Mercury and organochlorines in four sperm whales stranded on the Belgian coast, November 1994

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1 BULLETIN DE L'INST!TUT ROYAL DES SCIENCES NATURELLES DE BELGIQUE BIOLOGIE, 67-SUPPL.: 69-73, 1997 BULLETIN VAN HET KONINKLIJK BELGISCH INSTITUUT VOOR NATUURWETENSCHAPPEN BIOLOGIE, 67-SUPPL.: 69-73, 1997 Mercury and organochlorines in four sperm whales stranded on the Belgian coast, November 1994 by Claude R. JOIRIS, Ludo HOLSBEEK, Michele BOSSICART & German TAPIA Abstract Four sperm whales (three subadult males stranded on the Belgian coast, a fourth older male found dead at sea) were analysed for total mercury, methylmercury and organochlorines. All four were part of a total of 24 sperm whales that stranded on the North Sea coasts over a period of six months, a highly unusual phenomenon. Total mercury levels ranged from 0.5!Jglg fw in kidney and 1 in muscle, up to 15 in liver. The finding of at least 90% of the mercury in its inorganic form confirms the existence of detoxification mechanisms in the liver of cetaceans. PCB concentrations in muscle, liver, kidney and blubber ranged from 10 to 25!Jg/g lipids. These results are in the same order of magnitude as literature data, which however does not imply that there is no impact on the populations. Social affiliation with a particular adult bull rather than a direct effect of pollutants may have been the primary cause of the stranding of the three younger animals: they apparently remained close to the older one (the leader?) dead at sea, and stranded in very shallow water. Indirect impact of anthropogenic pollutants influencing the behaviour and/or the health of a social cluster is one plausible hypothesis to explain why a large number of sperm whales got trapped in the North Sea, but limited data available on the large bull fail to support this. Keywords: sperm whale, stranding, mercury, organochlorines, detoxification, social behaviour. Quatre cachalots (trois males sub-adultes echoues a la cote beige et un quatrieme male plus age trouve mort en mer) ont fait l'objet d'analyses de mercure total, de methyl-mercure et d'organochlores. Les quatre animaux faisaient partie d'un ensemble des 24 cachalots qui s'echouerent sur les cotes de la mer du Nord sur une periode de six mois, un phenomene tres inhabituel. Les niveaux de mercure total variaient de 0.5!Jg/g (poids frais) dans le rein et 1 dans le muscle jusqu'a 15 dans le foie. Le fait d'avoir trouve au moins 90% du mercure sous sa forme inorganique confirme!'existence de mecanismes de detoxication dans le foie des cetaces. Les concentrations en PCB dans le muscle, le foie, le rein et le lard variaient de 10 a 251Jg/g lipides. Ces resultats sont du meme ordre de grandeur que les donnees foumies par la litterature, ce qui n'implique pas toutefois qu 'il n'y ait pas d'impact sur les populations. Plutot qu'un effet direct a attribuer aux polluants I 'attachement social a un male adulte particulier peut avoir ete la cause premiere de l'echouage des trois animaux plus jeunes: apparemment, ils resterent a proximite du plus age (le leader?) qui eta it mort en mer et s' echouerent dans des eaux tres peu profondes. L'effet indirect de polluants anthropogenes influenyant le comportement et!ou la sante d'un groupe social constitue une hypothese plausible pour expliquer pourquoi un grand nombre de cachalots se retrouverent pieges en mer du Nord, mais les quelques donnees disponibles provenant du grand male ne viennent pas a l'appui de cette hypothese. Mots-cles: cachalot, echouage, mercure, organochlores, detoxication, comportement social. Introduction In the early morning of November 18th, 1994, three sperm whales Physeter macrocephalus were found stranded in close proximity to one another on the western part of the Belgian coast near the town of Koksijde. All three were young males between 14.5 and 15.5 m in length, corresponding to an estimated age of 20 to 30 years (MARTIN, 1980). The same day, a fourth and much larger animal (#4, 18 m, estimated age 55+ years) was found dead at sea not far from the shore at the town of Nieuwpoort; he was towed to land for further study. The general state of the older animal (#4) clearly indicated that he must have been dead at sea for at least one day; its dangerous state of decay did not allow a full autopsy nor ecotoxicological sampling. The other three sperm whales evidently stranded alive but were dead when found the same morning. Recent strandings and mortalities in the North Sea of in total 24 sperm whales over a period of six months (1 in the UK, 1 in the Netherlands, I in Germany, 3 dead at sea in Norway, 4 in Belgium, 11 in the Orkney Islands UK, and 3 in the Netherlands) raise questions about the health status and prospects of the sperm whale populations. In particular we found heavy metals and organochlorine residues that are at least suspect as having a negative impact on the animals. Analyses for total and organic mercury content as well as for PCBs and a series of organochlorine pesticides were performed on muscle, liver, kidney and blubber tissue as avail.able; comparison of our results with complementary data for selenium, metallothioneins, cadmium, lead, copper, chromium and zinc (BOUQUEGNEAU et al., this volume) on the one hand, and the results from anatomopathology (JAUNIAUX et al., this volume) on the other hand, allowed us to draw up general conclusions about the health status of the animals involved. Finally, we tried to answer whether or not the levels of stable

2 70 Claude R. JOIRIS, et al. pollutants found might have had any influence, directly or indirectly, on the death of the animals, and in the mortality of sperm whales in the North Sea area during the winter of 1994/95. Methods Total mercury was analysed using specific Atomic Absorption Spectrometry performed on a Perkin-Elmer MAS-50 Mercury analyser: samples were mineralised at 200 C with sulphuric acid (H2S04l and oxidized by adding hydrogen peroxide (H20 2). A few drops of potassium permanganate (KMn0 4) were added to determine that the oxidation was complete, excess KMn04 being removed by addition of hydroxylammonium chloride (HONH 3Cl). The solution was then transferred to a reaction vessel where mercury was reduced with stannous chloride (SnC1 2) to Hg 0 vapour. Methylmercury was measured by ECD-gas chromatography with a 0.75 ID Supelco SP-1000 column on a Packard 437 chromatographer (isotherm 120, injector 200, detector 250 ). Copper sulphate (CuS04), sodium bromide (NaBr) solution and toluene were added to the dried homogenate samples. The aqueous and non-aqueous (toluene) layers were mixed. After centrifugation, 51 6th of the toluene was removed and set aside, and the extraction was repeated on what remained. Methyl mercury was extracted from the toluene by addition of a solution ofna 2S 20 3 which forms a specific thiol-methyl mercuric complex. The mercury containing complex was drawn back into a fresh toluene phase for chromatography by addition of NaBr. PCBs and organochlorine pesticide concentrations Fig. 1 -,.. ~ ""r.. a:r~ ~ : ~,..., "" So C!: (!;) (t, C!: os: Chromatograph pattern for organic mercury analysis: double injection 1 J..!l. I~. I. ~ Fig. 2 - Chromatograph for PCB analysis: blubber sperm whale #1 (A) and reference Aroclor 1260 (600 pg/ J..!l, B). were determined by ECD-gas chromatography using a capillary CP-Sil 4 column on a Shimadzu 14-A chromatographer: carrier gas N2, temperature programme from 60 to 270, injection T 270, detector T 300 after an hexane extraction and a florisil clean-up. Results and discussion Concentrations of mercury, total PCB and DDE are given in Table 1. Concentration of total mercury ranged from 0.5 J..lglg fw in kidney up to 15 in liver. The organic mercury fraction (methylmercury) represented on average 6% in liver, 21% in kidney and 76% in muscle, probably reflecting the existence of a slow detoxifying mechanisms for methylmercury transported to the liver (KOEMAN et al., 1975; MARTOJA and VIALE, 1977; MAR TOJA and BERRY, 1980; CAPELLI et al., 1989; CARLINI and FABBRI, 1989; WAGEMAN et al., 1981; HANSEN et al., 1990; JOIRIS et al., 1991; PALUDAN-MULLER et al., 1993). The importance of age has been frequently established where it concerns stable pollutants in marine mammals (FALCONER et al., 1980; SUBRAMANIAN et al., 1988; ltano and KAWAI, 1981; JOIRIS et al., 1991). Even so, we found no obviously higher concentrations in the older whale. Main differences to be expected, however, could have been at the level of the liver, since this tissue reacts more quickly to acute contamination or remobilisation of residues accumulated in lipids. Data for total PCB concentration (calculated on the basis of Aroclor 1260 standard mixture) ranged from 0.3 J..tg/g fw in muscle and liver up to 13 for blubber. Expressed on a lipid weight basis, all but one tissue had concentrations exceeding 10 J..tg/g. DDE concentration :s':5

3 Mercury and organochlorines in four sperm whales 71 Table 1 - Concentrations of total mercury and methylmercury (both in 1-1g/g fw), percentage ofmethylmercury, and concentrations of total PCB (LPCB compared to Arochlor 1260) and DDE (both expressed as 1-1g/g fw and 1-1g/g lw) in muscle (M), liver (L), kidney (K) and blubber (BI). Data to be published in HOLSBEEK et al., 1998 (submitted). Sperm Whale Nr. 1 Tissue M L K Bl Total Hg 1-lg/g fw MeHg 1-1g/g fw %MeHg % LPCB (1260) 1-1g/g fw DDE 1-1g/g fw LPCB (1260) 1-1g/g lw DDE 1-1g/g lw M L K Bl M L M Bl never exceeded 7 1-lg/g lw., Aldrin and Heptaclor were below the detection limit of lg/g lw. The results not only show high concentrations of organochlorines and mercury, they also indicate a very high total load if we consider that e.g. 30 to 40% of the body weight consists of blubber, an equal amount of muscle. Based on this assumption, the total burden for each sperm whale can be roughly estimated at 150 g PCBs, 15 g Hg, 20 g DDE, 7 g Cd and 7 g Pb. This implies that each animal represents a load of at least 200 g of stable pollutants. This fact has implications for the disposal of carcasses. A comparison with literature data is difficult to make, not only because data are not abundant, but also because different units are used. However, our data correspond with the levels mentioned in recent literature (Table 2). The fact that the levels of organochlorine compounds we found do not exceed levels described in published data does not imply lack of effect. Comparable organochlorine levels were found to cause, or at least were suspected to have caused, reproductive and immune-deficiency problems in marine mammals (HELLE et a{, 1976; SUBRA MANJAN et al., 1987; ADDISON, 1989; S!MMONDS et al., 1993; DEGUISE et al., 1994; TANABE et al., 1994; KUEHL and HAEBLER, 1995). An overall comparison with the results for other heavy metals showed elevated levels for PCBs and non-detoxified cadmium, while on the other hand mercury was detoxified and bound to selenium (BOUQUEGNEAU et al., this volume). All four sperm whales were concluded to be in poor health conditions, on the basis of total weight and blubber thickness. Conclusions It cannot be excluded, but it seems unlikely that the recent strandings and mortalities in the North Sea of in total 24 Table 2 - Selected literature data on Hg, PCBs and DDE concentration in sperm whale muscle (M), Liver (L), kidney (K) and blubber (Bl) (n: number of samples). n M L K Bl Unit Origin Reference LHg I lg/g fw France Medit. THIBAUD & DuGUY 1973 LHg g/g fw Belgium JOIRIS et a/., 1991 LPCB g/g lw France At!. ALZIEU & DUGUY, 1979 LPCB g/g lw Spain At!. AGUILAR, g/g lw id. id. LPCB g/g Iw Iceland BORRELL, 1993 pp'dde g/g lw Spain At!. AGU!LAR, g/g lw id. id. pp'dde g/g Iw Iceland BORRELL, 1993 pp'dde g/g fw California WOLMAN & WILSON, 1970 pp'dde g/g fw South Africa HENRY & BEST, 1983

4 72 Claude R. JOIRIS, et al. sperm whales over a period of six months were purely accidental. A comparison of the results obtained by the three participating teams on pathology and toxicology suggests that social behaviour, more specifically the fact that the three younger bulls probably stayed with the dead older one, led to their own stranding and death after being trapped in shallow water by tidal movements. Elevated concentrations for Hg, PCBs or Cd are most probably not the direct reason for the stranding or death of the four Belgian sperm whales. On a larger, North Sea scale, it is as unlikely that pollution would be the direct cause for the stranding or death of 24 sperm whales. If the North Atlantic sperm whale population was affected directly by actual levels of stable pollutants, other mortalities on other locations whould already have confirmed this hypothesis. This is clearly not the case. Nevertheless, this does not imply that contaminant levels could not have indirectly affected the behaviour and/or the health of some of the members of a larger social group, causing the stranding of the rest. This hypothesis implies that all four were members of the same social group, probably even part of a larger bachelor group. It seems indeed unlikely that within the same year, several sperm whales would die of old age- at sea- in the North Sea area. The fact that all four sperm whales were in poor health condition: lesions, ulcers, a low body weight and high concentrations of stable pollutants cannot be overlooked. The most interesting question of the death at sea of the older individual, however, is not (yet) resolved, due to incomplete sampling. Acknowledgments This study was conducted as part of the contract on 'Pathology and Ecotoxicology of seabirds and marine mammals in the North Sea and adjacent areas', funded by the Belgian Federal Office for Scientific, Technical and Cultural Affairs. Literature ADDISON, R. F., Organochlorines and marine mammal reproduction. Can. J Fish. Aquat. Sci., 46: AGUILAR, A., Organochlorine pollution in sperm whales, Physeter macrocephalus, from the temperate waters of the Eastern North Atlantic. Mar. Poll. Bull., 14: ALZIEU, C. and DuGUY, R., Teneurs en composes organochlores chez les cetaces et les pinnipedes frequentant les cotes fran<;aises. Oceanol. Acta, 2: BORRELL, A., PCB and DOTs in blubber of cetaceans from the Northeastern North Atlantic. Mar. Poll. Bull., 26: CAPELLI, R., DE PELLEGRINI, R., MINGANTI, V., and POGGI, R., Preliminary results on the presence of inorganic, organic mercury and selenium in dolphins (Stenella coeruleoalba) from the Ligurian Sea. 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Env., 3: KUEHL, D.W. and HAEBLER, R., Organochlorine, organobromide, metal and selenium residues in bottlenose dolphins (Tursiops truncatus) collected during an unusual mortality event in the Gulf of Mexico, Arch. Environ. Contam. Toxicol., 28: MARTIN, A.R., An examination of sperm whale age and length data from the Icelandic catch. IWC, SC/31/Doc 16: MARTOJA, R. and VIALE, D., Accumulaton de granules de selenium mercurique dans le foie d'odontocetes: un mecanisme possible de detoxication du methylmercure par le selenium. C. R. A cad. Sci. Paris, 285: MARTOJA, R. and BERRY, J.-P., Identification of tiemannite as a probable product of demethylation of Hg by selenium in cetaceans. A complement to the scheme of the biological cycle of Hg. Vie Milieu, 30: PALUDAN-MULLER, P., AGGER, C.T., DIETZ, R. and KINZE, C.C., Mercury, cadmium, zinc, copper and selenium in harbour porpoise (Phocoena phocoena) from West Greenland. 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5 Mercury and organochlorines in four sperm whales 73 SUBRAMANIAN, A.N., TANABE, S. and TATSUKAWA, R., Use of organochlorines as chemichal tracers in determining some reproductive parameters in Da11's porpoise Phoconoides dalli. Mar. Environ. Res., 25: TANABE, S., IWATA, H. and TATSUKAWA, R., Global contamination by persistent organochlorines and their ecotoxicological impact on marine mammals. Sci. Tot. Environ., 154: THIBAUD, Y. and DuGUY, R., Teneur de mercure chez les cetaces des cotes de France. ICES report C.M. 1973/N: 2. WAGEMANN, R, SNow, N.B., LUTz, A. and ScoTT, P., Heavy metals in tissues and organs of the narwhal (Monodon monoceros). Can. J Fish. Aq. Sci., 40, Suppl. 2, N 2. WoLMAN, A. and WILSON, A., Occurrence of pesticides in whales. Pest. Mon. J., 4: Claude R. JOIRIS, Ludo HOLSBEEK, Michele BossiCART & German T APIA Laboratory for Ecotoxicology & Polar Ecology Free University Brussels VUB Pleinlaan 2 B-1050 Brussels, Belgium