J. Great Lakes Res. 19(4):766-775Internal. Assoc. Great Lakes Res., 1993

Toxic Compounds and Health and Reproductive Effectsin St. Lawrence Beluga Whales

Pierre Beland,l Sylvain DeGuise,l,2 Christiane Girard,2 Andre Lagace,2Daniel Martineau,l,3 Robert Michaud,l Derek C.G. Muir,4 Ross J. Norstrom,S

Emilien Pelletier,6 Sankar Ray,7 and Lee R. Shugart8

1St. Lawrence National Institute ofEcotoxicology,460 du Champ-de-Mars, suite 504, Montreal, Quebec H2Y IB4

2Faculte de Medecine Veterinaire, St-Hyacinthe, CP 5000,St-Hyacinthe, Quebec J2S 7C6

3NY State College ofVeterinary Medicine, Cornell University,Ithaca, New York 14853

4Department ofFisheries and Oceans Canada, Freshwater Institute,501 University Crescent, Winnipeg, Manitoba R3T 2N6

5Environment Canada, National Wildlife Research Center,100 boul. Gamelin, Hull, Quebec KIA OH3

6INRS-Oceanologie, 310 allee des Ursulines, Rimouski, Quebec G5L 3AI

7Toxicology Section, Science Branch, Fisheries and Oceans Canada, PO Box 5667,St John s, Newfoundland AlC 5XI

8Environmental Sciences Division, Oak Ridge National Laboratory,PO Box 2008, Oak Ridge, Tennessee 37831

ABSTRACT. An epidemiologic study was carried out over a period of 9 years on an isolated popula­tion of beluga whales (Delphinapterus leucas) residing in the St. Lawrence estuary (Quebec, Canada).More than 100 individual deaths were aged, and/or autopsied and analyzed for toxic compounds, and thepopulation was surveyedfor size and structure. Arctic belugas and other species ofwhales and seals fromthe St. Lawrence were used for comparison. Population dynamics: Population size appeared to be stableand modeling showed this stable pattern to result from low calfproduction and/or low survival to adult­hood. Toxicology: St. Lawrence belugas had higher or much higher levels of mercury, lead, PCBs, DDT,Mirex, benzo[a]pyrene metabolites, equivalent levels of dioxins, furans. and PAR metabolites, and muchlower levels of cadmium than Arctic belugas. In other St. Lawrence cetaceans, levels of PCBs and DDTwere inversely related to body size, as resulting from differences in metabolic rate, diet, and trophic posi­tion. compounded by length of residence in the St. Lawrence basin. St. Lawrence belugas had muchhigher levels than predicted from body size alone; levels increased with age in both sexes, althoughunloading by females through the placenta and/or lactation was evidenced by overall lower levels infemales and very high burdens in some calves. No PCDDs and only low levels of some PCDFs weredetected in St. Lawrence belugas. while proportions of toxic non-ortho (coplanar) PCBs were low rela­tive to proportions seen in other species. At least ten different PCB methylsulphone metabolites weredetected in St. Lawrence belugas. Levels ofB[a]P adducts to DNA in St. Lawrence beluga brain and liverapproached those associated with carcinogenis in small laboratory animals. Pathology: St. Lawrence bel­ugas were not emaciated. and major findings were: a high prevalence of tumors (40% ofanimals) includ­ing eight malignant neoplasms; a high incidence of lesions to the digestive system (53%), to the mam­mary glands (45% of adult females), and to other glandular structures (11%); some evidence ofimmuno-suppression; frequent tooth loss and periodontitis. Two animals had severe ankylosing spondylo­sis and another was a true bilateral hermaphrodite. No such lesions were observed in 36 necropsies ofArctic belugas and of seals and cetaceans from the St. Lawrence.

INDEX WORDS: Beluga whales, St. Lawrence River, PCBs, toxic substances, population dynamics.

766

St. Lawrence Beluga Whales 767

INTRODUCTION

The St. Lawrence estuary and adjacent waters ofthe Gulf of St. Lawrence in Eastern Canada are thesole year-round habitat for a small isolated popula­tion of beluga whales (Delphinapterus Ieucas). Acommercial hunt lasting into the middle of this cen­tury reduced the population from several thousand toa few hundred animals (Reeves and Mitchell 1984).Among suspected causes for its recent failure to re­cover, the possible impact of toxic compounds origi­nating from the Great-Lakes / St. Lawrence basinwas suggested by Martineau et al. (1987). A long­term study of this population was initiated in 1982,eventually covering distribution, habitat, photo-iden­tification, behavior, population dynamics, toxicology,and pathology. The following is a summary of majorfindings relating to the hypothesis that exposure totoxic compounds has a significant impact on life-his­tory parameters and individual health in this popula­tion. For this purpose, a series of animals found deadon the shore or drifting at sea were examined over an8-year period, while other marine mammals from thesame environment and beluga whales from the Arc­tic were used as controls.

RESULTS AND DISCUSSION

Population Dynamics

NumbersEight aerial surveys betyveen 1987 and 1992 to

define distribution and group sizes reported anaverage total of 461 animals (cv = 9.2%; Michaud1993). Although these surveys were not designed toestimate actual numbers, and the population may besomewhat larger, the low coefficient of variationsuggests that it is stable in numbers.

Mortality and Age-structureThe average number of deaths reported per year is

14.5, which is equivalent to a minimal overall deathrate of 3,2% (assuming a population of 450 animals).The age structure of the carcasses (n =103) that wereexamined over an 8-year period shows mortality tobe increasing at an early adult age (Fig. 1). Mortalityin the first year of life is likely to be higher thanmeasured, as dead calves are less likely to be found(Caughley 1977), especially in a large estuarine sys­tem. The observed mortality curve is unlike the U­shaped curve typical of long-lived mammals withfew offspring. Modeling using Leslie matrices sug-

20 1982·90

II) n = 103iij:l'0"S;:'6 10.50z

oo 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30

Age (years)

FIG. I. Age structure of beluga whales (DeJphi­napterus leucas) found dead in the St. Lawrence,1982-1990.

gests that when such a population is stable in num­bers and structure, juveniles (grey animals, or allthose between ages 1 and 6) account for 28%-30% oftotal numbers, indicating relatively low calf produc­tion and/or survival to adulthood (Beland et al.1988). Estimates from field surveys reported 31% ju­veniles (Michaud 1993), in accordance with predic­tions from the model, but definitely lower than inArctic populations (Sergeant 1986).

ReproductionBums and Seaman (1985) reported that in a sam­

ple of 171 belugas killed in Alaska, 35% of femaleswere nongravid, 35% were newly pregnant, and30% had term foetuses or had recently given birth.Among 34 females found dead in the St. Lawrence,ratios were 79%, 3%, and 18% respectively. Con­trary to Alaskan females, where reproduction oc­curred until maximum age, none of the St.Lawrence females above age 21 were pregnant orshowed evidence of a recent pregnancy. Brodie(1971) and Sergeant (1973) described ovarian activ­ity in Arctic belugas, observing an increase withage of the number of corpora a1bicantia and corpora1utea, from none before sexual maturity to 10-15 atage 25+. Fewer corpora were seen in St. Lawrencebelugas, although serial sectioning was not done inmany animals. Because of the frequent presence ofaccessory follicles, and the obvious fact that ovula­tion does not equal successful pregnancy, Bums andSeaman (1985) concluded that corporal counts can­not be used to infer the number of past pregancies.They proposed to base average female productivitysolely on the presence in mature females of an ac­tive corpus luteum associated with a foetus. Theyobserved this co-occurrence in 110 of 171 females

768 Beland et al.

(64%); in our study, there was a single case out of22 females (4.5%), a highly significant difference(chi2 =30.1, P <0.001). Finally, a high frequency oflesions to mammary glands was observed (36% offemales examined), seriously compromising normalfeeding of young. This constitutes a definite handi­cap, in a species where calves are thought to sucklefor more than 1 year. The above differences be­tween Arctic and S1. Lawrence belugas may besomewhat biased, as samples were obtained throughdifferent means. They nevertheless show that a sig­nificant portion of the St. Lawrence female popula­tion is not as productive as Arctic populations.

Toxicology

Chemical analyses on S1. Lawrence beluga whaletissues have demonstrated that this whale populationhas been exposed over a long period of time to a va­riety of organic and metallic chemicals of industrialand agricultural origin (Martineau et at. 1987, Masseet al. 1986, Muir et at. 1990, Norstrom and Simon1990, Ray et al. 1991, Shugart et al. 1990, Wage­mann et at. 1990, Beland et al. 1992).

MetalsA comparative study of toxic metals in belugas

from several populations (Wagemann et al. 1990)showed that only mercury, lead, cadmium, and sele­nium definitely set S1. Lawrence belugas apart fromArctic whales (Table 1). As in other mammals, mer­cury accumulated with age in the liver of S1.Lawrence whales, but levels were higher than in

most cetaceans of the northern hemisphere (see re­view in Wagemann et al. 1990). As elsewhere(Koeman et al. 1973, Wagemann et al. 1983,Norstrom et al. 1986), high selenium levels werecorrelated with high mercury levels. Lead concen­trations in liver and muscle tissues were about tentimes higher in S1. Lawrence than in Arctic belugas.On the contrary however, S1. Lawrence belugawhale tissues contained much less cadmium thanthose of Arctic belugas and of most other marinemammals from the northern hemisphere.

The toxic effects of chronic exposure to heavymetals have been little studied in marine mammals.In man, mercury toxicity becomes evident when totalbody burden exceeds 20 mg, which has been set asthe acceptable limit in Ontario, Canada. Assumingcomparable effects and the same pharmacodynamicsfor mercury in whales, Beland et at. (1992) estimatedfrom data on body weights and from mercury levelsin tissues, that an exposure equivalent to the humantolerance limit would be attained by age 19 in belugawhales of the S1. Lawrence.

Organochlorines: overviewA comparative study of various organochlorine

compounds in belugas from most Canadian popula­tions found that the same compounds were present inall populations (Muir et at. 1990). All were at lowlevels in Arctic animals, but generally at higher lev­els in belugas from the S1. Lawrence (Tables 2, 3).High levels of three groups of compounds, PCBs,DDT, and Mirex, clearly distinguished S1. Lawrence

TABLE. 1. Mercury, cadmium, lead, and selenium in the liver ofbeluga whales from Canadian waters.

Population

ArcticHudson BaySt. Lawrence

n

941535

Age(avge)

11.413.217.5

Mercuryppm

0,04 - 1820,60 - 1521,42 - 756

Cadmiumppm

0,03 - 973,47 - 39,6<,005 - 1,5

Leadppm

<0,001- 1,160,039 - 0,600,004 - 2,13

Seleniumppm

0,92-87,42,88-28,52,72-307

Ranges, in dry weights, from Wagemann et ai. 1990.

TABLE 2. Major organochlorine contaminants in the blubber ofbeluga whales from Canadian waters.

PCBsOrigin Sex Age ppm

Arctic M 0-33 1,88-5,09Arctic F 0-24 0,31-6,73St. Lawrence M 4-23 53,9-89,2St. Lawrence F 2-29 14,5-68,7

Ranges, in wet weights, from Muir et al. 1990. nd = not detected.

DDT-totppm

1,23-9,730,18-5,9552,4-1233,95-42,7

Mirexppm

nd-0,06nd-0,03

0,19-1,540,38-2,66

St. Lawrence Beluga Whales

TABLE 3. Organochlorine contaminants in the blubber ofSt. Lawrence belugas.

769

males, ppm (sd), n = 4 females, ppm (sd), n =5

Compound mean

Age 17.5 (9.1)% lipids 86.8 (2.7)HCB 1.34 (0.44)sum CBz 1.34 (0.44)gamma HCH 0.10 (0.01)sum HCH 0.37 (0.11)t-nonachlor 3.67 (0.30)sum CHLOR 7.43 (0.63)4-4'DDE 65.8 (19.1)sum DDT 101 (32.6)PCC 14.7 (2.46)Mirex 1.00 (0.64)Dieldrin 0.93 (0.12)sumPCBs 75.8 (15.3)

range

4.0-23.583.2-89.60.82-1.900.82-1.900.09-0.120.28-0.513.25-3.916.54-8.0238.5-80.652.4-12311.7-17.60.19-1.540.81-1.0653.9-89.2

mean

15.6 (l0.4)86.6 (3.9)

0.60 (.043)0.60 (.043)0.11 (0.03)0.24 (0.10)1.86 (0.86)3.55 (1.99)13.9 (11.3)23.0 (17.3)6.34 (3.51)1.11 (0.99)0.56 (0.31)37.3 (22.0)

range

2.5-29.080.4-91.40.22-1.270.22-1.270.08-0.140.12-0.320.87-2.821.50-6.381.73-26.83.95-42.72.05-10.30.38-2.660.21-0.8714.5-68.7

Wet weights, from Muir et aZ. 1990.HCB: hexach1orobenzene; CBz: ch1orobenzene isomers; HCH: hexachlorocyclohexane isomers;CHLOR: chlordane-related compounds; PCC: toxaphene.

whales; all three increased exponentially with age.PCB and DDT levels were lower in females, mostlikely as a result of significant transfer to offspringthrough placenta and milk, but did not plateau as inother species of marine mammals. This is interpretedas an indication of low calf production or low calfsurvival; it is corroborated by the finding of highestsingle values of organochlorines in very young ani­mals, which would then be more likely to suffer fromthe known toxic effects of these compounds.

The tissues of other St. Lawrence marine mam­mals showed very little Mirex and generally muchlower concentrations of PCBs and DDT than tissuesof beluga whales. PCBs and DDTtot levels were in­versely related to species size (Fig. 2). These resultswere interpreted as resulting from diet, from rela­tive length of food chain, from time of residence inthe contaminated system of the St. Lawrence, andfrom Kleiber's law inversely relating metabolism tobody size (Beland et at. 1992) . Compared to otherspecies, St. Lawrence beluga whales were muchmore contaminated than predicted on the basis ofbody size alone.

MirexThis compound best distinguishes Arctic from St.

Lawrence belugas, being on average 72 times moreabundant in the blubber of the latter. Mirex origi­nates essentially from Lake Ontario (Durham andOliver 1983), from where it has found its way

60 Beluaa1200 kg

m50 ,

EQ, 40.8 m

mtil 30 m mlD(,) 20 m11. III

10 m m Bm m

0kg: 100000 75000 10000 3000 250 70

BM BP BA GM LA pp

Species and weight

FIG. 2. Total PCBs (Ilg/g) in the blubber of St.Lawrence cetaceans (all ages and sexes). Body weightsare approximate maxima for species. BM: Blue whale(Balaenoptera musculus), BP: fin whale (Bal­aenoptera physalus), BA: minke whale (Balaenopteraacutorostrata), GM: pilot whale (Globicephalamelaena), LA: white-sided dolphin (Lagenorhynchusacutus), PP: harbour porpoise (Phocoena phocoena).In comparison, PCB levels in beluga whales rangefrom 5 to 600 ppm. From Biland et al. 1992.

downstream into the St. Lawrence through particu­lates and migrating fauna. A mass-balance equationsuggests that all the Mirex, and about half of otherorganochlorine compounds present in beluga tis­sues, could derive from a relatively small number ofLake Ontario eels, Anguilla rostrata. These wouldbe consumed by belugas when the adult fish passthrough their range during the annual fall migrationof eels toward the Atlantic (Beland, unpubl. data).

770 Beland et at.

TRI TETRA PENTA I-EXA HEPTA OCTA I\ICNA

PCB Homologs

FIG. 3. PCB homologs in an Aroclor standard and inbeluga blubber from the St. Lawrence estuary (afterMuir et al.1990).

DDTThe major DDT component was 4,4'-DDE which

represented 66% and 57% of total DDT in St.Lawrence belugas, and was the most abundant ofall organochlorine compounds (Table 2). The ex­tremely high levels of DDTtot in belugas are similarto or higher than in other Canadian East Coastcetaceans, all reflecting the past heavy use of thepesticide for agricultural and forestry uses.DDE/DDTtot ratios approaching 0.6 suggest oldrather than recent DDT inputs (Aguilar 1987, Mar­tineau et al. 1987).

PCB CongenersA total of 60 PCB peaks representing 65 con­

geners were identified in beluga blubber, withtwelve congeners accounting for more than 50% ofthe total. In St. Lawrence belugas, hexa- and hep­tachloro congeners predominated (Fig. 3), and thehomolog pattern resembled a 1: 1 mixture of Aroclor1254:1260 more closely than did the pattern in Arc­tic animals. PCB-153, -138, -187/182 and -180 (allsubstituted at the 2,4 or the 2,4,5- positions on bothphenyl rings) accounted for a higher proportion ofPCBs in St. Lawrence male belugas. The differencesin profiles probably reflect differences in pathwaysof PCB contamination, with atmospheric deposition,as opposed to local discharge, being the majorsource for Arctic food webs (Muir et al. 1990). Theyare also likely indicative of greater metabolic activ­ity in the more contaminated animals due to mixedfunction oxidase induction by xenobiotics (Mar­tineau et al.1987, Muir et al. 1990), so that only themost recalcitrant structures remain. St. Lawrencebeluga blubber contained only minute amounts ofPCB congeners substituted with a single chlorine

Dioxin-like CompoundsDioxins (PCDDs) and furans (PCDFs) were found

in very small amounts or not at all in tissues of St.Lawrence belugas (Norstrom and Simon 1990, Be­land et al. 1992). None were detected in liver tissues,while no PCDDs and only small amounts of PCDFs,all not fully substituted at the 2,3,7,8 positions, werefound in blubber (maximum concentration of 8-31ng/kg). Major congeners were three H6CDFs, domi­nated by l24689-H6CDF, and two P5CDFs, 12478­and l2489-P5CDF. This distribution was interpretedas indicative of chlorophenol and pentachlorophenolsources rather than combustion or Aroclor sources(Norstrom and Simon 1990).

The total absence of PCDDs in St. Lawrence belu­gas was unexpected in view of the knownT4CDDIPCB ratios in Lake Ontario fauna, and of itscontribution to downstream ecosystems, as demon­strated by Mirex levels in belugas. Total PCB levelsin beluga were 14 times higher in the St. Lawrencethan in an Arctic sample, but TCDD was unde­tectable in animals from both areas (Norstrom et al.1992). Rough calculations would have predictedT4CDD concentrations in the blubber of St.Lawrence belugas in the range of 10-200 ng/kg fromLake Ontario alone, without allowing for furthercontributions from downstream sources such aspaper mills. These results, which are similar to thosefrom narwhal (Norstrom et al. 1990, 1992) and fromoffshore killer whales, Orcinus orca, (Ono et al.1987) suggest that some odontocetes possess a cy­tochrome P-450 CYPlA-type enzyme with the capa­bility of metabolizing TCDD-like substrates(Norstrom et al., 1992). This is consistent with theabove findings regarding PCB congeners with noortho chlorine substitution and at least two meta­para chlorine substitutions on both rings (coplanarPCBs), a structure which is similar to that of PCDDs.

PAHsAnalytical extraction and quantification in mus­

cle, brain, liver, and kidney tissues of St. Lawrence

atom (tetrachloro-#60, pentachloro-#105, hexa­chloro-#156) or with no chlorine atom (tetrachloro­#77, pentachloro-#126, hexachloro-# 169) in anortho position (2,2',6,6') (Table 4). Some ten differ­ent PCB methylsulphone congener metabolites wereidentified in beluga whale tissues (Kuroki et al.1991). These secondary metabolites have intriguingtoxic properties in other species, such as highly spe­cific binding to lung tissue.

• males• femaleso Aroclor

12421254: 1260

40

o

~ 30U0.E 20

~'0 10

St. Lawrence Beluga Whales

Table 4. Concentrations ofcoplanar PCB congeners in the blubber ofSt. Lawrence beluga whales.

As Percentages ofConcentration (pg/g) Total PCBs (x104)

Congen. #IUPAC: #77 # 126 # 169 #77 # 126 # 169

Females (n =5)Average 660.0 1,786.7 220.2 25.0 60.8 11.9std dev. 682.3 1,616.5 170.3 18.0 7.83 13.6

Males (n =5)Average 1,245.7 3,607.6 251.9 17.8 51.7 3.3std dev. 1,270.0 3,367.3 380.6 2.87 1.32 2.84

wet weights

771

belugas showed little or no PAHs (Beland et al.1992). This was to be expected, as PAHs are readilydegraded by fish and mammals, and only metabo­lites remain, usually identifiable as adducts to pro­teins or DNA.

Using the highly sensitive 32P-postlabeling tech­nique, Ray et al. (1991) found detectable levels ofaromatic DNA adducts (16-158 nmole adducts /mole total nucleotides) in all beluga whales sampledfrom two sites in the Canadian Arctic and from theSt. Lawrence estuary. Average levels at both loca­tions were comparable, suggesting that exposure ofwhales to varied and ubiquitous PAHs, many ofwhich originate from natural sources, is generalized.This method measures adducts originating from anybulky aromatic compound, and it is not knownwhether some may originate from internal processesnot related to PAH exposure (Randerath et al. 1986),particularly in populations that differ in terms of theactivity level of their detoxifying enzymatic sys­tems. Kurelec et al. (1989) have recently reportedthat the background levels of adducts detectable bythis technique can completely override any pollutionrelated adducts. Only in extremely polluted environ­ments would injury beyond background levels bemeasurable. In dry weight, Mackenzie delta sedi­ments contain 650-840 ppb of total PAHs (Ray et al.1991), and the more contaminated sediments of theSaguenay River contain 500-4,500 ppb (Martel et al.1986), compared to 48,000 ppb in Buffalo Riversediments (Black 1983). Dunn et al. (1987) andVaranasi et al. (1989) found high levels of pollution­related adducts in fish where sediments contained upto 72,000 ppb of PAHs in dry weight.

Using an HPLC method coupled with fluores­cence detection, adducts specific to benzo[a]pyrene(B[a]P) were detected in St. Lawrence belugas, butnot in Arctic belugas (Martineau et al. 1988,

Shugart et al. 1990, Pelletier et al. 1990). Levels inbrain and liver tissues approached or exceededthose found in animals, both terrestrial and aquatic,exposed under controlled laboratory conditions to acarcinogenic dose of B[a]P (Martineau et al. 1988,Pelletier et al. 1990). It is not known howeverwhether the levels attained resulted from acute orchronic exposure, nor to what extent the health ofthe animals influenced the formation of adducts(Shugart et al. 1990). B[a]P, as a by-product of alu­minum smelting, has been deposited in large quan­tities in the Saguenay River basin from the 1930sup to this day (Martel et al. 1986). Its bio-availabil­ity was demonstrated in an experiment in whichmussels transplanted to the Saguenay mouth accu­mulated B[a]P to levels much above regional back­ground (Picard-Berube and Cossa 1983).

Pathology

Among the dead beluga whales recovered be­tween 1983 and 1990, 45 (20 males, 25 females)fresher specimens were necropsied at the Faculty ofVeterinary Medicine, University of Montreal, in St­Hyacinthe, Quebec (Martineau et al. 1985, 1986,1988; Girard et al. 1991; Beland et al. 1992, andunpubl. data). The age structure of these whaleswas representative of the larger sample shown inFigure 1. Sculp (skin and blubber) weights were al­most all within the range of freshly killed Arctic an­imals, and emaciation was present in only threecases. Findings from macroscopic and histopatho­logical examinations are summarized below.

NeoplasmsEigtheen animals (40%) had at least one neo­

plasm (in four other suspected cases, autolysis pre­cluded conclusive histopathological examination).

772 Beland et aI.

Various tissues were affected, and eight neoplasmswere malignant (Table 5). Most of these neoplasmshad rarely or never been reported in cetaceans be­fore. These 24 tumors amount to more than half thetotal number of 41 tumors ever reported fromcetaceans of the world (Geraci et al. 1987). Whalesin our sample were between 16 and 29+ years ofage; knowing the age structures of the animals ofother species with neoplasms would help in furtherinterpreting the observed differences. However, itwould appear that beluga whales in the St. Lawrenceare exposed to one or more potent carcinogens, andthe diversity of tumors suggests that. more than onetype of chemical compounds may be involved.

Digestive SystemOverall, the digestive system was the site of more

lesions, and of a wider variety, than other tissues.Tooth loss was common (Fig. 4), with or withoutobservable periodontitis; less than 60% of animalshad the normal complement of 28-36 teeth. Ulcersin the mouth, the esophagus, the first two gastriccompartments (with perforation in two cases), andthe intestine were frequently observed. More thanhalf of all neoplasms were found in tissues of thedigestive system, including five malignant tumors;nine animals had gastric papillomas, a lesion rarelyobserved in domestic animals (Head 1990) andcetaceans (Geraci et al. 1987). Parasites were gen­erally found in low to moderate quantities, withoutcausing significant damage; three animals were ex-

ceptions, being heavily parasitized by nematodes(Anisakis sp.) in one case, and tapeworms (aff. Di­phyllobotrium) in two cases. Tapeworms had beenreported only once before in beluga whales(Kleinenberg et al. 1964). Interestingly, the diges­tive system is also the more common site of lesionsdescribed from beluga whales that died in captivity(Steuer 1989).

Respiratory SystemSixteen belugas had pneumonia, mostly of parasitic

nematode origin. Six additional animals had otherpulmonary lesions, bringing to 22 (out of 45, or 50%)the number of animals with lesions to the respiratorysystem. Three animals had lesions not reported beforein cetaceans: bronchial polyp, pulmonary chon­droma, and ciliate protozoan pneumonia. The latter issuggestive of immune suppression.

Endocrine SystemTen animals had hyperplasic nodules and cysts to

adrenal glands. There were single cases each ofmultinodular goitre and thyroid abcess.

Reproductive SystemApart from one case of testicular necrosis, male

reproductive organs appeared normal. One adultanimal was a true bilateral hermaphrodite. Femalereproductive activity and success were low, as evi­denced by rate of pregnancies and by ovarian activ-

TABLE 5. Twenty-four neoplasms (* =malignant)observed in eighteen beluga whales (Delphinapterusleucas)from the St. Lawrence in a series of 45 necrop­sies, 1983-1990.

No. teeth

11-15 16-20 21·25 26-31 32-370·5 6-10o

30 Delphinapterus leucas

III 51. Lawrence Estuaryiii::l

"'5 20i5.!:oz 10

FIG. 4. Tooth loss in beluga whales, Delphi­napterus leucas, (calves not included) found deadin the St. Lawrence Estuary, 1982-91. Accordingto Doan and Douglas (1953) and Kleinenberg etaI. (1964), Arctic beluga whales have between 24and 44 teeth; alveoli in St. Lawrence belugasnumbered 28-37.F 22, 24

F 21+M 20,29+M 19, 28+F 22+M 16M 19+F 22+F 24, 25M 18+

M 24+M-F 14-29+

No. ofSex Age(s)Neoplasms cases

Salivary gland adenocarcinoma* 1Gastric (1st compart.) papilloma 9Gastric (2nd compart.)

adenocarcinoma* 1Intestinal adenocarcinoma* 2Splenic fibroma 2Hepatocellular carcinoma* 1Bladder carcinoma* 1Bladder haemangioma 1Mammary adenocarcinoma* 1Ovarian tumor 2Thymic lymphosarcoma* 1Pulmonary chondroma,

pulmonary lipoma 2

St. Lawrence Beluga Whales 773

ity (in terms of the numbers of visible copora luteaand corpora albicantia). There were two cases ofovarian tumors, and one case of ovarian cyst. Twoof the 25 females necropsied had died of dystocia.Mastitis, either purulent, necrotic, subacute, orchronic, were present in one or both mammaryglands of 9 females (36%).

Museulo-skeletal SystemTwo adult animals (out of 45, or 4.4%) had anky­

losing spondylosis, aggravated by scoliosis in onecase. Among the 125 or so live animals that havebeen photo-identified in the St. Lawrence, eight(one calf, three juveniles, and four adults) havevery conspicuous spinal deformations resemblinglordosis and/or scoliosis. In a popupation totallingsome 450-500 animals, these animals would repre­sent a proportion near 2%. The etiology of theseconditions is unknown, and one can only speculateon the relative importance of developmental prob­lems, possibly induced by chemical aggressions, asopposed to genetic expression of rare traits in a rel­atively small population.

Multisystemie and Viral LesionsFour juvenile animals had moderate to severe

multisystemic lesions. A skin lesion was associatedwith a herpes virus-like particle, not previously iso­lated or observed in cetaceans; the same agent wasobserved subsequently in an identical condition af­fecting captive beluga whales (Barr et al. 1989).Most adults had more than one severe chronic lesion.

BacteriologyMost bacteria identified in various tissues were

opportunistic species on animals already debilitatedby other conditions. There was one case of sys­temic nocardiosis, a condition usually present inold or immune suppressed animals.

ParasitologyMost animals had a few species of parasites, in

low to moderate numbers, except in three caseswith severe intestinal or gastric infestations as re­ported above.

For reference, five Arctic beluga whales (ages 3­21 +) from the Inuit hunt at Eskimo Point (HudsonBay, NWT), as well as thirteen cetaceans (ages 0­9+) belonging to four species and seventeen pin­nipeds (ages 0-22) of three species found dead along

the St. Lawrence system were necropsied. Only oneand the same lesion, a moderate eosinophilic gastro­enteritis, was observed in the five Arctic belugas.The major cause of death (half of the cases) amongthe thirty St. Lawrence marine mammals other thanbelugas was direct human action (fishing gear andvarious traumas, including firearms and boat hull orpropeller injuries), a factor of no significance in bel­uga whale mortality. No neoplasms, nor any of thechronic lesions currently observed in belugas fromthe same environment were found in St. Lawrencecetaceans and pinnipeds.

CONCLUSION

Almost all toxic chemicals considered as criticalin the Great Lakes ecosystem (Canada 1991),namely mercury, lead, PCBs, DDT, mirex, toxa­phene (PCC), HCB, dieldrin, and benzo[a]pyrenewere also the more abundant, and some at very highlevels, in St. Lawrence beluga whales. The only no­table exceptions were dioxin-like compounds (diox­ins, furans, coplanar PCBs) which were absent or invery low amounts. This suggests that belugas maybe able to metabolize TCDD-like compounds, al­though toxicity may be incurred from resultingmetabolites (Norstrom et al. 1992).

The same whales in which the above toxic com­pounds were measured showed a series of rarelyobserved chronic lesions, some evidence for im­mune suppression and reproductive impairment, aswell as a high incidence of neoplasms. Many ofthese lesions or impairments have been observedin terrestrial and freshwater animals, both in thelaboratory and in the wild, with equivalent orlower concentrations of the same chemicals (seediscussions in Martineau et al. 1987, 1988). Onthe contrary, none were found in much less conta­minated Arctic beluga whales nor in cetaceans andseals from the St. Lawrence, a difference that can­not be explained solely by the fact that half ofthese animals had been killed voluntarily or acci­dentally.

The sample of St. Lawrence beluga whales exam­ined is representative of mortalities and ofprocesses that are still active in the live population.The design of the present study and the nature ofthe target species did not allow the traditional clini­cal approach required to demonstrate specific ef­fects of any given chemical on the whales. It wasalso not possible to measure physiological or be­havioral responses in live animals. Evidence pre-

774 Beland et al.

sented here regarding decreasing productivity of fe­males with age would agree with a dose-responserelationship between organochlorines in the diet,and impaired reproduction and vitamin A defi­ciency in seals (Reijnders 1986, Brouwer et ai.1989). It would however be illusory to try and linka specific contaminant to a given observed effectwhen several toxic compounds are present and ac­tive simultaneously in so many tissues of a givenanimal. Whereas results from epidemiologic studiesare equivocal with regards to the carcinogenicity oforganochlorines, they are collectively known asfunctional teratogens that alter endocrine, immune,metabolic, and neurologic functions through vari­ous mechanisms that are particularly active duringthe maturation process (see other papers in this spe­cial section). The evidence presented here supportsa causal relationship between several compounds ofknown toxicity and the health and reproductive im­pairments observed in beluga whales of the St.Lawrence. We believe that the more feasible ap­proach for definitely establishing a first link wouldbe through an assessment of the immune functionsof St. Lawrence beluga whales.

ACKNOWLEDGMENTS

This study was funded by Fisheries and OceansCanada and the Wildlife Toxicology Fund, an initia­tive of World Wildlife Fund Canada and Environ­ment Canada, with contributions from the St.Lawrence Action Plan, Alcan, the Fondation de laFaune du Quebec, Environnement Quebec, andGreenpeace (Canada).

REFERENCESAguilar, A 1987. Using organochlorine pollutants to dis­

criminate marine mammal populations: a review and cri­tique of the methods. Mar. Mammal Sci 3:242-262

Barr, B., Dunn, J.L., Daniel, M.D., and Banford, A. 1989.Herpes-like viral dermatitis in a beluga whale. J. Wildl.Dis. 25:608-611.

Beland, P., Vezina, A, and Martineau, D. 1988. Potentialfor growth of the St. Lawrence (Quebec, Canada) belugawhale (Delphinapterus leucas) population based onmodelling. J. Cons. into Explor. Mer. 45:22-32.

___, De Guise, S., and Plante, R. 1992. Toxicologyand pathology of St. Lawrence marine mammals. Rept.Wildlife Toxicology Fund, World Wildlife Fund(Canada), Toronto.

Black, J.J. 1983. Field and laboratory studies of environ­mental carcinogenesis in Niagara River fish. J. GreatLakes Res. 9:326-334.

Brodie, P.P. 1971. A reconsideration of aspects of growth,

reproduction and behavior of the white whale, Delphi­napterus leucas, with reference to the CumberlandSound, Baffin Island, population. J. Fish. Res. BoardCan. 28:1309-1318.

Brouwer, A.P., Reijnders, J.H., and Koeman, J.H. 1989.Polychlorinated biphenyl (PCB) contaminated fishinduces vitamin A and thyroid hormone deficiency inthe common seal (Phoca vitulina). Aquat. Toxicol.15:99-106.

Burns, J.J., and Seaman, G.A. 1985. Investigations ofbelukha whales in coastal waters of western and north­ern Alaska. II. Biology and ecology. Rept. Alaska Dept.Fish & Game, Contr. NA 81 RAC 0049.

Canada. 1991. Toxic chemicals in the Great Lakes andassociated effects, 2 vols. Environment-, Fisheries andOceans-, and Health and Welfare Canada, Supply andServices Canada, Cat No. En 37-95/1990-1E.

Caughley, G. 1977. Analysis of vertebrate populations.NY: Wiley.

Dunn, B.P., Black, 1.1., and Maccubbin, A 1987. 32P-post­labeling analysis of aromatic DNA adducts in fish frompolluted areas. Cancer Res. 47:6543-6548.

Durham, R.W., and Oliver, B.G. 1983. History of LakeOntario contamination from the Niagara river by sedi­ment radio-dating and chlorinated hydrocarbon analysis.J. Great Lakes Res. 9:160-168.

Geraci, J.R., Palmer, N.C., and St. Aubin, D.J. 1987.Tumors in cetaceans : analysis and new findings. Can. J.Fish. Aquat. Sci. 44: 1289-1300.

Girard, c., Lagace, A, Higgins, R., and Beland, P. 1991.Adenocarcinoma of the salivary gland in a beluga whale(Delphinapterus leucas). J. Vet. Diagn. Investig. 3:264­265.

Head, K.W. 1990. Tumors of the alimentary tract. InTumors in domestic animals, 3rd ed, ed. J.E. Moulton,pp. 347-435. Berkeley: U. California Press.

Kleinenberg, S.E., Yablokov, AV., Belkovich, B.M., andTarasevich, M.N. 1964. Beluga (Delphinapterus leucas): Investigation of the species. Akad Nauk SSSR,Moscow, Transl. by Israel Program for Scient. Transl.,Jerusalem 1969.

Koeman, J.H., Peeters, W.H.M., Koudstaal-Hoi, C.H.M.,Tjioe, P.S., and DeGoeij, J.J.M. 1973. Mercury-sele­nium correlations in marine mammals. Nature 245:385­386.

Kurelec, B., Garg, A, Krca, S., Chaco, M., and Gupta, C.1989. Natural environment surpasses polluted environ­ment in inducing DNA damage in fish. Carcinogenesis10:1337-1339.

Kuroki, H., Bergman, A., Norstrom, R., Langelier, K.,Beland, P., Haraguchi, K., and Masuda, Y. 1991. PCBmethyl sulphones in polar bear and whales. Dioxin '91Conference, Chapel Hill, NC, Sept. 1991.

Martel, L.M., Gagnon, J., Masse, R., Leclerc, A., andTremblay, L. 1986. Polycyclic aromatic hydrocarbons insediments from the Saguenay fjord, Canada. Bull. Envi­ron. Contam. Toxicol. 37:133-140.

St. Lawrence Beluga Whales 775

Martineau, D., Lagace, A., Masse, R., Morin, M., andBeland, P. 1985. Transitional cell carcinoma of the uri­nary bladder in a beluga whale (Delphinapterus leucas).Can. Vet. J. 26:297-302.

___, Lagace, A., Beland, P., and Desjardins, C. 1986.Rupture of a dissecting aneurysm of the pulmonarytrunk in a beluga whale (Delphinapterus leucas). J.Wildl. Dis. 22:289-294.

___, Beland, P., Desjardins, C., and Lagace, A. 1987.Levels of organochlorine chemicals in tissues of belugawhales (Delphinapterus leucas) from the St. LawrenceEstuary, Quebec, Canada. Arch. Environ. Contam. Toxi­col. 16:137-147.

___, Lagace, A., Beland, P., Higgins, R., Armstrong,D., and Shugart, L.R 1988. Pathology of stranded bel­uga whales (Delphinapterus leucas) from the St.Lawrence estuary, Quebec, Canada. J. Compo Pathol.98:287-311.

Masse, R., Martineau, D., Tremblay, L., and Beland, P.1986. Concentrations and chromato-graphic profile ofDDT metabolites and polychlorobiphenyl (PCB)residues in stranded beluga whales (Delphinapterus leu­cas) from the St. Lawrence Estuary, Canada. Archiv.Environ. Contam. Toxicol. 15:567-579.

Michaud, R 1993. Distribution estivale du beluga du Saint­Laurent; synthese de 1986 a 1992. Rapp. tech. can. sci.halieut. aquat. No 1906.

Muir, D.C.G., Ford, c.A., Stewart, R.E.A., Smith, T.G.,Addison, R.F., Zinck, M.E., and Beland, P. 1990.Organochlorine contaminants in belugas, Delphi­napterus leucas, from Canadian waters. Can. Bull. Fish.Aquat. Sci. 224:165-190.

Norstrom, R., and Simon, M. 1990. Levels and possiblesources of polychlorinated dibenzo-p-dioxins (PCDDs)and polychlorinated dibenzofurans (PCDFs) in belugawhale tissues collected from the St. Lawrence in 1987and 1988. Can. Wildl. Serv., Wildl. Toxicol. Branch,Rept. CRD-90-9.

___, Schweinsberg, R.E., and Collins, B.T. 1986.Heavy metals and essential elements in livers of thepolar bear (Ursus maritimus) in the Canadian Arctic.Sci. Total Environ. 48:195-212.

___, Simon, M., Muir, D.C.G. 1990. Polychlorinateddibenzo-p-dioxins and dibenzofurans in marine mam­mals in the Canadian North. Environ. Pollut. 66:1-19.

___, Muir, D.C.G., Ford, c.A., Simon, M., Macdon­ald, C.R., and Beland, P. 1992. Indications of P-450mono-oxygenase activities in beluga (Delphinapterusleucas) and narwhal (Monodon monoceros) from pat­terns of PCB, PCDD and PCDF accumulation. MarineEnviron. Res. 34:267-272.

Ono, M., Kannan, N., Wakimoto, T., and Tatsukawa, R1987. Dibenzofurans a greater pollutant than dioxins ?Mar. Pollut. Bull. 18:640-643.

Pelletier, E., Beland, P., and Blouin, N. 1990. Developpe­ment d'une methode d'evaluation de l'impact des HAP

sur les organismes aquatiques. Rept. INESL, Environ­ment Canada, Montreal, Contr # KA313-9-3949.

Picard-Berube, M., and Cossa, D. 1983. Teneurs en benzo3,4, pyrene chez Mytilus edulis de l'estuaire et du Golfedu Saint-Laurent. Mar. Environ. Res. 10:63-71.

Randerath, K., Reddy, M.V., and Disher, RM. 1986. Age­and tissue-related DNA modifications in untreated rats:detection by 32P-postlabeling assay and possible signifi­cance for spontaneous tumor induction and ageing. Car­cinogenesis 7:1615-1617.

Ray, S., Dunn, B.P., Payne, J.F., Fancey, L., Helbig, R.,and Beland, P. 1991. Aromatic DNA-carcinogen adductsin beluga whales (Delphinapterus leucas) from theCanadian arctic and the Gulf of St. Lawrence. Mar. Poll.Bull. 22:392-396.

Reeves, RR., and Mitchell, E. 1984. Catch history and ini­tial population of white whales (Delphinapterus leucas)in the river and gulf of St. Lawrence, eastern Canada.Naturaliste-Can. (Rev. tcol. Syst.) 11 1:63-121.

Reijnders, P.J.H. 1986. Reproductive failure in commonseals feeding on fish from polluted coastal waters.Nature 324:456-457.

Sergeant, D.E. 1973. Biology of white whales (Delphi­napterus leucas) in western Hudson Bay. J. Fish. Res.Board Can. 30:1065-1090.

___. 1986. Present status of white whales in the St.Lawrence estuary. Naturaliste-Can. (Rev. tcol. Syst.)113:61-81.

Shugart, L.R, Martineau, D., and Beland, P. 1990. Detec­tion and quantitation ofbenzo-(a)pyrene adducts in brainand liver tissues of beluga whales (Delphinap-terus leu­cas) from the St. Lawrence and Mackenzie estuaries. InFor the future of the beluga, ed. J. Prescott and M.Gauquelin, pp. 219-223. Proc. IntI. Forum, Tadoussac1988, Dniversite du Quebec Press, Sillery.

Steuer, K.L. 1989. A comparative institutional survey offactors influencing mortality in cetaceans in U.S. zoosand aquaria. Rept, Center for Coastal Studies, 59 Com­mercial Street, Provincetown, Mass, 02657, 56 p.

Varanasi, D., Reichert, W.L., and Stein, J.E. 1989. 32p_postlabeling analysis of DNA adducts in liver of wildEnglish sole (Parophrys vetulus) and winter flounder(Pseudopleuronectes americanus). Cancer Res. 49:1171-1177.

Wagemann, R, Snow, N.B., Lutz, A., and Scott, D.P. 1983.Heavy metals in tissues and organs of the narwhal (Mon­odon monoceros). Can. J. Fish. Aquat. Sci. 40 (Suppl2):206-216.

___, Stewart, R.E.A., Beland, P., and Desjardins, C.1990. Heavy metals and selenium in tissues of belugawhales, Delphinapterus leucas, from the Canadian Arc­tic and the St. Lawrence estuary. Can. Bull. Fish. Aquat.Sci. 224:191-206.

Submitted: 9 November 1991Accepted: 5 October 1993