow eels

Elvers and yellow eel

Yellow eels

Anguiila angudla

Stage of development

I

llydrocarhons

Rivers Mole and Taw {U.K.)

Lower EIh¢ River

Household waste dump near Amsterdam (Netherlands)

l)iehlrm I)I)E l,indane

Muscle c{Hlt'ent rill ittn

Muscle ('orlcent ratlorl

030 6.18mg kp, 0.08 1.74mg kg 0.06 0.63mg kg 0.21 5.84 mg kg O..5Vt 10.9:ling kt~ 120 19191/g kg 64 2911tg kg I 25 Itg kg I

Whole fish and liver t'ont'elltration

Muscle. gill and ovary accunilllation

144 ng g 97 ng g l I I ;

Inter-renal activity

Hydrocarbons

Brittany (wreck of Amoco Cadiz) Brittany (wreck of Amoco Cadiz)

2,3,7,8-'rci)!) (tetra('hlorodihenz.-p-dioxin) IlCB ItCH l,lndane DI)T P('lis

(;ill at}d ovary histolmthology

tlydrocarhons

Whoh. fish ccmcentration

Brittany (wreck of Amoco Cadiz)

Loire estuary

Whole fish t on('entration

0..502 O.1413/tg g 0.016 O.140#g g 0.043 0.101 pg g 0.014 O.194pg g 0.012 O.O37pg g 0.023 O.07:lltg g 16.3mg kg ! il.3mg g I 11 3 2 m g kg ] 11 32 mg kg 1H3 470mg kg ; 188 8 6 8 m g k g I

PCB DDT I)I)D I)DE [,indane Dieldrin Hydrocarbons Squalene

Gill and ski" congestion and hemorrhage Muscle concentration

Biological effects

North and Baltic Seas

!

Observed concentrations

5.47 7 5 n g g 25ng g l 51 ng g I

Lindane

Chemical

z.ilCH I)DD DDT

Olivier lagoon {Mediterranean) Rearing ponds {Audenge. Croisic and Salins du Midi)

Geographical area

The eel and natural waters contaminated by organic pollutants

TABLE 1

(continued)

Hmntlton. 19s5

I,ehmp-lhitey aml tlardy. 19S.5 Heida. 1983 Ih.ida and ()lit,. 19/4.5 Krut, e et al.. 19/43

1!)81

I,opez el a l . 19~qa.I) Marchand. 19Sl i,eloup-]httt.y el al..

Feral eL al.. 1979

Awad. 1979

Huschenbeth. 1977

Schat'hter et Ill., 1969 Aubert et al., 197'7

Reference

Yellow eels

Anguilla rostrata

St. Lawrence River St. Lawrence Rwer

Lake Ontario St. Lawrence River St. Lawrence estuary

Lake Ontario St. Lawrence River Lake Ontario

Northwest Gulf of Mexico

Atlantic coast of Canada

The Netherlands

Dutch soft waters

Donana National Park (Spain)

Hernandez et al., 1987

Leuven and Oyen, 1987 Van den Berg et al., 1987

Muscle concentration

Frequency of occurrence

Bertrand et al., 1986 Dutil et al., !987 Castonguary et al., 1989

Fillet concentration Whole fish concentration

4.901~g g - 1 0.12-0.191~g g - l 0.77 1.611~g g - I

PCB

Mirex

Mortality and gill pathology Flesh concentration

Dutil et al., 1985

Fillet concentration 6.4 38.5 ng g - 1

2,3,7,8-Tetrachloro-dibenzo-p-dioxin {TCDD) PCB Mirex

O.l-195ng g - I

Desjardins et al., 1983 Ryan et al., 1984 Flesh concentration

?

Giam et al., 1978

Whole fish concentration

Sims et al., 1977

Anonymous, 1987b

Muscle concentration

Frevuency of occurrence

Bimbos and Mau, 1986

Reference

Muscle concentration

Biological effects

Whole fish concentration

l

0.44 l~g g - !

1.7 5.2rag kg I

1 6 ng k g - l

? ? 0.05 mg k g - l 2.5mg kg ! 0.48 1.6 mg k g - ! 0.11-0.54mg kg k 1 0.0911g g - I 0.1414g g-- 1 O.021tg g ! O.191tg g - !

Observed concentrations

0.5611g g 15.01~g k g - I 2.01~g k g - ! 5.01~g k g - l 0.I0-0.22 j~g k g - t

PCB (nroclor 1254 and 1260) DDT PCB p.p'-DDT p4~'-DDE Mirex

PCDDs {polychlorinated dibenzo-p. -dioxins) PCDFs (dibenzofurans)

I,indane DDT HCB PCB PCBs HCB DDT DDE Lindane PCBs Acid wate~'~ (pH < 5)

River Rhine

River Rhine

Chemical

Geographical area

1 (continued)

Stage of development

TABLE

2

20 mg 1- !

Phenols

Detergent LAS (linear alkylate) sulphonate lmg I -l

200mg kgI

6 x 1000mg kg - !

-

? 2.45mg i 1

0.04-11.6 mg 1- I 4.6 7.5 mg 1- I

20-40 mg I - 1

0.1 ppm

PCP (Na pentachlorcphenate)

12.5 mg day- 1

Yellow eels

Five anionic detergents, suifosuccimc acid, polyoxyethylene alcohol sulfate and alkylbenzene sulfonates Twelve effluents from chemical plants Aliphatic hydrocarbons Phenols Sulphides Oils PCB (Clophen A50)

pollutants

Concentration

by organic

o-p'-DDD

Chemical

contamination

Silver eels

Anguiila anguiila

Stage of development

The eel and experimental

TABLE

Repetitive oral dosing seawater IO°C 1-2 weeks Single oral dose Seawater 1O-! 4°C 1-4 months Perfusion of the gills freshwater 18oC 24 48 h

Brackishwater pH 7.3

Freshwater daily inject,on 3-26 days 21°C Seawater (pH 8.1) or freshwater (pH 7.1) 12°C (pH 8.1) 4--8 to 55 days no food Freshwater 14°C, pH 6.5 0.5 h-7 days Seawater 20°C

Experimental conditions

Gill vasodilation

Sublethal metabolic effects

Acute toxicity (MTL. 24.4b and 96 h)

Acute toxicity

Lethality and concentration

Concentrahon in liver, muscle and blood. Metabolic effects Recovery

Pituitary, adrenal tissue lesions

Biological effects

(continued)

Bolis and Rankin. 1980

Johanason-Sjobeck et al.. 1975

Dave et al., 1975

Grauby et al., 1973

Cossa and Maggi, 1973

Caries, 1973

Holmberg et al., 1972 Holmberg and Saunders, 1979

Olivereau, 1964

Reference

Anf~uilla rostrata Yellow eels

Yellow eels

Elvers

Stage of development

DDT PCB {Arochlor 12211

Twelve organochlorine and organophosphorus insecticides Endrin Dieldrin p-p-DDT Aldrin Heptachlor Methoxychlor Lindane Malathion DDPV Methyl-parathion p.p'-DDT

Polyethoxylated nonyl phenols (surfactant) Lindane endosulfan

Lindane Parathion methyl PCBs (Clophen A50)

Chemical

TABLE 2 (continued)

,

10-4moll

!

1 ppm 14C-DDT 0.075 ppm DDT 25 75 ppm Arochlor

(50 ppm)

1.4

0.6 l . l # g l 1 0.9 8#g 1 1 4 714g I I 5 181~g 1 1 IO 71~g 1 1 12 2 5 j 4 g l - I 56 7014g ! 1 82/tg 1 1 1800 2300/~g ! I 16900 270011g 1 !

0.32 O.70mg i I 0.020 0.040rag 1 !

0.5 8000 mg I - l

0.085#g g - t dry wt

0 349mg 1 l 4.19 6.75 mg 1 - l

Concentration

Seawater 13 16°C 3 weeks Seawater 15°C

Salinity, 24%0 20°C pH 8.0 7.1 7.7mg 1 I

Disruption in osmoregulation

Osmotic inhibition in the intestine

Acute toxicity (LCs0, 24, 50. 96h)

(continued)

Kinter et al., 1972

Janicki and Kinter. 1971

Eisler, 1970, 1972

Ferrando et al., 1987

Miossec and Bocquene, 1986

Larsson, 1984

Whole fish concentration

Contaminated sediment freshwater 8oc reduced pressure fed chironomids Seawater {33%0) 12°C Tap water 15, 22, 29°C pH 7.9 photoperiod Acute toxicity (LCso, 48h) gill histopathology Acute toxicity (LCs0, 24, 48. 72, 96h)

Canyurt, 1983

Reference

Acute toxicity (LCs0, 24 h)

Biological effects

Freshwater in aquaria

Experimental conditions

c~

Yellow eels

AnguiUa japonica

Elvers

NH 3

Oil spill eliminator CDunall') Dimethylnitrosamine

CC!4

Kepone

?

Freshwater 25°C

2.844 mg 1- t (pH 5) 820mg 1- z (pH 7) 16.8mg 1 - ! (pH 9)

0-110 ppm ?

Frc3hwater 19°C pH 6.9 02:6.5 mg ! - z Injection tapwater 14--20°C Seawater

1

0.01 cc/lO{~g body wt

35--22~#g I -

Kidney histopathology (nephroblastema) Acute toxicity (LCs0, 24 h) hematological changes growth suppression gill pathology

Liver histopathology, biochemical changes Biochemical changes

Acute toxic:,~y t~'~50, '~ "~ ~ h)

Yamagata and Niwa, 1982

Mizuhashi, 1978

Inui, 1968, 1969 King et al., 1978

Roberts and Bendl, 1982

of the effluentsfrom a refinery and from chemical plants has been tested and the high concentration of phenols (7.5-19mg l-~) was found responsible for fish kills (Grauby et al., 1973). The eel was one of the fish with a higher intake (49 ppm in the flesh) than other species, due to a high fat content of muscle tissue.

Pesticides In A. anguilla, the lethal concentration (LC~0, 24h) was 0.35mg 1-' for lindane, which was lower than for tilapia and higher than for carp. For methyl parathion, the LCs0 (24 h) was 4.19mg 1-~, lower than for either tilapia or carp (Canyurt, 1983). In A. rostrata, 96 h bioassays with 12 insecticides revealed (Eisler, 1970) a descending order of toxicity from the most toxic, endrin (0.6 ppb), to the least toxic, methyl parathion (16 900 ppb). It still appeared then that the eel was one of the most susceptible species of estuarine fish compared with bluehead, mummichog, killifish, mullet and puffer. Similarly, elvers (stage VIA) were more sensitive to kepone (LCs0, 96h: 35/~g I-~) than were other species (bluegill,fathead minnow and catfish)and the values of M A T C (0.14pg I-~) were well above the kepone concentration observed in water samples (James River), according to Roberts and Bendl (1982). The toxicity of insecticides is strongly affected by changing temperature. Thus, it was shown (Ferrando et al., 1987) that e~dosulfan exhibited a positive temperature correlation toxicity (LCs0) which increased with increasing temperature from 15 to 29°C. In contrast, lindane had a negative temperature correlation. Endosulfan was more toxic to the eel than lindane: the principal site of action of these two chlorinated pesticides is the central nervous system as a result of alterations in ion transport across the excitable membrane. It was concluded that, because of its action as a neurotoxicant, application of endosulfan at high temperatures would be hazardous to eels.

Detergents and surfactants The acute toxicity of five anionic detergents was tested in elvers, but they were degraded by bacteria in a few days (Cossa and Maggi, 1973). However, in elvers (stage VIA2), polyethoxylated nony]phenols, a non-anionic surfactant group, showed a toxicity (LCs0, 24h) which varied from 1.2 to 10 000rag l-~, in inverse relation to the number of ethylene oxide groups in the molecule (Miossec and Bocquene, 1986); the higher the lipid solubility, the higher the toxicity.

Ammonia Lethal effectsfollowing a growth-suppressing effect of unionized NH3 were examined by Yamagata and Niwa (1982).

BIOACCUMULATION The concentrations of various chemicals in the eel (whole body or different organs) have been compared with those in water (or sediment) and measured in order to evaluate the hazards of accidental aquatic contamination. Criteria of water/fat partition are used in order to explain the accumulation processes in the muscle, liver or ovary tissues.

Hydrocarbons Examination of hydrocarbon-contaminated fish from the Loire estuary, France, revealed, despite individual variability due to strong differences in environmental conditions and ecological factors, a higher concentration of total hydrocarbons and squalene in a "fat fish" such as Anguilla than in a "meager fish" such as Trisopterus or Dicentrarchus (Awad, 1979). In Brittany, following an oil spill (Amoco Cadiz shipwreck), hydrocarbons accumulated more in lipid-rich tissues such as the ovary (188 ppm) than in muscle and gill. A partial depuration of eel tissues was only noted 8 months after the spillage (Feral et al., 1979).

Phenols and pentachlorophenol (PCP) The phenol concentration was reported to be higher in the blood than in the liver and gills, but decreased rapidly (perhaps due to bacterial oxidation process or to liver detoxification) in eels which survived an exposure of 20 mg l- ~(Caries, 1973); the concentration of phenol in fresh muscle tissues (19-49 pg g-~) probably being responsible for the bad smell emanating from the flesh (Grauby et al., 1973). In addition, pentachlorophenol, used as a fungicide or molluscicide or found in pulp-mill eliluents, was reported to be absorbed through the gills and/or the skin in eel (A. anguilla). The highest levels were found in the liver (33.4 ppm after 8 days exposure) and in the muscle tissue (PCP content only one-quarter of that of the liver); PCP continued to have an effect (1.2 ppm) in spite of a recovery period of 2 months (Holmberg et al., 1972). This lipid-soluble contaminant was mainly stored in the mitochondria and seemed particularly available ~%r binding to mitochondriai proteins.

Pesticides Pesticides are also accumulated in the wild eel. Anguilla anguilla Discharges of pesticides into the Rivers Mole and Taw (U.K.) resulted in high levels of aldrin and dieldrin in eels caught just downstream of the discharge that exceeded concentrations found in other fish such as sahnon,

10 trout, loach, bullhead and minnow. With high variability in individual concentrations of pesticides,Hamilton (1985) concluded that eel populations have been significantlyaffected and that levels of contaminants could be considered potentially dangerous to piscivores. Similarly, P C B and pesticides' levels in eels from the River Rhine were shown to be relatively high and exceeded the allowed concentrations (Bimbos and Mau, 1986).Because of high fat levels,eels from the Rhine and Main Rivers should be forbidden for human consumption, especially for women who are breast-feeding. In addition, levels of hexachlorobenzene (HCB) (0.11-0.54mg kg -I) and polychlorinated biphenyl (PCB) (0.48-1.6mg kg -I) in the lox,.-~rRiver Rhine (the Netherlands) exceeded, in 1~79 and 1983, the tolerance limit for sole (Anonymous, 1987b). Determination of organochlorine pesticide concentrations (lindane, D D T and PCBs) in eels from the lower Elbe River (Hamburg, Schleswig-Holstein and Niedersachsen) showed (Kruse et al.,1983) that 91°% (355 out of 391 investigated eels) cvntained levels exceeding the regulatory limits. Lipophilic, persistent pollutants, such as PCBs, are available to aquatic organisms from contaminated sediments in lakes and water cou~'ses,which may act as a source of PCBs to bottom-dwelling fish such as the eel. It w~s shown by Larsson (1984) that eels, which live and feed in direct contact with the sediment, may be exposed to higher amounts of P C B than fish in the open sea. It.was demonstated that PCBs (Clophen A50), when added to sediment in aquaria, were released from the sediment to the water (desorption) and taken up by the eels directly from the water through the gills(water/fatpartitioning). Moreover, P C B concentrations were highest (471.6/~g g-~) when eels were allowed to feed on benthic macroinvertebrates in the sediment (chironomids), as a result of accumulation through the food chain (Larsson, 1984). Similarly, eels contained the highest concentrations of organochlorine residues (DDT, DDE, lindane, dieldrin, heptachlor and PCBs) due to the biological magnific. ation process in these tertiary consumers (Hernandez et al.,1987). Accumulation of DDT, DDD, lindane and dieldrin was determined in the North Sea and the Baltic. A. anguilla was found to be more contaminated by organochlorines than were marine fish such as cod and herring (Huschenbeth, 1977). In Western France (Audenge, Croisic), H C H and D D T concentrations were higher in yellow eels than in elvers and were correlated with the lipid concentrations nf muscle tissue. Contamination was even greater in eels (1029 ng g-I HCH~ than in trout, mullet and seabass (Aubert et al.,1977). Eels caught in the vicinity of a refuse dump near Amsterdam contaminated with organochlorine waste compounds, mainly 2,3,7,8-tetrachlorodibenzo.pdioxin (2,3,7,8-TCDD), contained a small quantity (1 ppt) of this chlorodioxin. The concentration was lower than that in pike liver and lower than calculated levels based on water-sediment partition coefficientsand biological accumulation factors, because of interfering factors such as suspended solids. Consequently, there is no real health hazard for people consuming eels caught in waterways adjacent to the dump (Heida, 1983). However, in another work,

11

Heida and Olie (1985) showed that the highest 2,3,7,8-TCDD levels (144 ppt fresh wt in whole-body samples and 97 ppt in the liver) were found in the eel. Because of the toxicity of these dibenzofurans, the local population was dissuaded from consuming the eels. Not far from this chemical waste dump, the liver of fisheating birds (cormorants, grey herons, grebes) was shown to contain high levels of 2,3,7,8-pentachlorodibenzofurans (PCDF) and 2,3,7,8-tetrachlorodibenzo-p-dioxin. The same congeneric pattern of chemicals was found in the eels as in the three bird species. By considering the eel as a major food source for the cormorant, it was concluded (van den Berg et al., 1987) that fish-eating predators were contaminated through eels, and bioaccumulation factors could be calculated from the eel to the cormorant. Anguilla rostrata DDT and PCB concentrations in the American eel from various locations on the Atlantic coast of Canada were higher (0.56 and 0.44#g g !, respectively) than those in herring, mackerel, salmon and smelt (Sims et al., 1977), indicating preferential accumulation in the lipid-rich eels. Similarly, Ryan et al. (1984) found that eels from Lake Ontario had the highest TCDD concentrations (6.4-38.5 ppt) when compared with those of rockbass, black crappie and pimpkinseed. Moreover, the eels contained the highest concentrations of PCB, which appeared to parallel the fat content (36.6%). They concluded that fish samples with a high lipid content had a high PCB content and a high probability for the presence of dioxin. For example, data from the analysis of surface sediments and organisms from the St. Lawrence estuary showed that PCB concentrations were higher in the American eel (0.77 1.16#g g ' fresh wt) than in the herring, Clupea harengus (0.06-0.13#g g~; Bertrand et al., 1986). Mirex was also detected (0.18#g g !) in all eels caught in Lake Ontario (Desjardins et al.,-1983). Seventy-four percent of the migrating eels caught in the St. Lawrence River contained Mirex (0.17pg g I), and these were thought to originate from Lake Ontario (Dutil et al., 1985). These authors concluded that eel stocks can be discriminated on the basis of the presence in their tissues of synthetic chemicals such as pesticides that are distributed heterogeneously in the environment. Considering the insolubility of Mirex in water, sediments have been identified as the major environmental compartment containing Mirex. Finally, Castonguay et al. (1989) have presented a new method for stock discrimination using the environmental distribution of contaminants (14 pesticides and PCBs) and a comparison of organic contaminant levels among groups of eels from different geographic origins (referred to as the freshwater area of residence of the immature eels). The relatively high discrimination among eels from various sampling sites, based on their contamination levels (Mirex, heptachlor, epoxi.de, etc.) provided valuable information regarding fish stock discrimination. This presence or absence of Mirex allowed a distinction, in Lake St. Pierre, 400 km downstream from Lake Ontario, between eels originating from the Lake Ontario/St. Lawrence River region and those originating from tributaries of the St. Lawrence River (Castonguay et al., 1989).

12 HISTOPATHOLOGY

Histopathology has proven to be of obvious interestfor stu~!~yingthe chronic effects of different chemicals, using findings on organ injuries and tissue damage.

Liver The liver is one of the most studied target organs in ecotoxicological investigations. However, data on the impact of chemicals on eel liver are limited. Following an injection of carbon tetrachloride into the Japanese eel (Inui, 1968), the liver showed degenerative changes on Day 4. From Day 7 to Day 10, necrotic areas became very marked: swollen or atrophied cells,pycnotic and polymorphic nuclei, with the development of large haemorrhagic areas. Some indications of regeneration processes occurring in the deteriorated liver tissue were apparent from Day 10 to Day 20, and a rapidly increasing deposit of fat (oil droplets in hepatocytes) was observed in the liver. Finally, recovery through the regeneration of remnant liver cells was almost complete 30 day~ after the injection.Unspecific physiological changes were stillobserved during this period of eel hepatitis

Gill Another target organ is the gill,where congestion was observed, as well as haemorrhagic skin lesions in yellow eels of a Mediterranean lagoon followin~ lindane treatment against mosquitoes (Schachter et al., 1969). Some inflammatory reactions were observed in elvers' gillsfollowing a toxicity test using a non-ionic surfactant (polyethoxylated nonylphenols). Tissue changes were non-specific and corresponded to a classic defense response to any stressor agents, i.e.hypersecretory mucous activity (increasing barrier), hyperplasic activity and desquamative production (wider space between the toxic substance and the blood) and lamellar fusions (decreasing sensitive surface) (Miossec and Bocquene, 1986).Hypertrophy of lamellar epithelium was shown in the gillsof Japanese eels exposed to 40/~g l-~ ammonia (Yamagata and Niwa, 1982). Ammonia toxicity may be a limiting factor in eel culture (Saroglia et al., 1981). Following hydrocarbon contamination (Amoco Cadiz shipwreck), Lopez et al. (1981a,b) t'ound that the gills of A. anguilla showed hypertrophy and hyperplasia of ionocytes (chloride cells) and of mucous cells, with hypersecretion of mucus (PAS + ) associated with hyperaemia and lysis of blood platelets. In addition, hyperactivity was detected in two hypocalcemic glands (ultimobranchial body and corpuscules of Stannius). Finally, in the St. Lawrence River, diseased eels display few chloride cells and hypertrophic-hyperplasic cells, necrotic tissues and aneurisms, damage responsible for osmoregulatory failure and death (Dutil et al., 1987). These authors ruled out the possibility

13 that the disease is related to unknown contamination of the St. Lawrence River and its tributaries.

Ovary and inter-renal gland Structural modifications induced by Amoco Cadiz hydrocarbon contamination were analyzed histologically in the ovary of the European eel in Brittany (Lopez et al., 1981a,b). The nuclei of numerous oocytes were pycnotic and ovarian follicles entered into degenerescence throughout the necrosis process. Moreover, extreme stimulation of inter-renal activity (glandular hypertrophy followed by symptoms of exhaustion) was observed. Hence intensive stress of long duration (8 months) could be considered as potentially fatal (Leloup.Hatey et al., 1981; Lopez et al., 1981a,b; Leloup-Hatey and Hardy, 1985).

Kin Pathology of the integument of eels (epithelial tumours, "papillomatosis" or "cauliflower disease") was found mainly in Northern Europe and the northeast Atlantic, in coastal waters heavily polluted with sewage. These abnormalities were found in Poland (Pilarczik, 1973), on Danish shores (Christiansen and Jensen, 1947; Christensen, 1980), in the North and Baltic Seas and in Germany (Moiler, 1981, 1985, 1988) in the Lower Elbe (Schaperclaus, 1953; Pfitzner and Schubert, 1969; Schubert, 1969; Peters and Peters, 1977, 1979, 1984). Few diseased eels were caught in France (Nounou et al., 1980). It was suggested that skin lesions were related to poor environmental quality alid were probably due to the impact of pollution producing an increase in ulcers (Moiler, 1981). However, the etiology is uncertain and the precise influence of chemical pollution has not been clarified; evidence of a relationship between increased disease prevalence and environmental degradation is only circumstantial. It seems (Peters and Peters, 1984) that tumour diseases are related to an increased level of environmental (multifactorial?) pollution and are presumably caused by a numbor of factors (reduced oxygen concentration, harmful substances and increased temperature). In addition, the participation of a virus cannot be excluded, but no firm evidence has yet been demonstrated, in spite of considerable effort to do so. PHYSIOPATHOLOGY Some data are available showing physiological changes in eels associated with certain organic pollutants and organ perturbations of the major fish functions.

14

Osmoregulation DDT inhibited Na ~, K ~ and Mg '-'t ATPase involved in sodium transport in the intestinal mucosa (A. rostrata), disrupted osmoregulatory transport mechanisms and impaired osmoregulation (Janicki and Kinter, 1971). Thus, 1.4 × 10 -4 tool 1-1 DDT induced a 47% inhibition of water absorption, and i.4 × 10- 5tool l - ' is responsible for a 43% inhibition of Na * and Mg 2÷ ATPase in the intestine. Kinter et al. (1972) have also demonstrated the disruption of osmoregulation in the eel exposed to DDT and to PCBs. Sublethal metabolic effects of PCB after a single or repetitive oral dose indicated poor uptake and, among 27 metabolic parameters, very few were found to be sensitive to PCB (Dave et al., 1975). Water and organic ion metabolism was, however, found to be sensitive (an elevation of plasma chloride and a decrease in plasma calcium and muscle water content). In addition, Bolls and Rankin (1980) showed, in perfused gills of the European eel, that the detergent LAS (linear alkyl sulphonate) affected vascularization (restricted ability to dilate gills) and branchial permeability owing to a reduction of noradrenaline activity. These effects on the gills could have been due to detergent inhibition of fl-adrenergic receptors in the gills (detergents may act by increasing membrane fluidity and in altering the mobility and distribution of receptors within the membranes of the gills), in a similar manner to another group of lipid-soluble pollutants, i.e. the organophvsphorus pesticides. In addition, PCB caused transient blood anemia and hematocrit decreased; the hemolysis is considered to be due to the lipophilic effect of PCB on cell membranes (Johansson-Sjobeck et al., 1975).

Liver metabolism A pathological analysis of the effects of CCI4 on eel (A. japonica) liver demonstrated that the fat accumulatioa observed was a result of inhibition of the triglyceride secretory system in the liver (Inui, 1968). Moreover, serum transaminases :g],,tamate oxalacetate transaminase, glutamate pyruvate transaminase) were found to be extremely useful indicators of liver disease (hepatitis, Inui, 1969). The p8ttern of increase of both transaminases was closely correlated with the destruction of injured liver cells as observed histologically. Finally, an oil spill eliminator CDunall"), used in Taiwan after the wreck of an oil tanker, induced histochemical changes such as increased glycogen content of the liver and increased acid phosphatase activity of the liver, gill, and kidney of Japanese eels (King et al., 1978).

Stress Pentachlorophenol (PCP), used as a fungicide, bactericide, herbicide and insecticide, is a powerful uacoupliag agent of oxid_~tive phosphorylation. It is responsible for an increase in oxygen consumption and for a doubling of the glucose and lactate concentrations in the blood, parameters which are an

15 indication of stress for the American eel (Holmberg and Saunders, 1979). A change in other metabolic activities was also observed: PCBs also caused a hypermetabolic state characterized by a loss of body weight, an increase in opercular movements, a rise in hematocrit, hemoglobin and blood lactate, and an accelerated utilization of tissue energy reserves (cholesterol, trigycerides and free fatty acids levels in blood plasma), signs that showed striking similarities to a stress situation (Holmberg et al., 1972). Similarly, DDD activated the cells in the pituitary gland of the eel, indicating increased ACTH secretion (Olivereau, 1964). Finally, considerable stimulation of inter-renal activity (increase in the cortisol level in the plasma and greater corticosteroid activity) was also observed following hydrocarbon contamination of A. anguilla (Lopez et al., 1981b; Leloup and Hardy, 1985). These extensive reactions are similar to those described for chronic intense stress. CONCLUSION A number of environmentally important chemicals has stillnot been investigated with respect to eel toxicology. Nevertheless, it is of considerable interest to understand the modifications of the main physiological mechanisms involved in injuries of toxic origin. It may be assumed that the decrease in re~ ruitment of elvers throughout European coastal waters is of anthropogenic origin (Brusle, 1990b). Losses have been associated with lesions in gonads, eggs and larvae of European eel (Tesch, 1985). Although reproductive potential seemed to be weakened at the site of ovarian lesion of hydrocarbon-intoxicated silver eels (Lopez et al., 1981a,b), scientific proof is lacking and discussion is stillopen. However, several authors (Eisler, 1970; Grauby et al., 1973; Aubert et al., 1977; Marchand, 1981; Canyurt, 1983; Ryan et al., 1984; Hamilton, 1985; Heida and Olie, 1985; Bertrand et al.,1986) agree with the opinion that the eel is more vulnerable than other c o m m o n fish species, molluscs and crustaceans (Eisler, 1970) inhabiting contaminated fresh and marine waters. It is clear that more extensive research is necessary in order to evaluate how pollutants are ecologically detrimental to eel populations and to what extent they are undesirable for their survival. It is also of considerable interest to establish the health hazards to human consumers who use wild or cultured eels as food. Is is important to evaluate the obvious danger of accumulation in the eel of organic pollutants at sublethal doses~ which can lead to acute harmful effects at higher trophic levels, including predatory fish (e.g. cod, conger eel and haddock in marine waters, and salmon anu ~rout in freshwater; Tesch, 1985), eel-eating birds (e,g. cormorants, black-headed gulls and kingfishers; Tesch, 1985; Hernandez et al.,1987; van den Berg et al.,1987) and mammals (e.g. otters and seals, no available data, see Pierce et al., 1989). The main habitats of the eel and their natural food have been investigated in freshwater (Neveu, 1981) and brackish water bodies (Lecomte-Finiger, 1983; De Nie, 1988). A biological magnification process, which consists of increasing pollutant con-

16 c e n t r a t i o n s proceeding t h r o u g h t h e food c h a i n , from i n v e r t e b r a t e s to m a m m a l s , failed to be d e m o n s t r a t e d for eel species. Thus, no ~ n e o u i v o c a l finding exists on such a biological p a t h w a y and m a n y q u e s t i o n s st~ll r e m a i n to be answered. Finally, we need to e n c o u r a g e t h e use of the eel, a t e a c h s t a g e of its developm e n t (glass eel, elver, yellow eel, s i l v e r eel), as a l a b o r a t o r y a n i m a l s u i t a b l e for toxicological tests, as a l r e a d y r e c o m m e n d e d for h y d r o c a r b o n d i s p e r s a n t homolg a t i o n ( A n o n y m o u s , 1977) and r a d i o n u c l i d e s c o n t r o l ( K r u g e r , 1979). Indeed, t h e selection of t h e eel as a t o x i c o l o g i c a l s t u d y m a t e r i a l is r e c o m m e n d e d b e c a u s e of p r a c t i c a l (supply), biological ( e u r y h a l i n i t y ) a n d economic (fishery) advantages. REFERENCES Anonymous, 1977. Homologation des dispersants pdtroliers. Minist. Environ. Cadre de Vie, Paris, 21 pp. Anonymous, 1987a. Rapport du comitd d'experts sur la pollution transfronti~re du Rhin. La Gazette Omcielle de la P~che, Nos 920-921 (27 pp.) and 925-926 (55 pp.). Anonymous, 1987b. Rdsultats d'analyse de Poissons du Rhin. Agence Financi~re de Bassin RhinMeuse. Moulins les Metz, Rapp. No. 11686 D, 6pp. Aubert, J., G. Flatau, D. Puel, V. Breittmayer et R. Clement, 1977. Etude de la contamination des dlevages marins. Rev. Int. Oceanogr. Med., 45-46: 77-97. Awad, H., 1979. Etude comparde de la contamination par les hydrocarbures de deux dcosyst~mes estuariens, th~se Univ. Provence, Marseille, 224 pp. Bertrand, P., S. Fournier et Y. Vigneaulty, 1986. Concentrations en biphenyles polychlords et en mdtaux dans les sddiments de la Baie des Anglais (Qudbec). Rapp. Can. Sci. Halieut. Aquat., 568, 5 pp. Bimbos, D. und G. Mau, 1986. Schadstoffe in hessischen Flussfischen. Situation, Bewertung und Verzehrsempfehlungen. Fischwirt, 36: 69-71. Bolls, L. and J.C. Rankin, 1980. Interactions between vascular actions of detergent and catecholamines in perfused gillsof Europea eel,Anguilla anguilla L. and brown trout, Salmo trutta L. J. Fish Biol., 16: 6173. Brusle, J., 1987. Eel and pollutants, a general review of the effects of heavy metals. Eur. Int. Adv. Comm. (FAO), Working Party on Eel, Bristol, 188 pp. Brusle, J., 1990a. The effects of heavy metals on eels (Anguilla sp). Aquat. Living Res., 3: 131-141. Brusle, J., 1990b. L'anguille europdenne (Anguilla anguilla), une esp~ce jugde commune jusqu'a la derniere dbcennie, mdrite-t-elle d'acqudrir aujourd'hui le statut d'esp~ce menacde? Bull. Soc. Zool. Ft., 114: 61~73. Canyurt, M.A., 1983. Action toxique du lindance et du parathion methyl sur trois esp~ces de poissons d'eau douce. Bull. Cent. Etud. Rech, Sci., Biarritz, 14(3), 257-262. Caries, J.C., 1973. Mdthode analytique de dosages de phenols en solution aqueuse et dans des tissues animaux. Applicaiton /~ la toxicitd des phdnols sur les anguilles. DEA Ecol. USTL, Montpellier, 57 pp. Castonguay, M., J.D. Dutil and C. Desjardins, 1989. Distinction between American eels (Anguilla rostrata) of different geographic origins on the basis of their organochlorine contaminant levels. Can. J. Fish. Aquat. Sci., 46: 836-843. Christiansen, M. and A.J.C. Jensen, 1947. On a recent and frequently occurring tumour disease in eel. Rep. Dan. Biol. Stn., 3244. Christensen, N.O., 1980. Diseases and anomalies in fish and invertebrates in Danish littoral regions which might be connected with pollution. Rapp. P.-V. Reun., Cons. Int. Explor. Mer, 179: 103 109. Cossa D. et P. Maggi, 1973. Toxicitd relative de cinq ddtergents anioniques en milieu marin. 2. Relation entre la bioddgradaion et la toxi~itd aigue. Rev. Tray. Inst. P~ches Marit., 37(3): 419-428. Dave, G., A. Boman, M.L. Johansson-Sjobeck and U. Lidman, 1975. Metabolism effects of PCB

17 (polychlorinated biphenyls)in the European eel (Anguilla anguilla). In: J.H. Koeman and J.J.T.W.A. Strick (Eds), Elsevior, Amsterdam, pp. 197-205. De Nie, W.H., 1988. Faod, Feeding ~eriodicity and consumption of the eel Anguilla anguilla (L) in the shallow eutrophic Tjeukemeer (the Netherlands). In: Food, Feeding and Growth of the Eel (Anguilla anguilla L) l,~ a Dutch Eutrophic Lake. The Univ. Wageningen, pp. 29-51. Desjardins, C., J.D. Dutil et R. Gelinas, 1983. Contamination de ranguille (Anguilla rostrata) du basin du fleuve Saint-Laurent par le mirex. Rapp. Can. Sri. Halieut. Aquat., 141, 18 pp. Dutil, J.D., 1984. Electrolyte changes of serum and muscle, an~ related mortalities in maturing Anguilla rostrata migrating down the 3t Lawrence Estuary (Canada). Helgol. Meeresunters., 37: 425-432. Dutil, J.D. and R. Lallier, 1984. Testing bacterial infection as a factor involved in the mortality of eatadromous eels (Anguilla rostmta) m~tgrating down the St Lawrence Estuary (Canada). Natural. Can. (Rev. Ecol. Syst.), 1;t1: 395-400. Dutil, J.D., B. Legare et C. Desjardins, 1985. Discrimination d'un stock de poissoa, l'anguiile (Anguilla rostrata), bas6e sur la pr~sence d'un produit chimique de svnth~se, le mirex. Can. J. Fish. Aquat. Sci., 42: 455-458. Dutil, J.D., M. Besner and S.D. McCormick, 1987. Osmoregulatory and ionoregulatory changes and associated mortalities during the transition of maturing American eels to a marine envirnn. ment. Am. Fish. Soc. Symp., 1: 175190. Eisler, R., 1970. Acute toxicities oforganochlorine and organophosphorus insecticides to estuarine fishes. Tech. Pap. Bur. Sport Fish. Wiidl. (U.S.), 46" 3-12. Eisler, R., 1972. Pesticide-induced stress profiles. In: M.M. Ruivo (Ed.), Marine Pollution and Sea Life. Fishing News Ltd, pp. 22,9-233. Feral, J.P., P. Fusey, F. Gaill, E. Lopez, E. Martelly, J. Outdot et M. van Praet, 1979. Evolution des teneurs en hydrocmbures chez que~!ques organismes marins du Nord-Finist~re depuis r6chouage de l'Amoco Cadiz et compar~dson des m6thodes de dosages en infrarouge et spectro. fluorimetrie. C.R. Acad. Sci. Paris, 288(7): 713-716. Ferrando, M.D., E. Andrew-Moliner, M.M. Almar, C. Cebrian and A. Nunez, 1987. Acute toxicity of organoehlorinated pesticides to the European eel Anguilla anguilla: the dependency on exposure time and temperature. Bull. Environ. Contain. Toxicol., 39: 365-369. Giam, C.S., H.S. Chan and G.S. Neff, 1978. Phthalate ester plasticizers, DDT, DDE and polychlorinated biphenyls in biota from the Gulf of Mexico. Mar. Pollut. Bull, 9(9): 249-251. Grauby, A., C. Foulquier, B. Descamps and Y. Ja:flent, 1973. R6sultats relatifs h la toxieit6 d'eflluents industriels de la r6gion de Fos et de r6tang de Berre sur les Anguilles, les daphnies, les loups et les muges. CEA, Labo. Radio 6cologie cortinentale, contrat No. VEN-0368. Agence de Bassin RhSne M6diterran6e-Corse, 135 pp. Hamilton, R.M., 1985. Discharges of pesticides to the Rivers Mole and Taw, their accumulation in fish flesh and possible effects on fish stocks. J. Fish. Biol., 27(Suppl. A): 139-149. Heida, H., 1983. TCDD in bottom sediments and eel around a refuse dump near Amsterdam, Holland. Chemosphere, 12(4/5): 505-509 Heida, H. and K. Olie, 1985. TCDD and chlorinated dibenzofurans in top soil and biological samples from a contaminated refuse dump. Chemosphere, 14(6-7): 919-924. Hernandez L.M., M.C. Rico, M.J. Gonzalez, M.C. Montero and M.A. Fernandez, 1987. Residues of organochlorine chemicals and concentrations ~'f heavy metals in ciconiform eggs in relation to diet and habitat. J. Environ. Sci. health, B22(2): 245-258. Holmberg, B. and R.I. Saunders, 1979. The effects of pentachlorophenol on swimming performance and oxygen consumption in the American eel (Anguilla rostrata). Rapp. P.-V. Reun., Cons. Int. Explor. Mer, 174:144 149. Holmberg, B., S. Jensen~ X. Larsson, K. Lewander and M. Olsson, 1972. Metabolic effects of technical pentachlorophenol (PCP) on the eel Anguil'a anguilla L. Comp. Biochem. Physiol., 43B: 171-183. Huschenbeth, E., 1977. Uberwachung der Speicherung yon chlorierten Kohlenwasserstoffen im Fiseh. Arch. Fischereiwiss., 28(2/3): 173-186.

18

Inui, Y., 1968. Pathological study on the effects of carbon tetrachloride poisoning on the eel liver. Bull. Freshwater Fish Res. Lab., i8(2): 157-167. Inui, Y., 1969. Mechanism of the increase of plasma glutamic oxaIacetic transaminase and plasma glutamic pyruvic transaminase activities in acute hepatitis of the eel. Bull. Freshwater Fish Res. Lab., 19(1): 25-30. Janicki, R.H. and W.B. Kinter, 1971. Disrupted osmoregulatory events in the intestine of the eel Anguilla rostrata adapted to seawater. Science~ 173: 1146-1148. Johansson-Sjobeck, M.L., G. Dave and U. Lidman, 1975. Pathological effects of PCB (polychlorinated biphenyls) in the European eel Anguilla anguilla and the rainbow trout Salmo gairdneri. In: J.K. Koeman and J.J.T.W.A. Strick (Eds), Sublethsl Effects of Toxic Chemicals on Aquatic Organisms. Elsevier, Amsterdam, pp. 189-195. Josnin, J.M., 1987. Anguilles, civelles, Des restrictions abusives pvur les p~cheurs professionnels. Aqua Rev., 14: 20-22. King, D.W., H. Mao and L.H. Joanne, 1978. Effects of Dunnall oil spill eliminator on the glycogen, acid and alkaline phosphatase activity of the liver, gill and kidney of the eel (Anguilla japonica). Anat. Rec., 190(2): 612. Kinter, W.B., L.S. Merkens, R.H. Janicki and A.M. Guarino, 1972. Studies on the m~chanism of toxicity of DDT and polychlorinated biphenyls (PCBs): disruption of osmoregulation il~ marine fish Environmental Health Perspectives, US Department of Health, Education and Weif~-we, NIH 88146 pp. 169-173. Kruger, A., 1979. A method of labelling Anguilla anguilla with radionuclides. Rapp. P.-V. Reun. Corts. Int. Explor. Mer., 174: 150-154. Kruse, R., K. Boek and M. Wolf, 1983. Der Gehalt an Organchlor Pestiziden and polychlorierten Biphenylex~ in Elbaalen. Arch. Lebensmitelhyg., 34(4): 81-86. Larsson, P., 1984. Uptake of sediment released PCBs by the eel Anguilla anguilla in static model systems. Ecol. Bull., 36: 62-67. Lecomte-Finiger, R., 1983. R~gime alimentaire des civelles et anguillettes (Anguilla anguilla) dans trois ~tangs saum~tres du Roussillon. Bull. Ecol., 14(4): 297-306. Leloup-Hatey, J. et A. Hardy, 1985. Effet d'une pollution par les hydrocarbures sur la fonction interrdnale de ranguille (Anguilla anguilla L.). Ichthyophysiol. Acta, 9: 39-50. Leloup-Hatey, J., A. Hardy, E. Martelly et Y.A. Fontaine, 1981. Anguilles contamindes apr~s l'~chouage de rAmoco Cadiz. Modifications du fonctionnement de rinterrdnal. C.R. Acad. Sci. Paris, 293: 461-464. Leu,/en, R.S.E.W. and F.G.F. Oyen, 1987. Impact of acidification and eutrophication on the distribution of fish species in shallow and lentic soft waters of the Netherlands: an historical perspective. J. Fish. Biol., 31: 753-774. Lopez, E., J. Peignoux-Deville, F. Lallier, E. Martelly et Y.A. Fontaine, 1981a. Anguilles contami~ades par les hydrocarbures apr~s l'~chouage de rAmoco-Cadiz. Modifications histopathologiques des ovaires, des branchies et de glandes endocrines. C.R. Acad. Sci. Paris, 292: 407-411. Lol~ez, E,, J. Leloup-Hatey, A. Hardy, F. Lallier, E. Martelly, J. Gudot, J. Peignoux-Deville et Y.A. Fontaine, 1981b. Modifications histopathologiques et stress chez des anguilles soumises/t une exposition prolongde aux hydrocarbures. Dans: Amoco.Cadiz; Consdquences d'une Pollution Accidentelle par Hydrocarbures. CNEXO, Paris, pp. 645-653. Marchand, M., 1981. Amoco Cadiz: bilan du colloque sur les consdquences d'une pollution accidentelle par les hydrocarbures. Rapp. Sci. Tech. Publ. CNEXO, Paris 44:86 pp. Miossec, L. et G. Bocquene, 1986. Toxicit~ aigu~ et effects subldtaux, apr~s une courte exposition, de diff~rents nonylphdnols polydthoxylds sur la civelle. Rev. Tray. Inst. P~ches Marit., 48(1-2): 77-84. Mizuhashi, F., 1978. Studies on fish tumors. Master Thesis, Faculty of Fisheries, Mie University, Mie, Japan. Moiler, H., 1981. Fish diseases in German and Danish coastal waters in summer 1980. Meeresforschung, 29: 1-16. Moiler, H., 1985. Fish di:~eases in coastal waters: indicators of marine pollution? Anita. Res. Dev., 22: 106-115.

19 Moiler, H., 1988. Fishchbestande und Fischkrankheiten in der Unterelbe 1984-1986. Verlag ed. Kiel, FRG, 344 pp. Neveu, A., 1981. Variations saisonnibres et journali~-es de l'alimentation de l'anguille (Anguilla anguilla L.)dans des conditions naturelles. Oecol. Appl., 2(2): 99-116. Nounou, P., R. martoja et L. Orcel, 1980. Ulcerations des Poissons et mammif~res marins p~chds dans les eaux c6ti~res francaises. Publ. CNEXO, Paris, Rapp. Sci. Techn., 43:94 pp. Olivereau, M., 1964. L'h~matoxyline au plomb permet-elle l'identification des cellules cortico~ropes de l'hypophyse des t616ost~ens? Z. Zellforsch. 63: 496-505. Peters, G. and N. Peters, 1977. Temperature-dependent growth and regression of epidermal tumors iin the European eel (Anguilla anguilla L.). Ann. N.Y. Acad. Sci., 298: 245-260. Pet,~rs, G. and N. Peters. 1979. The influence of salinity or~ growth and structure of epidermal papillomas of the European eel Anguilla an,quilla L. J. Fish Dis., 2: 1326. Peters, N. and G. Peters, 1984. Papi]lomatosis of eels. Fiches d'identification des maladies or parasites des Poissons. Cons. Int. Exp. Met, fiche No. 1, CIEM, 3-4. Pfitzner, I. und G. Schubert, 1969. Ein Virus aus dem Blut mit Blumenkohlkrankheit behafteter Aale. Z. Naturforsch., 24: 790--792. Pierce, G.J., J.S.M. Diack and P.R. Boyle t989. Digestive tract contents of seals in the Moray Firth area of Scotland. J. Fish. Biol., 35(Suppl. A): 341-343. Pilarczyck, A., 1973. The morphological and histological structure of tumours in the "cauliflower disease" (papilloma) of eels. Acta Ichthyol. Piscatoria, III, 1: 91-106. Roberts, M.R. and R.E. Bendl, 1982. Acute toxicity of kepone to selected f-eshwater fishes. Estuaries, 5(3): 158-164. Ruiz, X. and G.A. Llorente, 1988. Dynamics of E~DT and PCB accumulation in muscle of' carp (Cyprinus carpus) and eel (Anguill~ ang,,illa~ from the Ebro delta, Spain. In: IXth CIESM Workshop Marine Pollution, Athens, Oct. 198:.~. Ryan, J.J., P.Y. Lau, J.C. Pilon, D. Lewis, H.A. McLeod and A. Gervals, 1984. Incidence and levels of 2,3,7,8-tetrachlorodibenzo-p-dioxin in Lake Ontario ~'ommercial fish. Environ. Sci. Technol., 18: 719-721. Saroglia, M.G., G. Scarano and E. Tibaldi, 1981. Acute toxiv~ty of nitrite to sea bass (Diee~tra,'e:hus labrax) and European eel (Anguilla anguilla). J. World Mar. Sci., 12(2): 121-126. Schachter, D., M. Marilley et A. Kiener, 1969. Pollution dc l'~'~tant de l'Olivier par du lindance en Septembre 1967. Mortalit~ de la faune. Bull. Fr. Piscicult.. 232: 83-89. Schaperclaus, W., 1953. Die Blumenkohlkrankheit der Aale u,~d anderer Fische der Ostsee. Z. Fisch. Deren Hilfswiss., 2: 105-124. Schubert, G., 1969. Elektronenmikroskopi~che UJ~tersuchungen an der Haut mit Blumenkohlkrankheit behafteter Aale. Fischereiwiss., 20:36 50. Sims, G.G., J.R. Campbell, F. Zemlyak and J.M. Graham, 1977. Organochlorine residues in fish and fishery products from the Northwest Atlantic. Bull. Environ. Con:am. Toxicoi., 18: 697705. Tesch, F.W., 1985a. Corresponding strong decreases in eel larvae and River Eros glass eel catches. Eur. Inl. Adv. Comm. (FAO), Working Party on Eel, Perpigr, an, 3 pp. Tesch, F.W., 1985b. A review on the competitive situation of the eel in relation to other species. EIFAC Working Party on Eel, Perpignan, 30 pp. Turgeon, C. et G Beaulieu, 1973. Pr4sence de mercure dans l'anguille d'Am~rique Anguilla rostrata. Direction g~nSrale des p~ches maritimes, Quebec, Rapport Annuel, pp. 259-266. Van den Berg, M., F. Blank, C. Heeremans, H. Wagemar and l:. Olie, J9,~7. Presence of polychlorinated dibenzo-p-dioxins and polychlorinated dibenzofur~,ns in fish.,,ating birds and fish from the Netherlands. Arch. Environ. Contam. To:-iccl., I~: I~9-~;~8. Yamagata, Y. and M. Niwa, 1982. Acute and cb~'onic toxici':y of atom.or is to oel Anguilla japonica. Bull. Jpn. Soc. Sci. Fish., 48(2): 171-176.