organochlorine residues and heavy metals in kidneys of polecats (mustela putorius) from switzerland

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Bull. Environ. Contain. Toxicol. (1990) 45:689-696 1990 Springer-Verlag New York Inc. Environmental Contamination ~and Toxicology Organochlorine Residues and Heavy Metals in Kidneys of Polecats (Mustela putorius) from Switzerland C. F. Mason 1 and D. Weber 2 1Department of Biology, University of Essex, Colchester C04 3SQ, United Kingdom and 2Hintermann and Weber AG, Hauptstrasse 44, CH-4153 Reinach, Switzerland Polecats (Mustela ~utorius) have declined in Switzerland and other parts o~ro~ sTn~e the middle of this century (Eiberle 1969; Mermod et al. 1983; Libois 1984; Weber 1988). Structural changes of the countryside resulting from modern agriculture, expansion of urban areas, destruction of wetlands and watercourses etc. may have affected polecat populations. However, pollutant burdens in polecats have not been studied, though contamination with organochlorines and heavy metals has been strongly linked with the decline, over the same time scale, of top carnivores such as the otter (Lutra lutra) and several species of raptor (Mason and Macdonald 1986; Newton 1979) in Europe. Polecats in Switzerland are specialized anuran predators, Rana temporaria and Bufo bufo featuring prominently in the diet {Weber 1989a). This semi-aquatic diet may render polecats more vulnerable to biomagnifying pollutants than other carnivores in the country. This paper reports on the concentrations of organochlorine residues and heavy metals (mercury, cadmium and lead) in a collection of polecat kidneys from Switzerland. MATERIALS AND METHODS Polecat carcasses were collected over the period 1983 - 1985 in Switzerland and adjoining areas of France (Weber 1988), where the species occurs in the lowland and the lower regions of the mountains. The most dramatic decline of polecat populations has occurred in the lowland region between the mountain chains of the Jura and the Alps. Human population density in the Swiss lowland is about 800 individuals per km ~. Industry is not only concentrated in the larger urban areas, but also distributed in numerous small towns and villages spread over the whole area. Agriculture in the lowlands is mainly arable farming. Rubbish incinerators are spread over the country and sewage sludge is deposited on arable land. The lower parts of the mountains consist mainly of forests, meadows and pastures. Human population density is low (about 30 persons per km L) *Send reprint requests to C.F. Mason at the above address. 689

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Page 1: Organochlorine residues and heavy metals in kidneys of polecats (Mustela putorius) from Switzerland

Bull. Environ. Contain. Toxicol. (1990) 45:689-696 �9 1990 Springer-Verlag New York Inc.

E n v i r o n m e n t a l C o n t a m i n a t i o n

~and Toxicology

Organochlorine Residues and Heavy Metals in Kidneys of Polecats (Mustela putorius) from Switzerland

C. F. Mason 1 and D. Weber 2

1Department of Biology, University of Essex, Colchester C04 3SQ, United Kingdom and 2Hintermann and Weber AG, Hauptstrasse 44, CH-4153 Reinach, Switzerland

Polecats (Mustela ~utor ius) have declined in Switzerland and other parts o ~ r o ~ sTn~e the middle of th i s century (Eiberle 1969; Mermod et a l . 1983; Libois 1984; Weber 1988). Structural changes of the countryside resul t ing from modern agr icu l tu re , expans ion of urban a r e a s , d e s t r u c t i o n of we t l ands and watercourses e t c . may have a f fec ted polecat popu la t i ons . However, pol lutant burdens in polecats have not been studied, though contamination with organochlorines and heavy metals has been strongly l inked with the decl ine, over the same time scale, of top carnivores such as the o t te r (Lutra lu t ra ) and several species of rap tor (Mason and Macdonald 1986; Newton 1979) in Europe. Po leca t s in S w i t z e r l a n d are s p e c i a l i z e d anuran predators, Rana temporaria and Bufo bufo featur ing prominently in the d ie t {Weber 1989a). This semi-aquat ic d ie t may render polecats more vulnerable to biomagnifying pol lutants than other c a r n i v o r e s in the c o u n t r y . This paper r e p o r t s on the concen t ra t i ons of o rganoch lor ine residues and heavy metals (mercury, cadmium and lead) in a co l lec t ion of polecat kidneys from Switzerland.

MATERIALS AND METHODS

Polecat carcasses were col lected over the period 1983 - 1985 in Switzerland and adjoining areas of France (Weber 1988), where the species occurs in the lowland and the lower regions of the mountains. The most dramatic decline of polecat populations has occurred in the lowland region between the mountain chains of the Jura and the Alps. Human population densi ty in the Swiss lowland i s about 800 i n d i v i d u a l s per km ~. I n d u s t r y i s not on l y concentrated in the larger urban areas, but also d is t r ibu ted in numerous small towns and v i l lages spread over the whole area. Agr icul ture in the lowlands is mainly arable farming. Rubbish inc inerators are spread over the country and sewage sludge is deposi ted on arable land. The lower par ts of the mountains c o n s i s t m a i n l y of f o r e s t s , meadows and p a s t u r e s . Human p o p u l a t i o n d e n s i t y i s low ( a b o u t 30 p e r s o n s per km L)

*Send repr in t requests to C.F. Mason at the above address.

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Page 2: Organochlorine residues and heavy metals in kidneys of polecats (Mustela putorius) from Switzerland

concentrating in the bottom of valleys where industry is also concentrated. The main wind direction is from (south-) west to (north-) east. An overview of chemical pollution in Switzerland is given in Biedermann et a l . (1984).

Detailed information on polecat carcasses is given in Weber (1987, 1988). Most were road casualties. Carcasses were mainly aged by counts of tooth cementum annuli (Weber, 1989b), but in some cases tooth wear and skull ossif ication were used, which sometimes leads to uncertain ageing, only minimum ages being defined.

Kidneys were stored deep frozen in glass vials prior to analysis. Methods of organochlorine analysis largely followed FAO (1983). Tissue was th in ly sliced and weighed. The tissue was stirred in lOml acetone:hexane (35:10) and homogenized. The supernatant was decanted into a sintered glass funnel and the f i l t r a t e was collected into a separating funnel containing 20ml NaCl/phosphate (11.7g NaCl in 11 0.1 M orthophosphoric acid), while sediment was resuspended in two further 10 ml aliquots of hexane:diethyl ether (9:1) and decanted after 5 min. The separating funnel was shaken and the aqueous phase was decanted and re-extracted in hexane. The solvent phase extracts were evaporated at 70~ to dryness and the weight determined. The extract was re-dissolved in toluene and pes t i c i des determined wi th a Carlo-Erba 4300 gas chromatograph, with a t r i t ium electron capture detector and using a capi l lary column. The detection level was O.01mg kg - I .

For the analysis of metals approximately O.5g samples of kidney were digested in 4 ml of a 4:1 (v/v) n i t r i c and perchloric acid mixture. I n i t i a l digestion was at room temperature for 36-48 h, followed by careful heating at a temperature of 40~ for lh, to prevent frothing, after which the temperature was raised to 140~ for a f inal 60-90 min. Samples were then allowed to cool and f ina l solut ions were made up to 10 ml with double d i s t i l l e d water. They were stored cool and analyzed wi th in one week. Total mercury in samples was measured by flameless atomic absorption. Cadmium and lead were measured using a double beam atomic absorption spectrophotometer (AA 1275/ GTA 95) with correction for non atomic absorption by use of a deuterium lamp. A mean of three readings on each sample was recorded and this was within +95% FL. Detection l imi ts were 0.~ ug kg -1 for mercury, 0.001 mg kg -~ for cadmium and 0.005 mg kg -~ for lead.

RESULTS AND DISCUSSION

Kidneys from a total of 80 animals (48 males, 31 females, one undetermined) were analyzed. Thirty-one animals were aged as j u v e n i l e s , 15 as subadul ts and 30 as a d u l t s , wi th 4 of undetermined age. The distr ibut ion of sites from which polecats were obtained is shown in F ig. l . Four additional animals, not shown on the map, came from the Jura of France, immediately to the west of the area shown in Fig.1.

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The resul ts of the analyses are summarized in Table 1. Lindane and DDE were ubiquitous, but at low concentrat ions. Dieldr in was present in only 39% of samples, again at low concen t ra t i ons . Because of the generally small amounts of residues present in the samples, a more detai led s t a t i s t i c a l analysis of organochlorine pest icides was not made.

PCBs (determined against an Aroclor 1260 standard) were presen1~ in al l samples, with a maximum concentration of 120.8 mg kg -~ l i p i d in an adu l t male. The d i s t r i b u t i o n of PCBs, in three concentration ranges, is ~hown in F i g . l . Concentrations of PCBs g r e a t e r than 50 mg kg - - in muscle t i s s u e are known to be associated with reproductive impairment in a related mustelid, the mink (Mustela vison~ (Jensen et a l . 1977) Concentrations g rea te r t h ~ 5"0 mg k-g =" l i p i d occurred in k idney t i s sue of 7 (8.9%) of the polecats, while 12 (14.2%) had concentrations in the range 10-50 mg kg - I l i p i d . The major i ty of polecats with elevated levels of PCBs were from the northeast of the country ( F i g . l ) .

Mean concentrations _qflPCBs~ in males (14.6 mg kg - I l i p i d ) and females (12.2 mg kg ip id ) were not s i g n i f i c a n t l y d i f fe ren t (d = 0.43, P > 0.05). However, s i g n i f i c a n t l y more males (15.9%) than females (6.5%~ had concentrations of PCBs in kidneys greater than 20 mg kg - l i p i d (G = 4 .97 , ~ < 0 . 0 5 ) . The mean concentration in juveni les (9.~6 mg kg -• l i p i d ) was lower tha~ that of subadults (14.89 mg kg- l i p i d ) and adults (16.89 mg kg- l i p i d ) , but the di f ference in mean concentrations between the three age c lasses was not s i g n i f i c a n t (F = 0.71, P > 0 .05 ) . However, 78 of the polecats were accurately aged to month (Weber 1989b). MeanIPCB concentrations in males aged 12 months or over (18.4 mg kg~' ) were h igher than in males less than 12 months (12.1 mg kg - ' ) , but the dif ference was not s i gn i f i can t (t=0.84, P> 0.05). Converselyq mean PCB levels in females aged 12 months or over (4.8 mg kg -~) was three l~imes less than in females younger than 12 months (14.8 mg kg- ' ) , but again the di f ference was not s ign i f i can t ( t = i . 8 , P> 0.05). Mean concentrations in males and females younger than 12 months were not s i g n i f i c a n t l y d i f fe ren t (t=0.37, P> 0.05), but males of 12 months or older had s i g n i f i c a n t l y greater mean PCB concentration than females in the same age group ( t=2 .34 , P< 0 .05) . There was no s i g n i f i c a n t re la t ionsh ip between body weight and PCB concentration in kidneys (r = 0.13, P> 0.05).

Heavy metal concen t ra t i ons were genera l l y low. Mercury was present in a l l samples and cadmium and lead were detected iq the major i ty . The highest concentration of mercury (5.45 mg kg -~ wet we ight ) was from an adu l t female from the nor theast of the c o u n t r y , as were f o u r ou t o f f i v e o t h e r a ~ i m a l s w i t h concen t ra t ions of mercury greater than 2 mg kg -~ wet weigh~. Mean concentrations of me~rcury in kidneys of males (1.05 mg kg -• and females (1.14 mg kg -z) were not s i g n i f i c a n t l y d i f fe ren t (d = 0.31, P > 0.05). The mean concentration of mercury in juveni les (0.76 mg kg -z) was s i g n i f i c a n t l y lower than that of subadults

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Tab le 1. C o n c e n t r a t i o n s (means, ranges ~nd p e r c e n t contaminated) of or~ganochlorine residues (mg kg'" l i p i d ) and heavy metals (mg kg -~wet weight) in kidneys of polecat (n=80).

Compound Mean Range % contaminated

lindane 0.94 .03 - 15.76 100

d ie ld r in 0.32 nd - 1.34 39

DDE 1.40 0.07 - 15.26 100

PCBs 13.50 1.14 120.8 100

mercury 1.04 0.07 - 5.45 i00

cadmium 0.11 nd - 0.36 95

lead 0.42 nd - 5.83 99

(1.16 mg kg -1) and adults (1.33 mg kg -1) (F = 4.37, P < 0.05). cadmium Meaq concentrations of in kidneys of juveni les (0.069 mg

kg'~) were s i g n i f i c a n t l y low~r than those of subadults (0.20 mg kg - I ) and adults (0.14 mg kg")- (F = 10.23, P < 0.001), but there was no re la t ionsh ip between lead concentration and age (F = 0.20, P > 0.05).

The polecat has become res t r i c ted in d i s t r i bu t i on in Switzerland over the last four decades, as i t has over much of continental Europe (Weber 1988). Habitat destruct ion is often c i ted as the primary reason for th i s decl ine, though the precise requirements of the species and how these may be in f luenced by hab i t a t m o d i f i c a t i o n are inadequate ly understood. The e f f e c t s of biomagnifying pol lutants could also be important, for polecats forage extensive ly in wetlands and, in Switzerland, semi-aquatic amphibians are the s tap le food (Weber 1989a). A more severe decline throughout much of Europe in populations of the o t te r (Lutra l u t r a ) , with a more exc lus ive ly aquatic d ie t , has been c T 6 a - r l - y ~ e d to organochlorine contamination (Mason & Macdonald 1986). Switzerland has advanced agr icu l ture in the lowlands and is highly i ndus t r i a l i zed , leading to contamination of aquatic ecosystems. For example, high concentrations of PCBs have been recorded in burbot (Lota lota) in Switzerland (Burgermeister et a l . 1983), l e a d i n g ~ au--u-t-~ors to conclude t ha t the e n t i r e aquatic ecosystem of the country is severely contaminated.

E x p e r i m e n t a l s t u d i e s w i t h mink have shown t h a t impa i r ed reproduction resul ts when females are fed a d iet containing PCB concentrations of 3.3 mg kg - I food, equivalent to a da i ly dose of Img (jansen et a l . 1977). These animals were found to have

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accumulated PCBs to a concentrat ion of 50 mg kg -1 in muscle fa t over a 66 day p e r i o d . O the r s t u d i e s have i n d i c a t e d t h a t r e p r o d u c t i o n in mink is i n h i b i t e d on a d a i l y i n t a k e of 25ug, whi le reproduct ive output was lowered in long-term experiments on a da i l y intake of 2.5ug (den Boer 1983). Experimental work has suggested, however, that fe r re ts (M__ t. P__t" furo) are more res is ten t to the e f fec ts of PCBs than mink, reproduct ion in fe r re ts being prevented ion a da i l y d ie t conta in ing PCBs at a concentrat ion of 20 mg kg -~, a l eve l t h a t was l e t h a l to mink (B leav ins et a l . 1980).

Concentrations of organochlor ine pest ic ide residues in Swiss polecats were low. Mean leve ls were markedly lower, for example, than in a sample of o t te rs from the B r i t i s h Is les (Mason et a l . , 1986a), and were s i m i l a r to l e v e l s in o t t e r s from the Orkney I s l a n d s , o f f no r t he rn Scot land (Mason and Reynolds 1988). Concentrat ions of PCBs were elevated in a number of polecats, the major i t y of them from the northeast of Switzerland ( F i g . l ) close to or downwind of the i n d u s t r i a l region of Zur ich. The current absence of the o t te r from much of i t s former European range is c o r r e l a t e d w i th cen te rs of i n d u s t r y and p r e v a i l i n g winds (Macdonald, in press) .

In view of the experiments on fe r re ts referred to above (Bleavins et a l . , 1980) and the apparent to lerance of f e r r e t s , compared w i t h mink, to PCBs, i t i s d i f f i c u l t to ~ s c e r t a i n whether concentrat ions of PCBs greater than 50 mg kg - I in l i p i d would be associated wi th adverse e f fec ts in w i ld polecats and could in part expla in the decl ine of the species. I t may, however, be s i g n i f i c a n t t h a t o n l y one a n i m a l ou t of seven w i t h PCB concentrat ions greater than 50 mg ~ I in kidney, was more than one year o ld, though animals greater than one year old made up 27% of the sample. Females aged 12 months or over had lower mean concentrat ions of PCBs than younger females, and s i g n i f i c a n t l y lower than males in the same age group. The most l i k e l y reason i s t h a t PCBs are t r a n s f e r r e d to the foe tus v ia the p lacen ta du r ing pregnancy and to the young in m i l k du r ing l a c t a t i o n (Bleavins et a l . 1982).

Concentrat ions of mercury, cadmium and lead were genera l ly low. Mean concentrat ions in polecat kidneys were, for example, much lower than in a sample of o t t e r kidneys from the B r i t i s h Is les (Mason et a l . 1986b) and are u n l i k e l y to be of t o x i c o l o g i c a l s i gn i f i cance . Hanko e t a l . (1970) reported that da i l y intakes of mercury of 5-7 mg kg - I in chicken proved le tha l to f e r r e t s , but such c o n c e n t r a t i o n s are u n l i k e l y ever to be encountered by polecats in the w i ld .

The concentrat ions of organochlor ine pest ic ide residues and heavy metals in t h i s sample of po leca ts from Sw i t ze r l and were low. However, a number of animals had elevated concentrat ions of PCBs, espec ia l l y those close to or downwind of the c i t y of Zur ich. The r e l a t i o n s h i p between PCBs and the d e c l i n e of the po leca t in Switzer land would be worthy of f u r the r study.

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Acknowledgments We thank WWF- Switzerland for f inanc ia l support. The Industr ial and Applied Biology Group, University of Essex, assisted with the analyses.

REFERENCES

Biederman R, Halder U, Kasser U, Kel ler L, Leu D, Martin C, Nierhaus-Wunderwald D (1984) Biozid-Report Schweiz. WWF Schweiz, Zurich, 641pp

Bleavins MR, Aulerich RJ, Ringer RK ( 1 9 8 0 ) Polychlorinated biphenyls (Aroclors 1016 and 1242) : effects on survival and reproduction in mink and ferrets. Arch Environ Contam Toxicol 9:627-635

Bleavins MR, Aulerich RJ, Ringer RK (1982) Placental and mammary transfer of PCBs. In: Lamb DW and Kenaga EE (eds) Avian and Wi ld l i fe Toxicology, Second Conference. American Society for Testing and Materials, Philadelphia, pp 121-131

Boer MH den (1983) Reproduction decl ine of harbour seals : PCBs in the food and the i r effect on mink. Annual Report, Research Ins t i tu te for Nature Management, pp 77-86.

Burgermeister G, Bedrani M, Tarradellas J ( 1983 ) Ut i l i sa t ion de la l o t t e comme i n d i c a t e u r de la p o l l u t i o n des eaux continentales par les polluants organochlores. Eau du Quebec 16:135-143

Eiberle K (1969) Vom l l t i s (Mustela putorius) in der Schweiz. Schweiz. Forstwesen 120:199-207

Food and Agriculture Organization (1983) Manual of methods in aquatic environmental research. Part 9 - Analyses of metals and organochlorines in f ish . FAO Fisheries Tech. Paper 212

Hanko E, Erne K, Wanntorp H, Borg K (1970) Poisoning in ferrets by tissues of alkyl mercury -fed chickens. Acta Vet Scand I I : 268-282

densen S, Kihlstrom dE, Olsson M, Lundberg C, Orberg J (1977) Ef fects of PCB and DDT on mink (Mustela v ison) during the reproductive season. Ambio 6:239

L ibo is RM (1984) Atlas des mammiferes sauvages de Wallonie (su i te) . Le genre Mustela L. en Belgique. Cab Ethol appliquee 4:279-314

Macdonald SM (in press) The status of the o t t e r in Europe. Proceedings of the F i f t h In te rna t iona l O t t e r Colloquium, Hankensbuttel

Mason CF, Ford TC, Last NI (1986a) Organochlorine residues in Br i t i sh ot ters. Bull environ Contam Toxicol 36:656-661

Mason CF, Last NI, Macdonald SM (1986b) Mercury, cadmium and lead in Br i t i sh ot ters. Bull environ Contam Toxicol 37: 844- 849

Mason CF, Macdonald SM (1986) O t t e r s , e c o l o g y and conservation. Cambridge University Press, Cambridge, 236pp

Mason CF, Reynolds P (1988) Organochlorine residues and metals in otters from the Orkney Islands. Mar Pollut Bull 19 : 80-81

Mermod C, Debrot S, Marchesi P, WeberJ-M (1983) Le putois (Mustela p utorius L.) en Suisse romande. Rev Suisse Zool 90: 847-856

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Newton I (1979) Population ecology of raptors. Poyser, Berkhamstead, 432pp

Weber D (1987) Zur Biologie des l l t isses (Mustela putorius L.) und den Ursachen seines Bestandsruckganges in der Schweiz. Dissertation, Universitat Basel, 194pp

Weber D (1988) Die aktuelle Verbreitung des l l t isses (Mustela putorius L.) in der Schweiz. Rev Suisse Zool 95: 1041- 1056

Weber D (1989a) The diet of polecats (Mustela putorius L.) in Switzerland. Z Saugetierkunde 54:157-171

Weber D (1989b) Zur Populationsbiologie schweizerischer l l t i sse (Mustela putorius L.) . Z Jagdwissenschaft 35:86-99

Received February 6, 1990; accepted February 20, 1990.

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