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Organochlorine contaminants in northeast Atlantic minke whales (Balaenoptera acutorostrata)
ENVIRONMENTAL POLLUTION
Environmental Pollution 101 (1998) 231-239
Organochlorine
contaminants in northeast Atlantic minke whales (Balaenoptera acutorostrata) L. Kleivane a, J.U. Skaare a$bt*
aNational Veterinary Institute, PO Box 8156 Dep., N-0033 Oslo 1, Norway bNorwegian College of Veterinary Medicine, Department of Pharmacology, Microbiology and Food Hygiene, Division of Pharmacology and Toxicology, PO Box 8146 Dep., N-0033 Oslo 1. Norway
Received 7 July 1997; accepted 19 February 1998
Abstract Blubber samples of 72 minke whales (Buluenopferu acutorostrutu) were obtained from the northeast Atlantic in July and August 1992, and evaluated for organochlorine contamination. The following organochlorines were determined: the industrial chemicals PCBs (polychlorinated biphenyls), and the organochlorine pesticides DDTs (dichlorodiphenyltrichloroethanes), HCHs (hexachlorocyclohexaneb), HCB (hexachlorobenzene) and CHLs (chlordanes). The concentrations of IZPCB (sum of concentrations of 18 PCB congeners) and XDDT (sum of concentrations of p,P’-DDT, p,p’-DDE, p,p’-DDD, o,p’-DDT and o,p’-DDD) ranged from 0.6-20.8 and 0.5-14.8 pgg-’ lipid weight, with mean concentrations at 3.8 and 2.5 pgg-’ lipid weight, respectively. The mean concentrations of HCB, the chlordane metabolites oxychlordane, cis-chlordane and truns-nonachlor, and the HCH isomers (a-, f& and y-HCH) were all < 1 hgg-’ lipid weight. Significantly higher concentrations of the three major pollutants (XPCB, XDDT and XCHL) were found in mature males as compared to mature females and juveniles of both sexes. No such relationship was found for XHCH and HCB. Stomach contents of northeast Atlantic minke whales indicate considerable heterogeneity in the diet when comparing different years, seasons and geographical areas. However, without knowing more about the minke whale migration pattern, or possible geographical segregation with age and sex, the interchemical variation of organochlorines between sampling areas may not reflect true geographical differences. 0 1998 Elsevier Science Ltd. All rights reserved. Keywords: Marine mammals; Minke whale; Pollution; Organochlorines;
1. Introdllction The presence of persistent organochlorines (OCs) in biota from ‘pristine’ areas like the Arctic and the Antarctic, are primarily ascribed to long-range transport. An essential part of this transport is thought to be of aerial origin, but transport by ocean currents and biological transport are also likely to occur (Barrie et al., 1992; Wania and Mackay, 1993). Surprisingly high OC levels, especially polychlorinated biphenyls (PCBs) and certain chlordane (CHL) metabolites, are found in Arctic and sub-Arctic species (Norstrom et al., 1988; Norheim et al., 1992; Wang-Andersen et al., 1993; Kleivane et al., 1995; Bernhoft et al., 1997. In terms of population sizes and feeding habits, the minke whale (Buluenopteru ucutorostratu) is an important species in
* Corresponding author. Tel.: + 47-22-59-7444; fax: + 47-22-597459; e-mail: [email protected] 0269-7491/98/%19.00 0 1998 Elsevier Science Ltd. All rights reserved. PII: SO269-7491(98)00043-8
PCB; DDT
the highly productive waters of higher latitudes both at
the northern and southern hemisphere. Minke whales from both hemispheres are thought to have opposite summer to winter migration patterns, undertaking seasonal migration between breeding and feeding areas at lower and higher latitudes, respectively. There is no evidence of exchange of genetic material between northern and southern minke whales (Kasamatsu et al., 1995). An intraspecies comparison of pollutant loads in specimens collected from Arctic and Antarctic waters may elucidate differences and similarities of levels and patterns of OC pollutants present at higher latitudes. The aims of this study was to investigate and characterize the OC pattern and levels in the northeast Atlantic minke whale stock, and to compare it with similar data previously reported by Tanabe et al. (1995) in southern hemisphere minke whales. This investigation also attempts to understand biological-related explanations of observed patterns of organochlorine concentrations based on age, sex and blubber characteristics.
L. Kleivane. J.U. SkaarelEnvironmental Pollution 101 (1998) 231-239
232
2. Materials and methods
investigations: West of Spitsbergen, Bear Island, coast of Kola, coast of Finnmark and Lofoten/VesterHlen (Fig. 1).
The animals were captured during July and August 1992 at the coasts of Nordland and Finnmark in northern Norway, in the Russian sector along the Kola Peninsula, and Arctic areas around Bear Island and Spitsbergen. Subcutaneous samples of 72 minke whales were obtained. Whales were classified according to sex and age as: adult males (AdM), juvenile males (JuM), adult females (AdF) and juvenile females (JuF; Table 1). Male sexual maturity was determined by paired testis weight of more than 500 grams (JonsgHrd, 1951; Christensen, 1981), whereas female sexual maturity was determined by presence of a foetus or corpora albicantia. Five separate sampling areas were defined during these
2.1, Analytical procedures
Weighed blubber samples were homogenized using an Ika Ultra Turrax, and PCB no. 112 was added as an internal standard. The sample was extracted twice with cyclohexane and acetone using an ultrasonic homogenizer (4710 series, Cole-Parmer), followed by clean-up with sulfuric acid (Brevik, 1978; Bernhoft and Skaare, 1994), and automatically injected in the split-mode (1 ul, 1:30; Fisons autosampler AS 550) on a Carlo Erba, HRGC 5300 Mega Series gas chromatograph and an electron capture detector (ECD-63Ni). The carrier gas
Table 1 Biological data (sex, age-groups, body length, blubber thickness, lipid content in blubber, area and time of catch) of minke whales (Balaenoptera acutorostrata) from northeast Atlantic waters
Juveniles Males (JuM) Females (JuF) Adults Males (AdM) Females (AdF)
Month
Number (n)
July/August July/August
15 13
July/August July/August
22 22
Area distribution Il/2/3/4/5~* (n)
Length mean (range cm)
Blubber thicknessa blow hole; mean (range mm)
Blubber thickness” flipper; mean (range mm)
Percentage lipid in blubber
{O/4/5/4/2} {5/l/l/2/4}
634 (500-712) 625 (485-742)
35 (1649) 33 (2541)
31 (24-39) 29 (21-38)
90 (85-90) 86 (72-96)
{l/8/4/5/4l {9/3/6/3/l 1
797 (720-878) 773 (670-882)
39 (24-60) 42 (3&61)
33 (2544) 37 (2462)
89 (82-97) 87 (71-96)
* 1, West Spitsbergen; 2, Bear Island; 3, Kola; 4, Finnmark; 5, Lofoten/VesterHlen. B SD between adults (AdM, AdF) and juveniles (JuM and JuF); ANOVA and Tukey-test, p < 0.05.
2O”W t75”N)
0”
2O”E
4O”E
6fJ”E
8O”E
100%
Fig. 1. Small-scale map showing the five areas: Lofoten/VesterHlen, Finnmark, Kola, Bear Island and West Spitsbergen selected during the scientific catches of minke whales (Balaenoptera acutorostrata) in 1992.
L. Kleivane, J.U. Skaare/Environmental Pollution IO1 (1998) 231-239
233
was hydrogen on a SPB-5 60-m capillary column (0.25mm ID, 0.25~mm film) with 5% Ar/CH4 as makeup gas. The chromatographic data were calculated using Maxima 820 Chromatography Workstation (Millipore Waters) software on an Olivetti PC M290. The standards included 21 PCB-congeners: PCB nos. -28, -74, -66, -101, -99, -110, -149, -118, -153, -105, -141, -138, -187, -128, -156, -157, -180, -170, -194, -206 and -209, pesticides: DDTs (dichlorodiphenyltrichloroethane) (pq’-DDT, P,P’-DDE, P,$-DDD, oq’DDT and o,p’-DDD), oxychlordane, cis-chlordane, transnonachlor, hexachlorocyclohexane-isomers (HCHb): yHCH, et-HCH, 8-HCH, and hexachlorobenzene (HCB). The PCB nos -28, -74 and -141 were not quantified on the GC-column in this study, due to co-elution problems (PCB no.74) and concentations close to or below the detection limit (PCB nos -28 and -141). The relative high level of PCB 128 in northeast Atlantic minke whales is suspected to involve a toxaphene congener CHB 50.
detector. Linearity was determined routinely, and varied from between 2 and 3 times the concentrations of the highest standard (SO-100 ng ml-‘). Sample dilution was carried out outside these limits. Analytical quality was certified by participation in international intercalibration tests on PCBs in marine material (Anon, 1995).
2.2. Analytical quality assurance
3. Results
Percent recovery was calculated for each sample series by adding a known amount of a PCB and/or pesticide standard to two uncontaminated blubber samples. Acceptable recovery was 8&110% of added standard. Reproducibility was continuously tested by analyzing control samples (ring seal [Phoca hispida] blubber) in each series. For the PCB-congeners, the detection limits in the matrix varied 0.005-0.017 ugg-‘; for the dichloro(DDT)-components 0.006 diphenyltrichlorethane 0.019 pg g-i. For chlordanes, the detection limits varied 0.005-0.007ugg-‘, for HCHs 0.003-0.015~gg-1, and for hexaclorobenzene (HCB) 0.002 ug gg ‘. Quantifications were carried out within the linear range of the
The levels of XPCB (18 PCB congeners; PCB nos -66, -101, -99, -110, -149,-118, -153, -105, -138, -187, -128, -156, -157, -180, -170, -194, -206and -209), XDDT (pq’-DDT, P,$-DDE, p,$-DDD, o,p’-DDT and o,p’-DDD), XHL (oxychlordane, trans-chlordane, cischlordane, trans-nonachlor, cis-nonachlor), XHCH (y-HCH, IX-HCH, B-HCH) and HCB found in blubber samples of northeast Atlantic minke whales are presented as mean levels, median levels and ranges in Table 2. The ZZPCB and CDDT were the major contaminants, with mean concentrations and ranges (minimum-maximum) of 3.8 (0.6-20.8) ug g-* lipid weight and 2.5 (0.5-14.8) ug g-’ lipid weight, respectively.
Table 2 Concentrations
(mean/median
2.3. Statistical analysis Analysis of variance (ANOVA) and Tukey’s test were used for comparisons of OC concentrations between the four whale groups (JuM, JuF, AdM and AdF). Least squares multiple parameters-test (cf. Sokal and Rohlf, 1981) was used to identify relationships between the blubber concentrations of contaminant (dependent variable) and biological parameters. All variables were log-transformed to conform with the requirements of the tests.
and range in pg gg’ lipid weight) of EPCB, EDDT, ECHL, EHCH
and HCB in blubber of minke whales
(Balaenoptera acutorostrata) from northeast Atlantic waters
Month
Number (n)
EPCBa Mean/median (range)
EDDT= Mean/median (range)
XHL= Mean/median (range)
EHCH Mean/median (range)
HCB Mean/median (range)
Juveniles Males (JuM)
July/August
15
Females (JuF)
July/August
13
2.9812.40 (0.60-5.82) 3.7712.69 (1.38-10.37)
1.9411.63 (0.524.52) 2.7712.18 (0.946.56)
0.91/0.88 (0.3&l .96) 1.28/1.26 (0.463.19)
0.09/0.09 (0.04-0.18) 0.15/0.12 (0.060.58)
0.23/0.20 (0.14-0.47) 0.36/0.32 (0.17-1.08)
Adults Males (AdM)
July/August
22
Females (AdF)
July/August
22
5.7714.77 (2.28-20.76) 2.2712.15 (1.25-3.94)
3.8613.29 (1.27-14.76) 1.51/1.25 (0.7G3.37)
1.63/1.54 (0.48-5.07) 0.75/0.58 (0.28-1.88)
0.15/0.15 (0.06-0.39) 0.08jO.07 (0.04-0.18)
0.26jO.25 (0.12-0.38) 0.19/0.18 (0.08-0.43)
EPCB, sum of concentrations of 18 PCB congeners; EDDT, sum of concentrations of p,d-DDT, g,p’-DDE, p,p’-DDD, o,p’-DDT and o,p’-DDD; CCHL, oxychlorodane, trans-chlordane, cis-chlordane, trans-nonachlor, cis-nonachlor; EHCH, y-HCH, a-HCH, j3-HCH; HCB, hexachlorobenzene. a SD between adult males (AdM) and other groups (AdF, JuM and JuF); ANOVA and Tukey test, p < 0.05.
234
L. Kleivane, J.U. Skaare/Environmental Pollution 101 (1998) 231-239
3.1. Biological aspects
For all sex and age groups, the blubber thickness of dorsal (behind blowhole) and lateral (behind flipper) measurements varied from 16 to 61 mm and from 21 to 62 mm, respectively (Table 1). No significant differences in blubber thickness or percentage of extractable lipid in blubber were found between JuM and JuF, or between AdM and AdF. However, significantly higher blubber thickness was found in AdF compared to JuM and JuF at the dorsal site (~~0.05). Negative correlation was found between dorsal blubber thickness and the level of XHCH (p < 0.07). Negative correlation was also found between fat percentage and the levels of CHCH (p < 0.01) and HCB (p < 0.01). The HCB was negatively correlated with length of the whales (p < 0.01). Significantly higher concentrations of the three major pollutants (EPCB, EDDT and XHL) were found in mature males as compared to mature females and juveniles of both sexes, while no such relationship was found for EHCH and HCB (Table 2). 3.2. Geographical aspects Sex and maturity were used as covariates during the statistical test, due to the variation of these parameters at different locations. The concentrations of EPCB, EDDT, XHL, XHCH and HCB differed significantly between animals from certain areas. Significantly higher pollutant levels were found in the southernmost area, Lofoten/VesterHlen, compared to the other four locations (XPCB; p < 0.02) and Finnmark and Kola (XDDT; p < O.OS), while the blubber levels of XHL were significantly higher at Spitsbergen compared to those at Kola and Finnmark (~~0.02). Intermediate levels of XDDT were found at Spitsbergen and Bear Island, with the highest concentrations in the Bear Island area. Significantly higher CHCH levels were detected in animals from Lofoten/Vesterblen and Bear Island compared to the three other locations (p < 0.01). Lowest ‘CHCH levels were found in whales from the coast of Finnmark and Kola. HCB was significantly lower in Finnmark compared to the other four locations (p < 0.04). The highest concentrations were detected at the northernmost location, Spitsbergen. A strong intercorrelation between the three major pollutants EPCB, CDDT and XHL, and the minor pollutants XHCH and HCB, was found (Table 3).
3.3. OC pattern and ratios The PCB congeners 101, 99, 110, 149, 118, 153, 105, 138, 187, 128, 180 and 170 were detected in all the animals, while PCB nos 156 and 194, and PCB nos 66 and 157 were detected in > 90% and > 70% of all the animals, respectively. The higher chlorinated PCBs (nos
Table 3 Correlation matrix of the blubber levels of CPCB, CDDT, CCHL, CHCH and HCB in minke whales (Balaenoptera acutorostrata) from northeast Atlantic waters
XPCB EDDT XHL CHCH HCB
XPCB
CDDT
CCHL
XHCH
HCB
1.oooo
0.9314 1.0000 0.9206 0.5556 0.6122
0.8667 0.9206 1.oOOo 0.6666 0.7336
0.4766 0.5556 0.6666 1.0000 0.7233
0.4909 0.6122 0.7336 0.7233 1.0000
0.9314 0.8667 0.4766 0.4909
XPCB, sum of concentrations of 18 PCB congeners; CDDT, sum of concentrations ofp,p’-DDT, p,p’-DDE, p,p’-DDD, o,p’-DDT and og’DDD; XHL, oxychlordane, trans-chlordane, cis-chlordane, transnonachlor, ci.s-nonachlor; XHCH, 7-HCH, a-HCH, B-HCH; HCB, hexachlorobenzene.
206 and 209) were detected in less than 40% of the whales. The major PCB congeners 153, 128, 138, 118, 180, 99 and 149 constituted 21.7%, 18.7%, 16.7%, 8.1%, 6.8%, 5.4% and 4.9% of CPCB, respectively. The PCB pattern in different sex and age groups is shown in Fig. 2. The overall mean ratio CDDT:CPCB in northeast Atlantic minke whales was 0.68 f 0.17, while the ratios DDE:EDDT and DDE:EPCB were 0.42 f 0.12 and 0.28 f 0.10, respectively. The major DDT compound was p,p’-DDE constituting 42.4~t 12.0% of XDDT. The other DDT components oq’-DDD, p,p’-DDD, o,p’-DDT and p,p’-DDT constituted 4.0* 1.3%, 17.5&4.0%, 13.0*4.3%, and 23.2+4.6% of XDDT, respectively. Of the HCH isomers, the a-HCH, P-HCH and y-HCH constituted 41.8* 12.0%, 41.6* 10.7% and 16.6*6.3%, respectively. The major chlordane component was transnonachlor constituting 49.8 & 6.1% of XHL, while cis-nonachlor, cis-chlordane and oxychlordane constituted 19.6*2.3%, 17.4&2.0%, and 9.7&2.4% of XHL, respectively.
4. Discussion 4.1. Ecological aspects In mammals, exposure to organochlorines is exclusively connected to dietary contamination. Top predator species of marine food webs accumulate high levels of these lipophilic and persistent chemicals (Skaare et al., 1990; Muir et al., 1992; Norheim et al., 1992; Tatsukawa, 1992; Kleivane et al., 1996; Bernhoft et al., 1997). Recent ecological studies indicate that the northeast Atlantic minke whale is an opportunistic top predator that feeds on regionally abundant prey. Counter to previous findings in the area of Spitsbergen and Bear Island in 1950 and 1989 (Jonsgbrd, 1982; Nordray and Blix, 1992), the minke whale diet in the 1992 season was dominated by fish, while the dietary contribution of
L. Kleivane, J.U. SkaarelEnvironmental Pollution 101 (1998) 231-239
PCB-209
and summer feeding areas at higher latitudes. In this context, the exposure to pollutants is mainly through feeding in highly productive waters at higher latitudes. Counter to the euryphagous nature of northeast Atlantic minke whales, Antarctic minke whales show a rather stenophagous krill-eating behaviour (Ichii and Kato, 1991). Tanabe et al. (1986) conclude that immature southern minke whales carried higher concentration ratios of DDEs to PCBs in their tissues than mature specimens, due to different feeding strategies. Thus, immature minke whales remain at lower latitudes during the summer and feed not only on euphausiids, but also on copepods and fish, whereas adult individuals migrate to higher latitudes and base their diet solely on less polluted euphausiids (Tanabe et al., 1986). However, during extensive studies of feeding behaviour of minke whales in northeast Atlantic waters (Haug et al., 1996) no similarities to the age-dependent feeding strategy of southern minke whales were found in the northeast Atlantic minke whale stock.
El AdF
I PCB-205
?? AdM
PCB-194
?? JuF JuM
a
PCB-170 PCB-180 PCB-157
235
Ii
4.2. Biological aspects 4.2.1.
0
20
40
60
80
100
120
140
Percentage of PCB 153 Fig. 2. Comparison of polychlorinated biphenyl (PCB) congener pattern of sum of concentrations of 18 PCB congeners (EPCB) in immature and mature minke whales (Ealaenoptera acutorostrata) of both sexes, caught in July and August in 1992. Data are presented as relative values to PCB 153, with SD. ‘Significantly higher ratio in mature females (AdF) compared to mature males (AdM). *Significantly higher ratio in AdM compared to mature AdF. %ignificantly lower ratio in female juveniles (JuF) compared to AdM. 4Significantly lower ratio in JuF compared to AdF.
planktonic crustaceans was very small (Haug et al., 1995). Variations in prey availability may have impact on the feeding habits and, possibly, on the migratory behaviour of northeast Atlantic minke whales (Haug et al., 1996). At present, no conclusive information on the migratory pattern of this whale species in north Atlantic waters is available. However, it is thought that the northeast Atlantic minke whale stock migrate seasonally between winter breeding areas at lower latitudes
Sex and age
The role of migration patterns in dietary OC exposure of various age- and sex-groups of northeast Atlantic minke whales is unclear. Although significant differences in the ratios of certain PCB congeners were found between different groups, no overall pattern of difference between sexes or age groups was found. When comparing different whale groups, there was a sexrelated difference in concentrations of PCB, DDT and chlordane in mature animals. Thus, a twofold concentration of these xenobiotics were found in males compared to females. This is comparable with similar studies on mature southern hemisphere minke whales (Tanabe et al., 1986) and is attributed to the OC transfer from females during gestation and lactation to the offspring, common in most marine mammal species (Tanabe et al., 1982; Aguilar et al., 1995; Espeland et al., 1997). In mature southern minke whales feeding only on euphausiids, sexes are probably equally exposed to OCs, while the minke whale diet in the northern hemisphere varies between different geographical areas, seasons, and years (Haug et al., 1996), and mature animals may have different feeding regimes and thus different OCs exposure. The data on minke whale prey indicate a considerable heterogeneity in the diet considering different years, seasons and different geographical areas (JonsgHrd, 1982; Nordoy and Blix, 1992; Haug et al., 1996). The present levels and patterns of OCs may reflect a cumulative exposure to these contaminants in different areas through seasons in a longlived animal like the minke whale, rather than actual geographical differences. However, it is interesting to note that both low and high OC contaminated minke
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(p&I) IIaUM0.I~pUE “aI.jS‘O ‘S%WpUl3 wasaId 01 ‘“1~“‘s ‘ESI 836 uoyj IualysJad ssaI s! ‘suoy!sod mod-vmu palnylsqnsun 8u~~ey ‘101 836 awls Ba.w eas walea 83d dq /ueaDo ~guvpv wayl.Iou aql ueyl also pacwangu! Q3a.up alow s! t2aJt! aDuaIMe7 2s 30 3lnf> ayl keys alwpu! osjt? pIno IaAaI 101 836 aA!leIaJ u! a3ua -lagp ayl ‘.IalzaMoH *suo$aJ 1wydv.Boa2l ayl uaaMlaq uoy~~yws~uo~ ,taJd II! saDua.raa!p Icq paugldxa aq kU s!Y.L ‘%LZI w S“!W ESI/IOI Pue StDdX 30 %LZ Ig IOI 83d Pvy SaIeyM ~~W~IlV l=MylJou =Jl s’=JayM ‘%OZ 01 01 Inoqv 30 so!W SSI/IOI umu Pue ‘S83dX 30 %5 > IO1 836 P”Y SaIqM quq1v maywu ayL .papa)ap 101 836 30 JunouIa ayl ur s! suoy?Indod apyM 0~) ayl uaaMlaq aDualag!p JO@U e ‘JaAaMoH .alqwedwoD aJt! dIIt?aJ sAaA.InsOM) u10.t~ slep lualxa JBYM 0~ a!onlEAa 01 ~p-wgp 11 %u!~etu snyl ‘a31ws s! (‘Dla snws aA!pnpoJdaJ ‘snlt?]s I??uoyJ)nu ‘XaS‘ago) sIEnp!A!pu! paldures aq) 30 BoIo!q ayl uo uopw1.1o3u~ uayM uoynw YJ!M auop aq sbt?~~t! ‘JaAaMoy ‘pInoys sa! -pnls pw suogqndod uaaMlaq eltrp 30 30 uosyredruo3 .ys!xa 01 waas sruawd 30 u! saDuaJag!p uoyyndodralu~ awes ‘(~661 “1~2Ia _raylnef)) aDuaiMa7 ‘1s 30 3Inf) ay, ~0~3 sajvyM ay+u ~UBIJV ~IJOU u! ~30 uo 3~0~ paqsgqnd ICpumaJ E u! pa$JodaJ slinsal BuypuodsaJJoD aql SE a&w aCurs ay) UI aJaM elvp 30 IuasaJd ayL
.palo@ aq IOU plnoys sdnoJ% a%v uaaMlaq put? saxas uaaM)aq sa@aleqs %wpaa3lua.raBIp 30 13aga ayl ‘IahaMoH yyutay:, asay uuo3sueqo!q 0~ a,! -pqv ItguaJagp IDagal Aw,uqDo)s aIeyM ay+u 3guvpv wayo.tou ayl II! saiaw a.nwuny 01 paJEduro3 saIeuxa3 aJnleuIuII ui sIaAaI30 Jayi$y 30 buapual aql ‘aJo3alayL yauu.u~!w auy?tu u! &g3e ar.ulCzua30 IaAaIatjl u! uoge -PEA pa]yaJ-xas paqyap (gj61) ~Ic0sqof) *xas pw a% qJ!M 6JEA 01 sleaddz put? ‘( 1661) gI0puty-j put? sad!s 6q paq!lDsap uaaq soy s~er.ur.uwuu! uoy23y!xolap aukua 30 &3Ede:, aqL *salgyM aquiur aJaydsway uJay)nos put! gu~pv lsaaqyou u! la3suEq uoyslaua% PUB &pedaD Dgoqwaw aIqe.n?dr_uoDE %ugsa%%ns ‘sv,nwyIod asayl 01 uogqaJ luapuadap xas .mI~uI!S t! MOqS Sq3OJSaIeyM
237
L. Kleivane. J.U. SkaarejEnvironmental Pollution 101 (1998) 231-239
pattern of minke whales resembles more that of a pinniped species than that corresponding to odontocete cetaceans (Kleivane et al., 1995; Table 4). The harp seal (Phocu groenlandica), which inhabits and feeds in the northern part of the feeding areas of the northeast Atlantic minke whale stock, is an opportunistic predator (Nilssen et al., 1994), and therefore resembles the minke whale more than the more coastal harbour porpoise (Phocoena phocoena), which feeds entirely on fish species (Aarefjord et al., 1995). A review by O’Shea and Brownell (1994) shows that few studies have determined organochlorine contaminants in representative samples of different baleen whale species inhabiting north Atlantic waters. Only larger sample sizes of sei and fin whales (Borrell and Aguilar, 1987; Borrell, 1993), and north Atlantic right whales (Eubuluenu glacialis) (Woodley et al., 1991) have been obtained to characterize organochlorine contaminants on a species level. In addition, a recent study (Gauthier et al., 1997) reports organochlorine data in blubber biopsies from fin (B. physulus), blue (Buluenopteru musculus) and humpback (Megupteru novueungliue) whales summering in the Gulf of St. Lawrence. The low organochlorine contamination in baleen whales relative to other marine mammal species is a general trend. However, baleen whales, odontocete cetaceans, and pinnipeds are not a biologically homogeneous group. Parameters like age, sex, nutritional status, health status, life span, size and metabolic rates may, in addition to diet, influence the level and pattern of OCs in these species (Aguilar et al., 1995; Skaare, 1995) Considerable differences may also exist in the xenobiotic metabolization capacity of these phylogenetically distant species (Tanabe et al., 1988; Norstrom et al., 1992). The PCB congener pattern in mature males of different Arctic and sub-Arctic marine mammal species is shown in Fig. 3. The minke whale xenobiotic metabolizing enzymes of the cytochrome P450 enzyme system were described by Goksoyr (1995). The same author found certain differences in the cytochrome P450 enzymes in minke whales and harp seals. Murk et al. (1994) reported in vitro metabolism of 3,3’, 4,4’-tetrachlorbiphenyl in harbour porpoise, however, no relevant information is available on the ability of this species to metabolise PCBs with adjacent nonchlorinated metu and puru positions. Thus, interspecies differences in xenobiotic metabolizing enzyme systems may explain some of the differences in OC contamination levels found between minke whale, harp seal and harbour porpoise. Aguilar (1984, 1988) indicates the possibility of comparing ratios of various chemicals to differentiate between offshore and inshore populations of the same species, interspecies contamination and the distance from pollution sources. When comparing the ratios CDDT:ZPCB and DDE:XDDT in adult males of the
?? minke whale ?? harbour porpoise harp seal
0
20
40
M)
80
104
Percentage of PCB 153 Fig. 3. Comparison of PCB congener pattern in males of three marine mammals, the minke whale (Balaenoptera acutorostrata), the harbour porpoise (Phocoena phocoena) and the harp seal (Phoca groenlandica) inhabiting entirely or partly Arctic or sub-Arctic waters. Data are presented as relative values to PCB 153, with standard deviation. ‘Significantly higher ratio in the minke whale compared to harbour porpoise and harp seal. *Significantly higher ratio in the harbour porpoise compared to minke whale and harp seal. ‘Significantly decreasing ratios from minke whale to harp seal to harbour porpoise. 4Significantly decreasing ratios from harbour porpoise to minke whale to harp seal.
three above species, certain similarities and differences were found. In minke whale, harbour porpoise and harp seal, similar ratios EDDT:EPCB were found (0.70,0.71 and 0.73, respectively). In minke whale, harbour porpoise and harp seal, the ratios DDE:XDDT were 0.38, 0.41 and 0.84, respectively. This indicates a proportionally higher concentration of DDE to XDDT in the Barents Sea harp seal population than the more coastal harbour porpoise and the migrating minke whale, which may reflect a past exposure to DDTs.
238
L. Kleivane, J. U. SkaarejEnvironmental Pollution 101 (1998) 231-239
Acknowledgements The present study was financially supported by the Norwegian Research Council under the Norwegian Marine Mammal Research Program 1989-1994. The authors acknowledge Oskar Espeland, Erna Stai and Anuschka Polder for performing the OC analyses, and Tore Schweder for statistical advice. We would also like to thank the scientists and the whalers participating in the scientific captures in 1992, Ivar Christensen at the Institute of Marine Research and Tore Haug at the Norwegian Institute of Fisheries and Aquaculture.
References Aaretjord, H., Bjorge, A.J., Kinze, CC., Lindstedt, I., 1995. Diet of the harbour porproise (Phocoena phocoena) in Scandinavian waters. Report of the International Whaling Commission, (special issue 16), 21 l-222. Aguilar, A., 1984. Relationship of DDE/EDDT in marine mammals to the chronology of DDT input into the ecosystem. Canadian Journal of Fisheries and Aquatic Sciences 41, 84O-844. Aguilar, A., 1988. Use of trace compounds to discriminate home ranges in cetaceans. Report of the International Whaling Commission 38, 125. Aguilar, A., Borrell, A., Pastor, T., 1995. Factors affecting variability of persistent pollutant levels in cetaceans. Presented at the Workshop on Chemical Pollutants and Cetaceans, Bergen, Norway, SC/ M95/P6 Anon, 1995. Report on the results of the ICES/IOC/OSPARCOM intercomparison programme on the analyses of chlorobiphenyls in marine media-step 2. ICES cooperative research report no. 207. Barrie, L.A., Gregor, D., Hargrave, B., Lake, R., Muir, D., Shearer, R., Tracey, B., Bidleman, T., 1992. Arctic contaminants: sources, occurence and pathways. Science of the Total Environment 122,1-74. Bernhoft, A., Skaare, J.U., 1994. Levels of selected individual polychlorinated biphenyles in different tissues of harbour seals (Phoca vitulina) from the southern coast of Norway. Environmental Pollution 86, 99-107. Bernhoft, A., Wiig, O., Skaare, J.U., 1997. Organochlorines in polar bears (Ursus maritimus) at Svalbard. Environmental Pollution 96, 159-175. Brevik, E.M., 1978. Gas chromatographic method for the determination of organochlorine pesticides in human milk. Bulletin of Environmental Contamination Toxicology 19,281-286. Borrell, A., 1993. PCB and DDTs in blubber of cetaceans from the northeastern north Atlantic. Marine Pollution Bulletin 26, 14615 1. Borrell, A., Aguilar, A., 1987. Variations in DDE percentage correlated with total DDT burden in the blubber of fin and sei whales. Marine Pollution Bulletin 18, 70-74. Christensen, I., 1981. Age determination of minke whales, Balaenoptera acutorostrata, from laminated structures in the tympanic bullae. Report of the International Whaling Commission 31, 245 253. Espeland, O., Kleivane, L., Haugen, S., Skaare, J.U., 1997. Organochlorines in mother and pup pairs in two arctic seal species, harp seal (Phoca groenlandica) and hooded seal (Cystophora cristata. Marine Environmental Research 44, 3 1s330. Gauthier, J.M., Metcalfe, C.D., Sears, R., 1997. Chlorinated organic contaminants in blubber biopsies from northwestern Atlantic balaenopterid whales summering in the Gulf of St. Lawrence. Marine Environmental Research 44(2), 201-223.
Gokseyr, A., 1995. Cytochrome P450 in marine mammals: isozyme forms, catalytic functions, and physiological regulations. In: Blix, A.S., Walloe, L. and Ulltang, 0. (Eds.). Whales, seals, fish and man, Elsevier Science, Amsterdam, pp. 629639. Haug, T., Gjesreter, H., Lindstrsm, U., Nilssen, K.T., 1995. Diet and food availability for northeast Atlantic minke whales (Balaenoptera acutorostrata), during the summer of 1992. ICES Journal of Marine Science 52, 77-86. Haug, T., Lindstrem, U., Nilssen, K.T., Rottingen, I., Skaug, H.J., 1996. Diet and food availability for northeast Atlantic minke whales (Balaenoptera acutorostrata). Report of the International Whaling Commission 46, 371-382. Henry, J., Best, B.P., 1983. Organochlorine residues in whales landed at Durban, South Africa. Marine Pollution Bulletin 14,223227. Ichii, T., Kato, H., 1991. Food and daily food consumption of southern mink: whales in the Antarctic. Polar Biology 11, 4799487. Jonsgard, A., 1951. Studies on the little piked whale or minke whale (Balaenoptera acutorostrata Lacepede. Norsk Hvalfangsttidene 40, 209232. Jonsgard, A., 1982. The food of minke whale (Balaenoptera acutorostrata) in the northern north Atlantic waters. Report of the Intemational Whaling Commission 32, 259-262. Kasamatsu, F., Nishiwaki, S., Ishikawa, H., 1995. Breeding areas and southbound migrations of southern minke whales Balaenoptera acutorostrata. Marine Ecology Progress Series 119, l-10. Kleivane, L., Skaare, J.U., Bjorge, A., de Ruiter, E., Reijnders, P.J.H., 1995. Organochlorine pesticide residues and PCBs in harbour porpoise (Phocoena phocoena) incidentally caught in Scandinavian waters. Environmental Pollution 89, 137-146. Kleivane, L., Espeland, O., Fagerheim, K.A., Hylland, K., Polder, A., Skaare, J.U., 1997. Organochlorine pesticide residues and PCBs in the east ice harp seal population. Marine Enviromental Research 3,117-130. Muir, D.C.G., Wagemann, R., Hargrave, B.T., Thomas, D.J., Peakall, D.B., Norstrom, R.J., 1992. Arctic marine ecosystem contamination Science of the Total Environment 122, 75-134. Murk, A., Morse, D., Boon, J., Brouwer, A., 1994. In vitro metabolism of 3,3\,4,4\-tetrachlorobiphenyl in relation to ethoxyresorufin0-deethylase activity in liver microsomes of some wildlife species and rat. European Journal of Pharmacology Environmental Toxicology and Pharmacology Section 270,253-261. Nilssen, K.T., Ahlquist, I., Eliassen, J.E., Haug, T., Lindblom, L., 1994. Studies of food availability and diet of harp seals (Phoca groenlandica) in the southern Barents Sea in February 1993, ICES CM. 1994/N, pp. 12-24. Nordoy, E.S., Blix, A.S., 1992. Diet of the minke whales in the northeastern Atlantic. Report of the International Whaling Commission 42, 393-398. Norheim, G., Skaare, J.U., Wiig, PI., 1992. Some heavy metals, essential elements, and chlorinated hydrocarbons in polar bear (Ursus maritimus) at Svalbard. Environmental Pollution 77, 51-57. Norstrom, R.J., Simon, M., Muir, D.C.G., Schweinsburg, R.E., 1988. Organochlorine contaminants in arctic marine food chains: identification, geographical distribution, and temporal trends in polar bears. Environmental Science & Technology 22, 1063-1071. Norstrom, R.J., Muir, D.C.G., Ford, C.A., Simon, M., Macdonald, C.R., Beland, P., 1992. Indications of P450 monooxygenase activeties in beluga (Delphinapterus leucas) and narwal (monodon monoceros) from patterns of PCB, PCDD and PCDF accumulation. Marine Environmental Research 34,267-272. O’Shea, T.J., Brownell, R.L. Jr, 1994. Organochlorine and metal contaminants in baleen whales: a review and evaluation of conservation implications. Science of the Total Environment 154, 179-200. Sipes, LG., Gandolfi, A.J., 1991. Biotransformation of toxicants. In: Amdur, M.O., Doull, J., Klaasen, C.D. (Eds.). Casarett and Doull’s toxicology. Pergamon Press, New York, pp. 88-126.
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Skaare, J. 1995. Organochlorine contaminants (OCs) in marine mammals from the norwegian Arctic. In: Schytte-Blix, A., Wallo, L., Ulltang, 0. @is.). Whales, seals, fish and man. Elsevier Science Amsterdam, pp. 599-605. Skaare, J.U., Markussen, N.H., Norheim, G., Haugen, S., Holt, G., 1990. Levels of polychlorinated biphenyls, organochlorine pesticides, mercury, cadmium, copper, selenium, arcenic, and zinc in the harbour seal. Phoca vitulina, in norwegian waters. Environmental Pollution 66, 309324. Sokal, R.R., Rohlf, F.J., 1981. Biometry. Freeman and Co, New York. Tanabe, S., Tatsukawa, R., Maruyama, K., Miyazaki, N., 1982. Transplacental transfer of PCBs and chlorinated hydrocarbon pesticides from the pregnant striped dolphin (Stenella coerdeoafba) to her fetus. Agricultural and Biological Chemistry 45, 1249-1254. Tanabe, S., Miura, S., Tatsukawa, R., 1986. Variation of organochlorine residues with age and sex in antarctic minke whale. National Institute of Polar Research, Tokyo. Memoirs. Special Issue 44, 174-181.
239
Tanabe, S., Watanabe, S., Kan, H., Tatsukawa, R., 1988. Capacity and mode of PCB metabolism in small cetaceans. Marine Mammal Science 4, 103-124. Tanabe, S., Sayaka, A., Yoshihiro, F., Hidehiro, K., Tatsukawa, R., 1995. Persistent organochlorine residues in the antarctic minke whale, Balaenoptera acutorostrata. Presented at the Workshop on Chemical Pollutants and Cetaceans, Bergen, Norway, SC/M95/Pl3. Tatsukawa, R., 1992. Contamination of chlorinated organic substances in the ocean ecosystem. Water Science and Technology 25, l-8. Wang-Andersen, G., Skaare, J.U., Presterud, P., Steinnes, E., 1993. Levels and congener pattern of PCBs in arctic fox, Alopex lagopus, in Svalbard. Environmental Pollution 82, l-7. Wania, F., Mackay, D., 1993. Global fractionation and cold condensation of low volatility organochlorine compounds in polar regions. Ambio 22, l&18. Woodley, T., Brown, M., Kraus, S., Gaskin, D., 1991. Organochlorine levels in North Atlantic right whale (Eubalaena glacialis) blubber. Archives of Environmental Contamination and Toxicology 21, 141-145.
Environmental Pollution 101 (1998) 231-239
Organochlorine
contaminants in northeast Atlantic minke whales (Balaenoptera acutorostrata) L. Kleivane a, J.U. Skaare a$bt*
aNational Veterinary Institute, PO Box 8156 Dep., N-0033 Oslo 1, Norway bNorwegian College of Veterinary Medicine, Department of Pharmacology, Microbiology and Food Hygiene, Division of Pharmacology and Toxicology, PO Box 8146 Dep., N-0033 Oslo 1. Norway
Received 7 July 1997; accepted 19 February 1998
Abstract Blubber samples of 72 minke whales (Buluenopferu acutorostrutu) were obtained from the northeast Atlantic in July and August 1992, and evaluated for organochlorine contamination. The following organochlorines were determined: the industrial chemicals PCBs (polychlorinated biphenyls), and the organochlorine pesticides DDTs (dichlorodiphenyltrichloroethanes), HCHs (hexachlorocyclohexaneb), HCB (hexachlorobenzene) and CHLs (chlordanes). The concentrations of IZPCB (sum of concentrations of 18 PCB congeners) and XDDT (sum of concentrations of p,P’-DDT, p,p’-DDE, p,p’-DDD, o,p’-DDT and o,p’-DDD) ranged from 0.6-20.8 and 0.5-14.8 pgg-’ lipid weight, with mean concentrations at 3.8 and 2.5 pgg-’ lipid weight, respectively. The mean concentrations of HCB, the chlordane metabolites oxychlordane, cis-chlordane and truns-nonachlor, and the HCH isomers (a-, f& and y-HCH) were all < 1 hgg-’ lipid weight. Significantly higher concentrations of the three major pollutants (XPCB, XDDT and XCHL) were found in mature males as compared to mature females and juveniles of both sexes. No such relationship was found for XHCH and HCB. Stomach contents of northeast Atlantic minke whales indicate considerable heterogeneity in the diet when comparing different years, seasons and geographical areas. However, without knowing more about the minke whale migration pattern, or possible geographical segregation with age and sex, the interchemical variation of organochlorines between sampling areas may not reflect true geographical differences. 0 1998 Elsevier Science Ltd. All rights reserved. Keywords: Marine mammals; Minke whale; Pollution; Organochlorines;
1. Introdllction The presence of persistent organochlorines (OCs) in biota from ‘pristine’ areas like the Arctic and the Antarctic, are primarily ascribed to long-range transport. An essential part of this transport is thought to be of aerial origin, but transport by ocean currents and biological transport are also likely to occur (Barrie et al., 1992; Wania and Mackay, 1993). Surprisingly high OC levels, especially polychlorinated biphenyls (PCBs) and certain chlordane (CHL) metabolites, are found in Arctic and sub-Arctic species (Norstrom et al., 1988; Norheim et al., 1992; Wang-Andersen et al., 1993; Kleivane et al., 1995; Bernhoft et al., 1997. In terms of population sizes and feeding habits, the minke whale (Buluenopteru ucutorostratu) is an important species in
* Corresponding author. Tel.: + 47-22-59-7444; fax: + 47-22-597459; e-mail: [email protected] 0269-7491/98/%19.00 0 1998 Elsevier Science Ltd. All rights reserved. PII: SO269-7491(98)00043-8
PCB; DDT
the highly productive waters of higher latitudes both at
the northern and southern hemisphere. Minke whales from both hemispheres are thought to have opposite summer to winter migration patterns, undertaking seasonal migration between breeding and feeding areas at lower and higher latitudes, respectively. There is no evidence of exchange of genetic material between northern and southern minke whales (Kasamatsu et al., 1995). An intraspecies comparison of pollutant loads in specimens collected from Arctic and Antarctic waters may elucidate differences and similarities of levels and patterns of OC pollutants present at higher latitudes. The aims of this study was to investigate and characterize the OC pattern and levels in the northeast Atlantic minke whale stock, and to compare it with similar data previously reported by Tanabe et al. (1995) in southern hemisphere minke whales. This investigation also attempts to understand biological-related explanations of observed patterns of organochlorine concentrations based on age, sex and blubber characteristics.
L. Kleivane. J.U. SkaarelEnvironmental Pollution 101 (1998) 231-239
232
2. Materials and methods
investigations: West of Spitsbergen, Bear Island, coast of Kola, coast of Finnmark and Lofoten/VesterHlen (Fig. 1).
The animals were captured during July and August 1992 at the coasts of Nordland and Finnmark in northern Norway, in the Russian sector along the Kola Peninsula, and Arctic areas around Bear Island and Spitsbergen. Subcutaneous samples of 72 minke whales were obtained. Whales were classified according to sex and age as: adult males (AdM), juvenile males (JuM), adult females (AdF) and juvenile females (JuF; Table 1). Male sexual maturity was determined by paired testis weight of more than 500 grams (JonsgHrd, 1951; Christensen, 1981), whereas female sexual maturity was determined by presence of a foetus or corpora albicantia. Five separate sampling areas were defined during these
2.1, Analytical procedures
Weighed blubber samples were homogenized using an Ika Ultra Turrax, and PCB no. 112 was added as an internal standard. The sample was extracted twice with cyclohexane and acetone using an ultrasonic homogenizer (4710 series, Cole-Parmer), followed by clean-up with sulfuric acid (Brevik, 1978; Bernhoft and Skaare, 1994), and automatically injected in the split-mode (1 ul, 1:30; Fisons autosampler AS 550) on a Carlo Erba, HRGC 5300 Mega Series gas chromatograph and an electron capture detector (ECD-63Ni). The carrier gas
Table 1 Biological data (sex, age-groups, body length, blubber thickness, lipid content in blubber, area and time of catch) of minke whales (Balaenoptera acutorostrata) from northeast Atlantic waters
Juveniles Males (JuM) Females (JuF) Adults Males (AdM) Females (AdF)
Month
Number (n)
July/August July/August
15 13
July/August July/August
22 22
Area distribution Il/2/3/4/5~* (n)
Length mean (range cm)
Blubber thicknessa blow hole; mean (range mm)
Blubber thickness” flipper; mean (range mm)
Percentage lipid in blubber
{O/4/5/4/2} {5/l/l/2/4}
634 (500-712) 625 (485-742)
35 (1649) 33 (2541)
31 (24-39) 29 (21-38)
90 (85-90) 86 (72-96)
{l/8/4/5/4l {9/3/6/3/l 1
797 (720-878) 773 (670-882)
39 (24-60) 42 (3&61)
33 (2544) 37 (2462)
89 (82-97) 87 (71-96)
* 1, West Spitsbergen; 2, Bear Island; 3, Kola; 4, Finnmark; 5, Lofoten/VesterHlen. B SD between adults (AdM, AdF) and juveniles (JuM and JuF); ANOVA and Tukey-test, p < 0.05.
2O”W t75”N)
0”
2O”E
4O”E
6fJ”E
8O”E
100%
Fig. 1. Small-scale map showing the five areas: Lofoten/VesterHlen, Finnmark, Kola, Bear Island and West Spitsbergen selected during the scientific catches of minke whales (Balaenoptera acutorostrata) in 1992.
L. Kleivane, J.U. Skaare/Environmental Pollution IO1 (1998) 231-239
233
was hydrogen on a SPB-5 60-m capillary column (0.25mm ID, 0.25~mm film) with 5% Ar/CH4 as makeup gas. The chromatographic data were calculated using Maxima 820 Chromatography Workstation (Millipore Waters) software on an Olivetti PC M290. The standards included 21 PCB-congeners: PCB nos. -28, -74, -66, -101, -99, -110, -149, -118, -153, -105, -141, -138, -187, -128, -156, -157, -180, -170, -194, -206 and -209, pesticides: DDTs (dichlorodiphenyltrichloroethane) (pq’-DDT, P,P’-DDE, P,$-DDD, oq’DDT and o,p’-DDD), oxychlordane, cis-chlordane, transnonachlor, hexachlorocyclohexane-isomers (HCHb): yHCH, et-HCH, 8-HCH, and hexachlorobenzene (HCB). The PCB nos -28, -74 and -141 were not quantified on the GC-column in this study, due to co-elution problems (PCB no.74) and concentations close to or below the detection limit (PCB nos -28 and -141). The relative high level of PCB 128 in northeast Atlantic minke whales is suspected to involve a toxaphene congener CHB 50.
detector. Linearity was determined routinely, and varied from between 2 and 3 times the concentrations of the highest standard (SO-100 ng ml-‘). Sample dilution was carried out outside these limits. Analytical quality was certified by participation in international intercalibration tests on PCBs in marine material (Anon, 1995).
2.2. Analytical quality assurance
3. Results
Percent recovery was calculated for each sample series by adding a known amount of a PCB and/or pesticide standard to two uncontaminated blubber samples. Acceptable recovery was 8&110% of added standard. Reproducibility was continuously tested by analyzing control samples (ring seal [Phoca hispida] blubber) in each series. For the PCB-congeners, the detection limits in the matrix varied 0.005-0.017 ugg-‘; for the dichloro(DDT)-components 0.006 diphenyltrichlorethane 0.019 pg g-i. For chlordanes, the detection limits varied 0.005-0.007ugg-‘, for HCHs 0.003-0.015~gg-1, and for hexaclorobenzene (HCB) 0.002 ug gg ‘. Quantifications were carried out within the linear range of the
The levels of XPCB (18 PCB congeners; PCB nos -66, -101, -99, -110, -149,-118, -153, -105, -138, -187, -128, -156, -157, -180, -170, -194, -206and -209), XDDT (pq’-DDT, P,$-DDE, p,$-DDD, o,p’-DDT and o,p’-DDD), XHL (oxychlordane, trans-chlordane, cischlordane, trans-nonachlor, cis-nonachlor), XHCH (y-HCH, IX-HCH, B-HCH) and HCB found in blubber samples of northeast Atlantic minke whales are presented as mean levels, median levels and ranges in Table 2. The ZZPCB and CDDT were the major contaminants, with mean concentrations and ranges (minimum-maximum) of 3.8 (0.6-20.8) ug g-* lipid weight and 2.5 (0.5-14.8) ug g-’ lipid weight, respectively.
Table 2 Concentrations
(mean/median
2.3. Statistical analysis Analysis of variance (ANOVA) and Tukey’s test were used for comparisons of OC concentrations between the four whale groups (JuM, JuF, AdM and AdF). Least squares multiple parameters-test (cf. Sokal and Rohlf, 1981) was used to identify relationships between the blubber concentrations of contaminant (dependent variable) and biological parameters. All variables were log-transformed to conform with the requirements of the tests.
and range in pg gg’ lipid weight) of EPCB, EDDT, ECHL, EHCH
and HCB in blubber of minke whales
(Balaenoptera acutorostrata) from northeast Atlantic waters
Month
Number (n)
EPCBa Mean/median (range)
EDDT= Mean/median (range)
XHL= Mean/median (range)
EHCH Mean/median (range)
HCB Mean/median (range)
Juveniles Males (JuM)
July/August
15
Females (JuF)
July/August
13
2.9812.40 (0.60-5.82) 3.7712.69 (1.38-10.37)
1.9411.63 (0.524.52) 2.7712.18 (0.946.56)
0.91/0.88 (0.3&l .96) 1.28/1.26 (0.463.19)
0.09/0.09 (0.04-0.18) 0.15/0.12 (0.060.58)
0.23/0.20 (0.14-0.47) 0.36/0.32 (0.17-1.08)
Adults Males (AdM)
July/August
22
Females (AdF)
July/August
22
5.7714.77 (2.28-20.76) 2.2712.15 (1.25-3.94)
3.8613.29 (1.27-14.76) 1.51/1.25 (0.7G3.37)
1.63/1.54 (0.48-5.07) 0.75/0.58 (0.28-1.88)
0.15/0.15 (0.06-0.39) 0.08jO.07 (0.04-0.18)
0.26jO.25 (0.12-0.38) 0.19/0.18 (0.08-0.43)
EPCB, sum of concentrations of 18 PCB congeners; EDDT, sum of concentrations of p,d-DDT, g,p’-DDE, p,p’-DDD, o,p’-DDT and o,p’-DDD; CCHL, oxychlorodane, trans-chlordane, cis-chlordane, trans-nonachlor, cis-nonachlor; EHCH, y-HCH, a-HCH, j3-HCH; HCB, hexachlorobenzene. a SD between adult males (AdM) and other groups (AdF, JuM and JuF); ANOVA and Tukey test, p < 0.05.
234
L. Kleivane, J.U. Skaare/Environmental Pollution 101 (1998) 231-239
3.1. Biological aspects
For all sex and age groups, the blubber thickness of dorsal (behind blowhole) and lateral (behind flipper) measurements varied from 16 to 61 mm and from 21 to 62 mm, respectively (Table 1). No significant differences in blubber thickness or percentage of extractable lipid in blubber were found between JuM and JuF, or between AdM and AdF. However, significantly higher blubber thickness was found in AdF compared to JuM and JuF at the dorsal site (~~0.05). Negative correlation was found between dorsal blubber thickness and the level of XHCH (p < 0.07). Negative correlation was also found between fat percentage and the levels of CHCH (p < 0.01) and HCB (p < 0.01). The HCB was negatively correlated with length of the whales (p < 0.01). Significantly higher concentrations of the three major pollutants (EPCB, EDDT and XHL) were found in mature males as compared to mature females and juveniles of both sexes, while no such relationship was found for EHCH and HCB (Table 2). 3.2. Geographical aspects Sex and maturity were used as covariates during the statistical test, due to the variation of these parameters at different locations. The concentrations of EPCB, EDDT, XHL, XHCH and HCB differed significantly between animals from certain areas. Significantly higher pollutant levels were found in the southernmost area, Lofoten/VesterHlen, compared to the other four locations (XPCB; p < 0.02) and Finnmark and Kola (XDDT; p < O.OS), while the blubber levels of XHL were significantly higher at Spitsbergen compared to those at Kola and Finnmark (~~0.02). Intermediate levels of XDDT were found at Spitsbergen and Bear Island, with the highest concentrations in the Bear Island area. Significantly higher CHCH levels were detected in animals from Lofoten/Vesterblen and Bear Island compared to the three other locations (p < 0.01). Lowest ‘CHCH levels were found in whales from the coast of Finnmark and Kola. HCB was significantly lower in Finnmark compared to the other four locations (p < 0.04). The highest concentrations were detected at the northernmost location, Spitsbergen. A strong intercorrelation between the three major pollutants EPCB, CDDT and XHL, and the minor pollutants XHCH and HCB, was found (Table 3).
3.3. OC pattern and ratios The PCB congeners 101, 99, 110, 149, 118, 153, 105, 138, 187, 128, 180 and 170 were detected in all the animals, while PCB nos 156 and 194, and PCB nos 66 and 157 were detected in > 90% and > 70% of all the animals, respectively. The higher chlorinated PCBs (nos
Table 3 Correlation matrix of the blubber levels of CPCB, CDDT, CCHL, CHCH and HCB in minke whales (Balaenoptera acutorostrata) from northeast Atlantic waters
XPCB EDDT XHL CHCH HCB
XPCB
CDDT
CCHL
XHCH
HCB
1.oooo
0.9314 1.0000 0.9206 0.5556 0.6122
0.8667 0.9206 1.oOOo 0.6666 0.7336
0.4766 0.5556 0.6666 1.0000 0.7233
0.4909 0.6122 0.7336 0.7233 1.0000
0.9314 0.8667 0.4766 0.4909
XPCB, sum of concentrations of 18 PCB congeners; CDDT, sum of concentrations ofp,p’-DDT, p,p’-DDE, p,p’-DDD, o,p’-DDT and og’DDD; XHL, oxychlordane, trans-chlordane, cis-chlordane, transnonachlor, ci.s-nonachlor; XHCH, 7-HCH, a-HCH, B-HCH; HCB, hexachlorobenzene.
206 and 209) were detected in less than 40% of the whales. The major PCB congeners 153, 128, 138, 118, 180, 99 and 149 constituted 21.7%, 18.7%, 16.7%, 8.1%, 6.8%, 5.4% and 4.9% of CPCB, respectively. The PCB pattern in different sex and age groups is shown in Fig. 2. The overall mean ratio CDDT:CPCB in northeast Atlantic minke whales was 0.68 f 0.17, while the ratios DDE:EDDT and DDE:EPCB were 0.42 f 0.12 and 0.28 f 0.10, respectively. The major DDT compound was p,p’-DDE constituting 42.4~t 12.0% of XDDT. The other DDT components oq’-DDD, p,p’-DDD, o,p’-DDT and p,p’-DDT constituted 4.0* 1.3%, 17.5&4.0%, 13.0*4.3%, and 23.2+4.6% of XDDT, respectively. Of the HCH isomers, the a-HCH, P-HCH and y-HCH constituted 41.8* 12.0%, 41.6* 10.7% and 16.6*6.3%, respectively. The major chlordane component was transnonachlor constituting 49.8 & 6.1% of XHL, while cis-nonachlor, cis-chlordane and oxychlordane constituted 19.6*2.3%, 17.4&2.0%, and 9.7&2.4% of XHL, respectively.
4. Discussion 4.1. Ecological aspects In mammals, exposure to organochlorines is exclusively connected to dietary contamination. Top predator species of marine food webs accumulate high levels of these lipophilic and persistent chemicals (Skaare et al., 1990; Muir et al., 1992; Norheim et al., 1992; Tatsukawa, 1992; Kleivane et al., 1996; Bernhoft et al., 1997). Recent ecological studies indicate that the northeast Atlantic minke whale is an opportunistic top predator that feeds on regionally abundant prey. Counter to previous findings in the area of Spitsbergen and Bear Island in 1950 and 1989 (Jonsgbrd, 1982; Nordray and Blix, 1992), the minke whale diet in the 1992 season was dominated by fish, while the dietary contribution of
L. Kleivane, J.U. SkaarelEnvironmental Pollution 101 (1998) 231-239
PCB-209
and summer feeding areas at higher latitudes. In this context, the exposure to pollutants is mainly through feeding in highly productive waters at higher latitudes. Counter to the euryphagous nature of northeast Atlantic minke whales, Antarctic minke whales show a rather stenophagous krill-eating behaviour (Ichii and Kato, 1991). Tanabe et al. (1986) conclude that immature southern minke whales carried higher concentration ratios of DDEs to PCBs in their tissues than mature specimens, due to different feeding strategies. Thus, immature minke whales remain at lower latitudes during the summer and feed not only on euphausiids, but also on copepods and fish, whereas adult individuals migrate to higher latitudes and base their diet solely on less polluted euphausiids (Tanabe et al., 1986). However, during extensive studies of feeding behaviour of minke whales in northeast Atlantic waters (Haug et al., 1996) no similarities to the age-dependent feeding strategy of southern minke whales were found in the northeast Atlantic minke whale stock.
El AdF
I PCB-205
?? AdM
PCB-194
?? JuF JuM
a
PCB-170 PCB-180 PCB-157
235
Ii
4.2. Biological aspects 4.2.1.
0
20
40
60
80
100
120
140
Percentage of PCB 153 Fig. 2. Comparison of polychlorinated biphenyl (PCB) congener pattern of sum of concentrations of 18 PCB congeners (EPCB) in immature and mature minke whales (Ealaenoptera acutorostrata) of both sexes, caught in July and August in 1992. Data are presented as relative values to PCB 153, with SD. ‘Significantly higher ratio in mature females (AdF) compared to mature males (AdM). *Significantly higher ratio in AdM compared to mature AdF. %ignificantly lower ratio in female juveniles (JuF) compared to AdM. 4Significantly lower ratio in JuF compared to AdF.
planktonic crustaceans was very small (Haug et al., 1995). Variations in prey availability may have impact on the feeding habits and, possibly, on the migratory behaviour of northeast Atlantic minke whales (Haug et al., 1996). At present, no conclusive information on the migratory pattern of this whale species in north Atlantic waters is available. However, it is thought that the northeast Atlantic minke whale stock migrate seasonally between winter breeding areas at lower latitudes
Sex and age
The role of migration patterns in dietary OC exposure of various age- and sex-groups of northeast Atlantic minke whales is unclear. Although significant differences in the ratios of certain PCB congeners were found between different groups, no overall pattern of difference between sexes or age groups was found. When comparing different whale groups, there was a sexrelated difference in concentrations of PCB, DDT and chlordane in mature animals. Thus, a twofold concentration of these xenobiotics were found in males compared to females. This is comparable with similar studies on mature southern hemisphere minke whales (Tanabe et al., 1986) and is attributed to the OC transfer from females during gestation and lactation to the offspring, common in most marine mammal species (Tanabe et al., 1982; Aguilar et al., 1995; Espeland et al., 1997). In mature southern minke whales feeding only on euphausiids, sexes are probably equally exposed to OCs, while the minke whale diet in the northern hemisphere varies between different geographical areas, seasons, and years (Haug et al., 1996), and mature animals may have different feeding regimes and thus different OCs exposure. The data on minke whale prey indicate a considerable heterogeneity in the diet considering different years, seasons and different geographical areas (JonsgHrd, 1982; Nordoy and Blix, 1992; Haug et al., 1996). The present levels and patterns of OCs may reflect a cumulative exposure to these contaminants in different areas through seasons in a longlived animal like the minke whale, rather than actual geographical differences. However, it is interesting to note that both low and high OC contaminated minke
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237
L. Kleivane. J.U. SkaarejEnvironmental Pollution 101 (1998) 231-239
pattern of minke whales resembles more that of a pinniped species than that corresponding to odontocete cetaceans (Kleivane et al., 1995; Table 4). The harp seal (Phocu groenlandica), which inhabits and feeds in the northern part of the feeding areas of the northeast Atlantic minke whale stock, is an opportunistic predator (Nilssen et al., 1994), and therefore resembles the minke whale more than the more coastal harbour porpoise (Phocoena phocoena), which feeds entirely on fish species (Aarefjord et al., 1995). A review by O’Shea and Brownell (1994) shows that few studies have determined organochlorine contaminants in representative samples of different baleen whale species inhabiting north Atlantic waters. Only larger sample sizes of sei and fin whales (Borrell and Aguilar, 1987; Borrell, 1993), and north Atlantic right whales (Eubuluenu glacialis) (Woodley et al., 1991) have been obtained to characterize organochlorine contaminants on a species level. In addition, a recent study (Gauthier et al., 1997) reports organochlorine data in blubber biopsies from fin (B. physulus), blue (Buluenopteru musculus) and humpback (Megupteru novueungliue) whales summering in the Gulf of St. Lawrence. The low organochlorine contamination in baleen whales relative to other marine mammal species is a general trend. However, baleen whales, odontocete cetaceans, and pinnipeds are not a biologically homogeneous group. Parameters like age, sex, nutritional status, health status, life span, size and metabolic rates may, in addition to diet, influence the level and pattern of OCs in these species (Aguilar et al., 1995; Skaare, 1995) Considerable differences may also exist in the xenobiotic metabolization capacity of these phylogenetically distant species (Tanabe et al., 1988; Norstrom et al., 1992). The PCB congener pattern in mature males of different Arctic and sub-Arctic marine mammal species is shown in Fig. 3. The minke whale xenobiotic metabolizing enzymes of the cytochrome P450 enzyme system were described by Goksoyr (1995). The same author found certain differences in the cytochrome P450 enzymes in minke whales and harp seals. Murk et al. (1994) reported in vitro metabolism of 3,3’, 4,4’-tetrachlorbiphenyl in harbour porpoise, however, no relevant information is available on the ability of this species to metabolise PCBs with adjacent nonchlorinated metu and puru positions. Thus, interspecies differences in xenobiotic metabolizing enzyme systems may explain some of the differences in OC contamination levels found between minke whale, harp seal and harbour porpoise. Aguilar (1984, 1988) indicates the possibility of comparing ratios of various chemicals to differentiate between offshore and inshore populations of the same species, interspecies contamination and the distance from pollution sources. When comparing the ratios CDDT:ZPCB and DDE:XDDT in adult males of the
?? minke whale ?? harbour porpoise harp seal
0
20
40
M)
80
104
Percentage of PCB 153 Fig. 3. Comparison of PCB congener pattern in males of three marine mammals, the minke whale (Balaenoptera acutorostrata), the harbour porpoise (Phocoena phocoena) and the harp seal (Phoca groenlandica) inhabiting entirely or partly Arctic or sub-Arctic waters. Data are presented as relative values to PCB 153, with standard deviation. ‘Significantly higher ratio in the minke whale compared to harbour porpoise and harp seal. *Significantly higher ratio in the harbour porpoise compared to minke whale and harp seal. ‘Significantly decreasing ratios from minke whale to harp seal to harbour porpoise. 4Significantly decreasing ratios from harbour porpoise to minke whale to harp seal.
three above species, certain similarities and differences were found. In minke whale, harbour porpoise and harp seal, similar ratios EDDT:EPCB were found (0.70,0.71 and 0.73, respectively). In minke whale, harbour porpoise and harp seal, the ratios DDE:XDDT were 0.38, 0.41 and 0.84, respectively. This indicates a proportionally higher concentration of DDE to XDDT in the Barents Sea harp seal population than the more coastal harbour porpoise and the migrating minke whale, which may reflect a past exposure to DDTs.
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Acknowledgements The present study was financially supported by the Norwegian Research Council under the Norwegian Marine Mammal Research Program 1989-1994. The authors acknowledge Oskar Espeland, Erna Stai and Anuschka Polder for performing the OC analyses, and Tore Schweder for statistical advice. We would also like to thank the scientists and the whalers participating in the scientific captures in 1992, Ivar Christensen at the Institute of Marine Research and Tore Haug at the Norwegian Institute of Fisheries and Aquaculture.
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