Heterogeneous distribution of organochlorine contaminants in the blubber of baleen whales: implications for sampling procedures

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Heterogeneous distribution of organochlorine contaminants in the blubber of baleen whales: implications for sampling procedures
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  Marine Environmental Research 31 (1991) 275 286 Heterogeneous Distribution of Organochiorine Contaminants in the Blubber of Baleen Whales: Implications for Sampling Procedures Alex Aguilar & Assumpci6 Borrell Department of Animal Biology (Vertebrates), Faculty of Biology, University of Barcelona, 08071 Barcelona, Spain (Received 13 April 1990; revised version received and accepted 16 May 1991) A BSTRA CT The concentration o[ DDTs and PCBs n'as determined #l two strata (imzer and outer) o['the blubber offin and sei whales.,fi'om the eastern North Atlantic. hi the two species residue levels qf all organochlorines in the outer layer were sign(fieantO~ higher than in the inner one. The DDE/'tDDTratio ~fidnot show signOqeant variation between strata, but the tDDT/PCB ratio was higher in the outer layer than in the inner one. Such d(fferences between strata cannot he explained by variation in the quantiO' q[ lipids present in the blubber and probab O' indicate a constant organochlorine distribution pattern in the blubber ¢)[ arge whales. The differential role of the blubber strata hz the [~tttening cycle, the heterogeneous lipid composition of blubber throughout its depth and the d_ifferent turnover rates qf pollutants in the layers are the probable factors responsible Jor these observed d(fferences in pollutant distribution between blubber strata. Because ~[ this heterogeneous distribution, blubber samples collected from cetaceans for pollutant anah'ses should include equal representation qf all layers in order to be representative o[the individual's pollutant load. This is especially hnportant when sampling stranded specimens or taking hiopo' samples from largeJree-ranging whales. INTRODUCTION Blubber is a hypodermic tissue which covers the body of cetaceans and serves as an energy reserve deposit and insulating cover. In large whales it reaches a thickness of several centimetres and represents about 20-40% of their total body weight (Lockyer, 1976). The most important biochemical 275 Marine Environ. Res 0141-1136/91/$03.50 (~ 1991 Elsevier Science Publishers Ltd, England. Printed in Great Britain.  276 Alex Aguilar, Assumpci~'~ Borrell constituents of blubber are lipids, which typically represent about 30-80% of the tissue's wet weight (Ackman et al., 1975; Lockyer et al., 1984; Aguilar & Borrell, 1990). Because of its large contribution to the cetacean's body mass and high lipid content blubber carries most of the load of lipophilic pollutants (such as organochlorines) present in the bodies of large whales. Therefore blubber is the tissue most commonly used for monitoring organochlorine residue levels in cetaceans (Wagemann & Muir, 1984). However, the blubber of large whales is not a homogeneous tissue throughout its depth but is composed of layers or strata with different roles and biochemical composition (Ackman et al., 1965, 1975: Lockyer et al., 1984). The inner layers are mostly devoted to fat storage, and their lipid content fluctuates greatly following the individual's reproductive and migratory cycle. The outer layers, however, have an insulation function and are little affected by changes in the nutritive condition. As a conse- quence of the differing roles of the strata, the lipid content decreases from the outermost layers to the innermost, the intensity of the gradient depending on the nutritive condition o1 each individual. Thus, in fat, pregnant females, no difference between the strata is usually observed, and the decreasing trend is nonexistent or even reversed. In whales of an intermediate body condition, e.g. most males or immature females, the gradient is almost always apparent, although the difference between strata is not very great. Finally, in lean females, typically those lactating or post- lactating, the gradient is great, and the inner layers contain only about 20% of the lipid present in the outermost external ones (Aguilar & Borrell, 1990l. Because distribution, metabolism and mobilization of organochlorines are closely linked to those oflipids it has been proposed that organochlorine concentrations may not be uniform in all strata and locations of the blubber in a given animal, even if concentrations are calculated on the basis of the lipid content of the tissue (Aguilar, 1985). A heterogeneous distribution of organochlorines in the blubber strata would have strong implications for the sampling methodology of whales because, given the great thickness that this tissue reaches in some large species, all blubber layers are not usually contained in the piece of tissue excised and analysed for the study. This problem is especially important when samples of the superficial layers of the blubber are collected from free-ranging individuals using a biopsy dart, a technique which has become common in the past few years (Winn et al., 1973: Aguilar & Nadal, 1984; Lambertsen, 1987; Mathews et al., 1988). In the present study the authors analysed the concentrations of DDTs and PCBs, the two groups of organochlorine compounds most widely found in cetaceans, in different strata of dorsal blubber from fin (Balaenoptera physalus) and sei (Balaenoptera borealis) whales and examined their variation pattern between layers.  D&tribution q]organochlor&es & whale blubber 277 Fin whale males Fin whale females Sei whale males Sei whale females TABLE Biological Information from the Whales Analysed N Body length (m) Age {years) x + SD .v 4__ SD 30 18'7_+0'9 18'5_+ 17"4 59 19"3_+ 1"1 12"1 -+ 8"9 10 13"2_+0'8 14"3_+7'2 13 13"7--+ 1"2 12"0_+5:0 MATERIAL Large pieces of dorsal blubber were obtained from whales caught off Spain and Iceland by commercial fishing operations. These were collected during flensing procedures, about 15-24h after the death of the animal, and contained the whole blubber depth, including the skin and some of the adjacent basal muscle. All samples were taken from the dorsal region posterior to the dorsal fin. This location was chosen because it is the one typically selected for sampling stranded specimens (Anon., 1985), as well as the one most easily accessible from a vessel during sampling by means of a biopsy dart. In total, samples were obtained from 89 fin whales (30 males and 59 females) caught offSpain in 1984 and from 23 sei whales (10 males and 13 females) caught off Iceland in 1985. Because whaling regulations prevent catching whales of small size the sample was composed almost only of adult individuals. Biological information from the specimens analysed tbr the study is shown in Table 1. From the srcinal piece of blubber excised, small pieces (about 2 3 g) were drawn from the outer (external) and inner (internal) regions of each sample, and processed independently. METHODS Whales were measured and sexed at the flensing platform by experienced people. Age was determined by counting growth layers in the core of the whale's ear plugs following standard procedures (Lockyer, 1984). Samples for organochlorine determination were wrapped in aluminium foil and kept in deep freeze until analysis. For lipid extraction the pieces of blubber were ground with anhydrous sodium sulphate in a mortar, and the mixture extracted with n-hexane for 4 h in a Soxhlet apparatus. The extract was then concentrated to 40ml, from which a 10-ml subsample to determine  278 Alex Aguilar, Assumpci~'~ Borrell tissue fat content was taken. An aliquot of the remaining extract containing 1 g of lipid was mixed with sulphuric acid for the clean-up following the procedures described by Murphy (1972). After centrifugation and phase separation, the lipid-free extract was concentrated to 1 ml and injected into a Perkin Elmer Sigma 3B gas chromatograph (injector temperature 250~C), equipped with an electron- capture detector of 63Ni (temperature 350~C), and a Perkin-Elmer Sigma 15 computing integrator. A fused-silica capillary column of 0-25 mm internal diameter, 60 m length, and a stationary phase SPB- 1 with a film thickness of 0.25/~m was used. Pure nitrogen at a flow rate of I ml/min was used as carrier gas. Temperature was programmed according to the following sequence: injection at 40°C; oven steady for the first 2 rain and then an increase from 40 to 160cC at a rate of 2YC/min; oven maintained at steady temperature for 1 rain and then an increase from 160 to 250°C at a rate of 2°C/min. From this point until the end of the analytical run the column remained isothermal at a temperature of 250~C. Heptachlor was used as an internal standard to calibrate fluctuations in the operational conditions. The identity of the DDT compounds was confirmed by an alkali conversion to their respective olefins and re-analysis by GLC. PCBs were identified and quantified by their peak characteristics and retention times in relation to a 1:1 standard mixture of Aroclors 1254 and 1260, and confirmed by their resistance to the chemical derivations detailed above. Eight replicates of samples fortified with standards gave the following percentages of recovery for the whole analytical process (mean + coefficient of variation): p,p'-DDE, 72 56% _+ 15'8; p,p'-TDE, 87 41% _+ 8.4; o,p-DDT, 81.91% ± 8 3; p,p'-DDT, 98 13% _+ 7.6; PCB, 90-97% _+ 8.0. Ten replicate chromatographic runs of a mixture of the DDT and PCB standards gave the following coefficients of variation in the quantification: p,p'-DDE, _+7.9%; p,p'-TDE, +6 5%; o,p-DDT, +5-5%; p,p'-DDT, ___8 2%; PCBs (mean of the eight peaks commonly used in the quantification), +8.7%. All the results are expressed in relation to the total lipid content of the tissue sample. Total DDT (tDDT) levels are calculated as the sum of all the DDT forms (p,p'-DDE, p,p'-DDT, o,p'-DDT and p,p'-TDE). RESULTS AND DISCUSSION The levels of DDTs and PCBs found in the outer and inner layers of the blubber from fin and sei whales, according to sex, are detailed in Table 2. As was expected, males displayed higher residues of contaminants than females of the same species, a difference attributable to the transfer process that  TABLE 2 Extractable Lipid Content (ELP) and Organochlorine Concentrations (Mean and Associated Standard Deviations) Found in the Inner and Outer Layers of the Blubber of Baleen Whales and the Level of Significance of the Difference Between Layers According to a t-Test (concentrations are expressed in ltg/kg on an extractable lipid basis) p,p -DDE p,p -TDE o,p'- DD T p,p'- DD T tDD T PCBs ELP Fin whale males Inner 420 ± 290 150 _+ 70 300 ± 180 Outer 580 + 320 210 ± 90 420_+ 230 Significance 0.05 0'01 0.05 180 ± 80 1 040 ± 600 1 430 ± 680 75.3 ± 14.1 270_+ 120 490_+690 l 820± 730 77"4±8-2 0"001 0-02 0"05 NS ~ 100_+ 50 500 _+ 270 770 ± 410 657 ± 21-6 130 ± 70 670 ± 350 880 ± 250 70'4 ± 5"4 0"002 0"01 0-05 NS 120 + 60 670 _+ 390 600 ± 290 15"7 ± 9'8 170 ± 90 970 ± 490 660 + 300 76.2 ± 6"3 0-05 0"05 N S 0"001 Fin whale females Inner 170 ± 100 80_+ 50 150 ± 90 Outer 240_+ 150 110_+ 50 200± 100 Significance 0"01 0-02 0"01 Sei whale males Inner 230+ 150 110± 60 210± 120 Outer 360_+210 140± 70 310± 140 Significance 0.05 NS 0.05 Sei whale females Inner 60 ± 30 40 +_ 20 60 ± 30 Outer 70 ± 50 40 ± 30 60 ± 40 Significance NS NS NS "NS, differences non-significant. 40_+ 30 200_+ 110 210_+90 31.4_+ 19-6 40+30 210+ 150 210+ 130 81.4+8.6 NS NS NS 0.001 ,,,,, 2" 2" b,-)
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