accumulation and lactational transfer of pcbs and pesticides in harbor seals (phoca vitulina) from...

The Science of the Total Environment 319(2004) 137–146

0048-9697/04/$ - see front matter� 2003 Elsevier B.V. All rights reserved.doi:10.1016/S0048-9697(03)00449-2

Accumulation and lactational transfer of PCBs and pesticides inharbor seals(Phoca vitulina) from Svalbard, Norway

Hans Wolkers*, Christian Lydersen, Kit M. Kovacs

Norwegian Polar Institute, N-9296 Tromso, Norway

Received 16 January 2003; accepted 11 July 2003

Abstract

The harbor seal population on Svalbard, the northernmost breeding site for this species, appears to have a truncatedage distribution with older animals being largely absent. PCBs and pesticides were measured in harbor seal males,females, milk and pups from Svalbard to explore whether contaminant exposure or accumulation is a possible causeof premature death for these animals. The levels and patterns of these contaminants were assessed. In addition,transfer of these compounds from females to their pups during lactation was assessed. Both PCB and pesticide levelswere low compared to more southern harbor seal populations. Animals from Svalbard contained 5–10 times lowercontaminant levels, compared to seals from the Norwegian mainland, and 30 times lower concentrations than thoseof harbor seals from the Gulf of St. Lawrence in eastern Canada. Ringed seals from Svalbard have contaminant levelsthat are comparable to the harbor seals, probably because the diet, as well as the metabolic capacity, of the twospecies is similar at this location. The findings of this study indicate that the early mortality observed for harbor sealson Svalbard, is not likely to be due to contaminant exposure. Female harbor seals transfer a modified contaminantmixture to their pups compared to that found within their own tissues; compounds with higher logK , such as someow

penta-chlorinated PCBs, were selectively transferred into milk. As a result, the contaminant pattern between malesand females differed, with penta-chlorinated PCBs more abundant in males than in females. In addition, pups receivea relatively high amount of the less lipophylic compounds and a low amount of the more lipophylic compounds. Thesimilar contaminant pattern in milk and pups suggested that they are probably unable to metabolize contaminants andconsequently, accumulate all ingested chemicals.� 2003 Elsevier B.V. All rights reserved.

Keywords: Harbor seal; Contaminants; PCB; Toxaphenes; Lactation transfer; Svalbard

1. Introduction

Harbor seals(Phoca vitulina) are one of themost widespread seal species in the northern hem-isphere. They have a coastal distribution ranging

*Corresponding author. Tel.:q47-77750521; fax:q47-77750501.

E-mail address: [email protected](H. Wolkers).

from temperate to Arctic regions on the east andwest coasts of North America, the KamchatkaPeninsula, as well as in Western Europe. At Sval-bard, Norway, this species reaches its most north-erly distribution with a population of more than600 animals(Prestrud and Gjertz, 1990). Svalbardharbor seals feed on a wide variety of fish species,but Atlantic cod(Gadus morhua) and polar cod

138 H. Wolkers et al. / The Science of the Total Environment 319 (2004) 137–146

(Boreogadus saida) are the most important preys(Andersen, 2001). Recent tracking data haveshown that adult animals are relatively stationaryand that their seasonal migration patterns are lim-ited to areas within the Svalbard Archipelago(Gjertz et al., 2001). Pupping in Svalbard harborseals occurs in the second half of June(Gjertz andBørset, 1992), and nursing lasts for approximately24 days. Sexual maturity is reached at an age of3–5 years for females and 4–6 years for males(Lydersen and Kovacs, 2001). However, in theSvalbard population older animals seem to bemissing. Out of a sample of 367 animals, forwhich age has been estimated, only three individ-uals were older than 15 years(oldest female 22years; oldest male 17 years) (Lydersen andKovacs, 2001).

As relatively long-lived predators in the arcticecosystem, harbor seals are potentially vulnerableto exposure to contaminants. Contaminant expo-sure is associated with disturbances of many phys-iological processes in the body. In Europe, interestin the contamination of harbor seals was sparkedin the late 1980s when these animals suffered amass mortality event, that was eventually attributedto a viral infection (for review: see Heide-Jørgensen et al., 1992). Studies under controlledconditions were carried out during the mid-1990sto assess the effects of contaminant exposure onthese animals(Ross et al., 1994). These studies,in addition to literature published earlier, showedthat contaminant exposure resulted in disruptionof reproduction-related processes(Reijnders,1986), immune competence(Ross et al., 1994)and vitamin A metabolism(Brouwer et al., 1989).

There is reason to believe that nursing pups mayface particularly high risks from contaminant expo-sure. Lactation in phocid seals is associated withhigh rates of mobilization of lipids to synthesizemilk (Lydersen and Kovacs, 1999). The lipid-richmilk and associated lipophylic contaminants arepassed on to nursing pups(Addison and Brodie,1987; Wolkers et al., 2002). Recent studies haveshown that seal milk contains substantially morecontaminants than a ‘normal’ seal diet of fish andcrustaceans(Wolkers et al., 2000, 2002). In fact,seal pups feed one trophic level higher than theirmothers and are concomitantly exposed to relative-

ly high contaminant levels. Additionally, the timeframe in which the contaminants are transferredfrom mother to pup is during a critical phase whenthe pups are developing their neural, endocrineand immune systems. As a result of transfer ofcontaminants through lactation, reproducingfemales show a marked reduction of their tissuecontaminant concentrations relative to adult males.Since contaminant transfer through milk has beenshown to be selective to some degree(Addisonand Brodie, 1987; Pomeroy et al., 1996; Wolkerset al., 2002), it might also be expected that thecontaminant patterns in adult males and adultfemales might differ.

The purpose of the present study was to assessthe contaminant levels and patterns in adult harborseals, and to study the transfer of the contaminantsto pups from their mothers during the lactationperiod. In addition, selectivity of contaminanttransfer from females to their milk, as well as thepups’ abilities to metabolize contaminants wereassessed.

2. Methods

2.1. Sampling

Six male harbor seals(aged 4–7 years old) aswell as 4 females(aged 10–12 years old) andtheir pups (12.5–23 kg) were live captured atPrins Karls Forland(788209N, 118309E), on thewest coast of Spitsbergen, Svalbard, Norway. Theseals were captured using nets set around haul-outsites. Adult animals were weighed to the nearestkg and pups were weighed to the nearest 0.5 kg.Seals that were not pups of the year were druggedwith Zoletil (0.5–1.0 mgykg body mass). Anincisor tooth was extracted from these animals forage determination, and a complete blubber corewas sampled dorsally at approximately 60% of thebody length from all animals including pups. Thesamples were wrapped individually in aluminumfoil and frozen until analyses. Ten milliliter ofmilk was collected from the adult females, 10 minafter an intra-muscular injection of 10 IU ofoxytocin. All sampling and animal handling pro-cedures were conducted according to Norwegian

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Animal Care Guidelines, and under permits fromthe Governor of Svalbard.

2.2. Chemical analyses

The accredited laboratories of the NorwegianInstitute for Air Research in Tromsø, Norway(according to EN 45001) carried out PCB andpesticide analyses as described previously(Kallen-born et al., 1994; Oehme et al., 1995). Themethods were validated by applying a level ofquantification of ten times signalynoise, based onblanks, while the level of detection was calculatedas three times signalynoise. As internal standards,

C-labelled PCB 118 was used for tri- to penta-13

chlorinated PCBs and all pesticides, C-labelled13

PCB 141 for all hexa-chlorinated PCBs and C-13

labelled PCB 178 for all hepta-chlorinated PCBs.Approximately 0.5 g of blubber was homoge-

nized in a tenfold amount of sodium sulfate. Thehomogenate was used for analyses and C-13

labelled PCBs were added as internal standards.Cyclohexaneyacetone(3:1, vyv) extraction of thehomogenate was performed and clean up wascarried out by gel permeation chromatography,using a two-column system filled with Bio BeadsSX-3 (Bio-Rad, Hercules, CA) and cyclohexaneyethylacetate(1y1, vyv) as mobile phase. PCBs(congener numbers 18, 26, 28, 44, 52, 74y76, 99,101, 105, 110, 114, 118, 126, 128, 138, 141, 146,153, 157, 167, 169, 170, 174, 180, 183, 187),toxaphenes(Parlar 26, 40, 44, 50, 51, 58, 69),DDTs, hexachlorobenzene and hexachlorocycloh-exanes were analyzed by gas chromatograph-massspectrometer using a CE Instruments 8560 MegaHigh-Resolution Gas Chromatograph(Milan, Ita-ly) and a J&W DB5-MS(Milan, Italy) fused silicacolumn (30 m=0.25 mm internal diameter, 0.25-mm film thickness), linked to a Finnigen MD 800quadrupole mass spectrometer(Manchester, UK)in selective ion mode. Electron impact was usedas the ionization method for the determination ofPCBs and DDTs. Negative ionization mode wasused to determine the other chlorinated pesticides.Extractable organic matter was determined gravi-metrically using cyclohexaneyacetone(3:1, vyv)extraction. Extractable organic matter values wereconsidered to be representative of the lipid fraction.

2.3. Data management

Geometric means and 95% confidence intervalswere calculated for concentrations of individualcontaminants. For all samples, individual contam-inants as well as main contaminant groups, i.e.PCBs of different chlorination, DDTs, toxaphenes,HCB and HCHs were expressed as the percent oftotal contaminants measured in order to comparethe pattern in males and females, as well as aselective transfer from females to milk. Differenceswere tested using at-test after logarithmic trans-formation of the individual data. Significance wasset atP-0.05.

The relative contribution of each compound,expressed as the ratio contaminantyPCB 153, wascalculated in pups and milk. Differences in thisratio between pups and their food(the milk)indicate if a compound accumulates more(ratiosignificantly higher in pups than milk) or less(ratio significantly lower in pups than milk) thanPCB 153(Bruhn et al., 1995).

3. Results

3.1. Contaminant concentrations in males, females,milk and pups

PCBs congeners 18, 26, 44, 74y76, 126, 169were below detection. Likewise toxaphene Parlar51, 58, 69 and the DDTs, except forp,p-DDE, andb- andg-HCH were also below detection.8PCBaveraged 2.2, 0.5, 0.3 and 0.5 ppm in males,females, milk and pups, respectively(Table 1).The hexa-chlorinated PCBs were the most abun-dant PCBs in all samples(Table 2).

Similar to PCBs, most pesticides were alsohighest in males. Toxaphenes were approximately0.2 ppm in males. They were 5–10 times lower infemales and pups, while the toxaphenes in milkwere approximately 20% lower than in females(Table 2). DDE was the most prevalent of allpesticides and reached over 1 ppm in males, whilefemales and pups had approximately 15% of thoselevels. Milk contained the lowest DDE concentra-tion; approximately 8% of the amount in males(Table 2). HCB and a-HCH were low in all

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Table 1Geometric mean PCB concentrations(ngyg lipid) and 95% confidence limits in blubber and milk of harbor seals

PCB 28 52 99 101 105 110 114 118 128 138 141 146 153 157 167 170 174 180 183 187 8PCB

Males Mean 2.5 23.1 205.7 92.3 3.1 22.9 2.6 70.1 28.9 395.5 29.1 260.7 610.2 6.9 2.8 64.0 6.6 180.7 26.8 71.3 2201.1(ns6) 95% low 1.3 14.4 164.4 73.2 0.8 6.5 0.8 53.9 21.3 294.2 24.6 189.3 443.1 2.0 0.7 48.0 2.0 131.2 20.9 57.0 1730.5

95% high 5.0 37.1 257.4 116.4 12.9 80.4 8.7 91.3 39.2 531.8 34.5 359.0 840.4 23.7 11.7 85.4 21.8 248.9 34.3 89.2 2799.6

Females Mean 1.9 3.2 14.0 8.5 4.1 3.7 1.3 16.8 6.2 79.4 3.7 48.2 116.0 2.5 6.6 27.9 1.8 57.5 10.0 22.8 458.8(ns4) 95% low 0.9 0.9 2.3 1.9 1.3 0.8 0.7 7.9 2.9 40.4 0.8 26.5 62.0 0.9 0.8 10.3 0.6 27.6 5.2 11.1 213.4

95% high 4.0 11.6 85.0 37.5 12.3 16.2 2.4 35.7 13.4 156.2 16.2 87.6 217.2 7.5 56.9 75.9 5.3 119.8 19.5 46.6 986.4

Milk Mean 1.9 3.8 34.4 15.7 -1 2.4 1.7 16.1 -1 47.8 2.4 8.4 89.7 1.2 1.3 4.4-1 18.9 3.9 8.2 271.6(ns4) 95% low 0.9 0.8 21.3 7.6 0.8 0.9 8.8 25.8 0.9 2.0 53.9 0.8 0.8 1.6 14.9 2.7 4.8 160.1

95% high 4.1 17.5 55.7 32.8 7.2 3.1 29.5 88.6 6.8 36.2 149.3 1.9 2.1 11.8 23.9 5.5 14.1 460.7

Pups Mean 4.0 7.6 37.0 20.3 3.2 4.8-5 22.6 4.2 63.5 3.1 34.3 96.5 3.1 2.5 7.7-1 22.9 4.1 6.5 540.9(ns4) 95% low 3.1 5.7 22.9 13.6 0.9 0.8 13.8 1.6 33.3 0.8 17.4 51.6 0.9 0.4 4.2 14.3 2.7 1.8 297.2

95% high 5.2 10.1 59.9 30.4 12.3 28.9 36.9 11.2 121.3 11.7 67.5 180.8 11.5 15.4 14.0 36.6 6.3 22.6 984.3

-: value below limit of detection.


Table 2Geometric mean concentrations(ngyg lipid) and 95% confidence limits of pesticides in harbor seals

Compound 5-PCB 6-PCB 7-PCB Tox Tox Tox Tox 8Tox p,p-DDE HCB a-HCH26 40 44 50

Males Mean 422.2 1381.5 354.1 59.7 22.0-4 88.5 170.7 1318.1 6.4 16.5(ns6) 95% low 359.8 1044.1 263.3 43.4 14.7 62.7 121.9 1070.5 3.3 5.4

95% high 495.5 1828.0 476.0 82.2 32.8 124.8 238.8 1622.9 12.5 50.2

Females Mean 56.8 273.3 121.8 10.2 5.6-4 7.6 21.2 188.3 2.1 5.9(ns4) 95% low 22.2 133.6 55.1 1.9 1.5 0.8 2.4 86.8 1.2 1.7

95% high 145.5 558.9 269.5 54.7 21.3 74.9 188.1 408.3 3.9 20.0

Milk Mean 69.2 161.8 36.2 8.0 5.3 -4 4.9 16.3 103.1 2.5 8.5(ns4) 95% low 38.4 96.2 25.5 2.0 1.5 0.7 2.5 48.0 2.0 6.6

95% high 124.6 272 51.6 33.0 18.2 32.7 108.0 221.4 3.1 10.8

Pups Mean 94.2 215.8 41.8 4.7 20.2-4 5.7 44.5 221.2 4.7 33.9(ns4) 95% low 53.9 107.6 22.8 1.0 12.3 0.8 23.3 101.0 1.0 16.4

95% high 164.6 432.8 76.7 21.5 32.9 42.2 84.9 484.5 21.5 70.0

-: value below limit of detection. 5-, 6-, 7-PCBspenta-, hexa- and hepta-chloro PCBs; Tox, toxaphene congener(Parlar 26, 40,44, 50); 8Tox, total toxaphene levels; DDE, dichlorodiphenyldichloro-ethylene; HCB, hexachlorobenzene; HCH,hexachlorocyclohexane.

animals, but the latter compound was higher inpups than in females or males(Table 2).

3.2. Contaminant patterns in males, females, milkand pups

PCB 99, 138, 146, 153 and 180 dominated inmales, making up approximately 75% of totalPCBs (Table 1). In females, concentrations ofthese compounds were substantially lower, and themost dominant PCB congeners(118, 138, 170,180 and 187) differed somewhat from males(Table 1). Pups and milk contained relatively highconcentrations of PCB 99 and 118, but also sub-stantial quantities of PCB 138, 146, 153 and 180(Table 1).

The relative presence of contaminants or con-taminant groups, expressed as percent of totalcontaminants measured, showed substantial differ-ences between males and females(Fig. 1a and b).A significantly higher relative presence of PCB99, p,p-DDE and total pesticides was found inmale compared to female seals while total hepta-chlorinated PCBs and individual congeners 170,180, 183 and 187 were less prevalent in males(Fig. 1a and b).

A significantly higher relative presence in milkcompared to that in the blubber of females was

found for the sum of the penta-chlorinated PCBsas well as individual congeners 99, 101 and 118(Fig. 1a and b). In contrast, the hepta-chlorinatedPCBs 170, 183 and 187 as well as the sum ofhepta-chlorinated PCBs measured were less prev-alent in the milk as compared to the females(Fig.1a and b). No such differences were found for anyof the pesticides.

3.3. Percentage of PCB 153 in milk and pups

The contaminant pattern, expressed as percentof PCB 153 showed no differences in PCB patternbetween pups and milk(Fig. 2). However, therelative presence of pesticidesp,p-DDE and a-HCH was significantly higher in pups comparedto milk (Ps0.01 andPs0.028, respectively) (Fig.2).

4. Discussion

Although harbor seals have been the subject ofa large number of toxicological studies, the currentstudy is, to our knowledge, the first to addresscontaminant transfer through lactation from moth-ers to pups as well as contaminant accumulationand metabolism in pups of this species. In addition,this is the first report of contaminant accumulationin the harbor seal population from Svalbard.


Fig. 1. (a) Relative contribution(%) of poly-chlorinated biphenyls(PCBs), p,p-DDE, a-HCH, hexachlorobenzene(HCB) andtoxaphenes(Tox) to total contaminants measured in male and female harbor seals and their milk. *Difference between male andfemale seals or females and their milk significant atP-0.05; **Difference between male and female seals or females and theirmilk significant atP-0.001.(b) Relative contribution(%) of tri-chloro, tetra-chloro, penta-chloro, hexa-chloro and hepta-chloroPCBs, total PCBs, DDTs, hexachlorocyclohexane(HCHs), toxaphenes(Toxs) and pesticides(Pests) to total contaminants measuredin male and female harbor seals and their milk. *Difference between male and female seals or females and their milk significant atP-0.05; **Difference between male and female seals or females and their milk significant atP-0.001.


Fig. 2. Contaminant congener pattern relative to PCB 153(compound XyPCB 153) in harbor seal pups and their food(milk).

In general, comparison of contaminant levelsbetween marine mammals from different studiesand geographic locations can be somewhat prob-lematic due to a lack of standardized samplingmethods. Additionally, variation in contaminantlevels can be due to age, sex and body condition,so these factors must also be accounted for inorder to make sensible comparisons. Finally, con-taminant exposure can change relatively rapidlyover time via changes in exposure due to restric-tions in production and use, or changes in theenvironment that alter delivery rates to specificsites, e.g. shifts in ocean currents. Therefore, geo-graphical differences in contaminant exposure inthese animals can only be assessed between sam-ples taken in similar time frames.

The harbor seals in this study occur at thenorthern edge of the species’ distribution and arelikely more sensitive to environmental disturbancesthan populations further south. The absence ofolder individuals may indicate that some unknownfactor(s) negatively impact longevity; exposure to

pollution could be such a factor. However, inaccordance with other seal species from Svalbard(Wolkers et al., 1998), overall levels of PCBs andpesticides measured in this study were relativelylow. Animals from the Norwegian coast showedPCB and DDT levels approximately 17 and 2–3ppm, respectively, i.e. approximately eight and twotimes higher, respectively, than in the Svalbardharbor seals. HCHs and HCB were approximatelytwo times higher in the southern harbor seals ascompared to the Svalbard animals(Ruus et al.,2002). In the Gulf of St. Lawrence harbor sealssuffer an even greater contaminant exposure(Berntet al., 1999). In male harbor seals from the GulfPCB and DDT levels were approximately 50 and8 ppm, respectively, that is approximately 25 and6 times higher, respectively, compared to malesfrom Svalbard. In females this difference was evenlarger; Gulf females had approximately 30 timesmore PCB and 15 times higher DDT levels, ascompared to Svalbard females. The fact that theGulf population of harbor seals appears to be in


good overall health, with normal pup production,in spite of the high contaminant exposure, makescontaminant exposure an unlikely factor in reduc-ing longevity of this species at Svalbard.

Except for a higher fraction of Atlantic cod inthe harbor seal diet, ringed and harbor seals fromthe Svalbard area have relatively similar diets(Gjertz and Lydersen, 1986; Weslawski et al.,1994; Andersen, 2001) and the PCB pattern sug-gests that contaminant metabolism is similar aswell (Wolkers et al., 1998). Overall, contaminantlevels found in the harbor seals were quite similarto those in ringed seals. This is an additionalindication that contaminant exposure is probablynot responsible for reducing longevity in harborseals, since the ringed seals in this area oftenexceed 30 years of age, with a record longevity of45 years for the species being documented fromSvalbard(Lydersen and Gjertz, 1987).

Although there might be some in utero transferof contaminants from mother to pup, the transferthrough lactation is considered as quantitativelyfar more important in mammals(Nakashima et al.,1997). Therefore, it is plausible that the differencein tissue contaminant concentrations foundbetween male and female harbor seals can beattributed to contaminant excretion through milkin females. When blubber lipids are mobilized formilk production, contaminants are co-transportedwith the lipids to blood and milk. However, dueto differences in affinity of individual contaminantsfor the relatively non-polar lipids in blubber andthe more polar lipids in blood and milk, a selectivetransfer occurs, regulated by the degree of thecontaminant’s lipophylicity and its molecularweight (You et al., 1999).

The relative presence of individual compoundsor compound-groups in females and their milkgives a direct assessment of selective female–milktransfer. The differences in contaminant patternsfound between males, females and milk can, atleast partly, be attributed to selective transfer fromfemales to their milk. Selective retention of com-pounds within females results in an over-represen-tation of that particular compound relative tomales, while a favorable transfer into the milkwould result in an under-representation. Penta-chlorinated PCBs(particularly congeners 99, 101

and 118) exhibit a clear selective transfer frommothers to their milk. This was reflected in maleshaving higher fractions of PCB 99 compared tofemales. A selective retention in females was foundfor the hepta-chlorinated PCBs(PCB 170, 180,183 and 187) and this was reflected in a higherrelative presence in females compared to males.Surprisingly, no selective transfer of the relativelypolar HCHs was detected, but since levels of thesecompounds were very low(close to detection),sampling error might have been relatively large.The higher fraction ofp,p-DDE in males comparedto females is possibly the result of a higherconversion of DDT to DDE in males.

The overall picture of selective transfer fromfemales to milk confirms previous findings in greyseals(Addison and Brodie, 1987; Pomeroy et al.,1996) and harp seals(Wolkers et al., 2002).Selective excretion in milk can most likely beattributed to the lipophylic nature(expressed aslog K ) of some contaminants. Higher-chlorinatedow

PCBs (log K f7) are selectively retained andow

the lower-chlorinated PCBs(log K f6) areow

selectively transferred into milk.The relative persistence of a particular contam-

inant in an animal can be assessed by comparingits relative presence, i.e. the percent of the recal-citrant PCB congener 153, in the animal relativeto its food (Bruhn et al., 1995). A similar orhigher fraction in the animal compared to the foodindicates a higher accumulation than PCB 153,while a lower fraction indicates a lower accumu-lation than PCB 153 and may indicate that thecompound is subject to metabolism by the animal.The results show that none of the contaminantsmeasured showed a reduced relative presence inpups compared to their food; i.e. the milk. A-HCHandp,p-DDE had a higher relative presence in pupthan in milk, suggesting a higher accumulationthan PCB 153, although metabolic conversion ofDDT to DDE might overestimatep,p-DDE accu-mulation. These results indicate that the contami-nants measured are all accumulating to the sameor a larger degree than PCB 153. The capacity ofharbor seal pups to metabolize contaminantsappears to be very low, as has been previouslyshown in harp seal pups(Wolkers et al., 2002).


5. Conclusion

This study has shown that the levels of contam-inants in the world’s most northerly-distributedharbor seal population are unlikely to have anynegative impacts on their longevity. PCB andpesticide levels were low compared to more south-erly populations and similar to levels found in thehealthy ringed seal population occupying the samearea. Female harbor seals transferred a modifiedcontaminant mixture to their pups compared tothat found in their own blubber, with a relativelylarge contribution of compounds with a lowlog K , such as the lower-chlorinated PCBs, andow

a relatively small contribution of compounds witha higher logK , such as the higher-chlorinatedow

PCBs. The contaminant pattern in milk and pupsrevealed that pups are probably unable to metab-olize ingested contaminants and consequently,accumulate all of the contaminants ingested in themilk.

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