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Have arctic marine mammals adapted to high cadmium levels?
Marine Pollution Bulletin
Edited by D. J. H. Phillips
The objective of BASELINE is to publish short communications on different aspects of pollution of the marine environment. Only those papers which clearly identify the quality of the data will be considered for publication. Contributors to Baseline should refer to 'Baseline--The New Format and Content' (Mar. Pollut. Bull. 24, 124).
Pergamon
Marine Pollution Bulletin, Vol. 36, No. 6, pp. 490-492, 1998 © 1998 Published by Elsevier Science Ltd All rights reserved. Printed in Great Britain 0025-326X/98 $19.00+0.00
Plh 0025-326X(98)00045-9
Have Arctic Marine Mammals Adapted to High Cadmium Levels? R. DIETZ*, J. NORGAARDt and J. C. HANSEN$ *Department of Arctic Environment, National Environmental Research Institute, Copenhagen, Denmark tAnatomical Institute, University of Aarhus, Aarhus, Denmark $Centre of Arctic Environmental Medicine, University of Aarhus, Aarhus, Denmark Over the last two decades, many heavy metal data have become available from the Arctic regions. These data have recently been assessed as part of the Arctic Monitoring and Assessment Programme (Dietz et al., 1996, 1997; Nilsson, 1997; Dietz et al., in press). Among the conclusions of this assessment is the fact that elevated cadmium levels are found in Arctic marine mammals and birds, and these levels may often be much higher than in animals from temperate regions. Within the Arctic, some of the highest cadmium levels have been found in marine mammals from the Northwest Greenland and eastern Canadian High Arctic (for example, Dietz et al., 1996a, b; Wagemann et al., 1996; Dietz et al., 1997). The cadmium levels in kidneys of some ringed seals from Northwest Greenland are higher than the critical concentration of 200 lag g-1 wet weight, a level associated with kidney damage in mammals including humans (WHO, 1992). A recent review for the risk assessment of cadmium in humans by Elinder and Jfirup (1996) stated, however, that this is a serious overestimation of the critical concentration of cadmium in the kidney. Both environmentally exposed human populations in general, and elderly persons, have displayed evidence of cadmium-induced renal dysfunction at a urinary excretion of the order of 490
> 3 nmol cadmium per mmol creatinine. This level corresponds to kidney cortex concentrations of cadmium of about 50 gg g - ~ wet weight, i.e. four times lower than the previously accepted critical concentration. As no pathological effect studies had been carried out previously on Arctic marine mammals exposed to high cadmium levels, a pilot study was initiated on ringed seals (Phoca hispida) from Northwest Greenland collected during the mid-1980s. The samples were selected among 462 ringed seals previously analysed for cadmium in kidneys, livers and muscles (Dietz et al., 1996). The cadmium concentrations in kidneys of these seals are shown in Fig. 1. Among these, fifteen kidney samples were selected for microscopic examination from three concentration ranges, these being 1.63-5.19, 86.5-91.3 and 259-581 lagg-i wet weight respectively (Table 1). The analysis had been carried out on whole kidneys, which means that the concentrations in the cortex would be approximately 25% higher than the values cited here. The most contaminated kidney cortex would hence correspond to a concentration of 726 lag g-1 Cd wet weight (such cortex values are normally referred to when discussing critical concentrations). A quite high incidence of renal tubular proteinurea could be expected at this level, as incidences of 10% and 50% corresponding to 200 and 300lagCdg -1 respectively have been observed in workers exposed to cadmium (Elinder and Jfirup, 1996). Samples of the kidneys were removed from the storage freezer (-20°C) and placed in 4% buffered formaldehyde at 4°C. After thawing, the kidney surface was examined for pathological changes. From all kidneys, a series of 2 ram-thick slices each containing 2-3 lobuli (renuli) were cut vertically through the kidney surface and postfixed in formaldehyde for 4 days. After dehydration and embedding in paraffin, 5 ~tm thick slices were cut and stained v~ith hematoxylin and eosin, as well as with Van Gieson for collagenous fibers. Macroscopic examination of the kidneys revealed a preserved and normal-appearing multilobular (renular) structure. Light microscopy showed that tissue preservation was sub-optimal, but the renal cortical and medullary zones appeared normal in all three groups, resembling typical seal kidneys as previously decribed by Dragert et al. (1975). No increase in interstitial connective tissue due to proximal tubular cellular damage or necrosis was observed, either in the cortical labyrinth or the medullary rays, and the major glomerular architecture was preserved. No differences in renal
Volume 36/Number6/June 1998 morphology could be observed between the experimental groups. These preliminary investigations indicate that marine mammals appear able to maintain considerable concentrations of cadmium without showing renal damage. Cadmium levels have always been high in the Greenland Arctic regions, as indicated by the lack of obvious temporal trends in sediment cores, as well as historic hair samples from the 15th century from both seals and Inuits (Hansen et al., 1989; Loring and Asmund, 1996). Ringed seals may therefore have habituated to the naturally high cadmium levels in their diet. High levels of other heavy metals such as mercury have also been observed in marine mammals (for example, Law, 1996). The half-time of methyl
mercury in marine mammals is 5-10 times longer than in humans, but there are several indications that the mercury in livers of marine mammals is detoxified and stored, as the inert mercury-selenium complex (tiemannite), in metallothioneins, or in non-degradable granules of the hepatocytes (Andr6 et al., 1990). Marine mammals placed at the top of the marine trophic network may have adapted to tolerate high heavy metal levels, but further studies are needed to consider potential effects or detoxifiying mechanisms of this animal group. Funding has now been allocated to look further into this aspect within the next year, using a larger number of animals and improved sampling techniques for the pathological examinations. Information on how marine l a l , r l l l , i I
600
500
~,
400
n
.~
3o0
e~
.~,
•
•
Kidney damage level (WHO. 1992) •"=
0
200
O
*| 100
I *e
IO ]OOiii~•!|~tlil,.,.O"OOO' 0•OOI• 800• O0 . iI 18O• " l0ottOOO0 Oi•Kldneydamagel t :iI~oOO OO0 • •. • evel Oi • i•(Elm ~derandJ"ru•p'199~, t .... 0
5
10
15
20
25
30
35
40
A g e (years)
Fig. 1 Cadmiumlevelsin kidneysof ringed seals fromGreenland.
TABLE 1 Mean (range) of cadmium concentrations (gg g 1 wet weight) and age information for the three groups of ringed seals from Northwest Greenland that were selected for microscopic examination
Group
Kidney(whole)
Liver
Muscle
Age
N
Low Intermediate High
3.13 (1.63-5.19) 88.1 (86.5-91.3) 399 (259-581)
0.684 (0.400-1.36) 30.8 (19.5-52.7) 58.1 (27.1-109)
0.023 (0.007-0.070) 0.303 (0.112-0.611) 1.58 (0.800-3.00)
0.6 (0-1) 4.0 (2-7) 7.8 (4-15)
5 5 5 491
Marine Pollution Bulletin
mammals deal with high cadmium burdens may have significance for human medical treatment of cadmiuminduced renal degradation. Andr6, J.M., Ribeyre, F. and Boudou, A. (1990) Mercury contamination levels and distribution in tissues and organs of delphinids (Stenella attenuata) from the eastern tropical Pacific, in relation to biological and ecological factors. Marine Environmental Research, 30, 43-72. Dietz, R., Riget, F. and Johansen, P. (1996) Lead, cadmium, mercury and selenium in Greenland marine animals. The Science of the Total Environment, 186, 67-93. Dietz, R., Johansen, P., Riget, F. and Asmund, G. (1997) Heavy metals in the Greenland Marine Environment, National Assessment, ln: AMAP Greenland 1994-96, Arctic Monitoring and Assessment Programme (AMAP). Danish Environmental Protection Agency, Environmental Project, 356, 119-245. Dietz, R., Pacyna, J. and Thomas, D. J. (in press). Heavy metals. AMAP International Assessment, Arctic Monitoring and Assessment Programme, Oslo, Norway. Dragert, J., Corey, S. and Ronald, K. (1975) Anatomical aspects of the kidney of the harp seal Pagophilus groenlandicus (Erxleben, 1777). Rapport Process verbeaux R~union International Exploration de la Mer, 169, 133-140.
Marine PollutionBulletin, Vol. 36, No. 6, pp. 492-500, 1998 © 1998 Published by Elsevier Science Ltd. All rights reserved. Printed in Great Britain 0025-326X/98 $19.00+0.00
PII: 0025-326X(98)00029-0
Polychlorinated Biphenyls and Cyclic Pesticides in Sediments and Macro-invertebrates from the Coastal Zone and Continental Slope of Kenya J. M. EVERAARTS, E. M. VAN WEERLEE, C. V. FISCHERM and TH. J. HILLEBRAND Department of Marine Biogeochemistry and Toxicology, Netherlands Institute for Sea Research, PO Box 59, I 790 AB Den Burg, Texel, The Netherlands Over 70% of the Earth's surface consists of oceans, coastal seas and estuarine zones. The importance of marine ecosystems is also illustrated by the fact that the coastal area is inhabited by about 60% of the world's population. Thus, in particular, estuarine and coastal systems, showing considerable biological activity, are exposed to a high degree of contamination. The load of anthropogenic compounds induces impairment of various physiological functions of individual organisms and affects the ecological quality of ecosystems. Polychlorinated biphenyls (PCBs) and chlorinated pesticides (e.g. DDTs, dieldrin) show a global distribution. They are ubiquitous toxic contaminants, due to their bioaccumulative capacity and persistence and specific physico-chemical properties. Technical PCB mixtures or the individual CB congeners and pesticides accumulate in biota of all trophic levels and 492
Elinder, C.-G. and Jfirup, L. (1996) Cadmium exposure and health risks: recent findings. Ambio, 25, 370-373. Hansen, J.C., Toribara, T.Y. and Muhs, A.G. (1989) Trace metals in human and animal hair from the 15th century graves at Qilakitsoq compared with recent samples. Meddelelser om GrOnland, Man and Society, 12, 161-167. Law, R. J. (1996) Metals in marine mammals. In Environmental Contaminants in Wildlife. Interpreting Tissue Concentration, eds. W. N. Beyer, G. H. Heinz and A. W. Redmon-Norwood, pp. 357-376. SETAC Special Publication Series. CRC Press Inc., Lewis Publishers Inc., Boca Raton, FL. Loring, D.H. and Astound, G. (1996) Geochemical factors controlling accumulation of major and trace elements in Greenland coastal and fjord sediments. Environmental Geology, 28, 2-11. Nilsson, A. (1996) Arctic pollution issues: a state of the Arctic environment report. Arctic Monitoring and Assessment Programme, Oslo, Norway. Wagemann, R., Innins, S. and Richard, P. (1996) Overview and regional and temporal differences of heavy metals in Arctic and ringed seals in the Canadian Arctic. The Science of the Total Environment, 186, 41-66. WHO (1992) Cadmium. Environmental Health Criteria, Vol. 134. World Health Organization, Geneva.
residues are reported in environmental compartments from all geographical latitudes (Preston, 1988; Everaarts et al., 1993). However, from certain regions such as the South Pacific and the western Indian Ocean, contaminant levels in various environmental compartments were neither extensively investigated nor well reported. Only recently, data from these areas were published, indicating low levels of PCBs and DDTs in water and fish from an estuary on the east coast of South Africa (Grobler et al., 1996). Levels of PCBs and a wide variety of pesticides were determined just above their detection limit in sediments and shellfish from Vanuatu and Tonga (Harrison et al., 1996). Concentrations of a wide variety of organic compounds in the estuarine and coastal environment of the Fiji Islands were also found to be low (<10 ng g-1 dry weight), and it was suggested that organochlorine pesticides had undergone conversion reactions, particularly enhanced due to the tropical climatic conditions (Morrison et al., 1996). Research on marine pollution is a priority area within the research and monitoring programs of the Kenyan Marine Fisheries Institutes, and necessary for pollution management and decision making (Anon, 1991). Pollution studies in the marine environment of Kenya mainly focused on the estuarine and coastal zone in the vicinity of Mombasa (T. Williams et al., 1997). However, other coastal areas, such as the Sabaki and Tana river mouths are even more impacted by freshwater run-offs or riverine influences. To the author's knowledge, only one publication reports on residues of organochlorine pesticides in fish from the estuarine environment of Kenya (Mugachia et al., 1992), which were considered to be low. The present study contributes to knowledge on the status of the marine ecosystems along the coast of
Edited by D. J. H. Phillips
The objective of BASELINE is to publish short communications on different aspects of pollution of the marine environment. Only those papers which clearly identify the quality of the data will be considered for publication. Contributors to Baseline should refer to 'Baseline--The New Format and Content' (Mar. Pollut. Bull. 24, 124).
Pergamon
Marine Pollution Bulletin, Vol. 36, No. 6, pp. 490-492, 1998 © 1998 Published by Elsevier Science Ltd All rights reserved. Printed in Great Britain 0025-326X/98 $19.00+0.00
Plh 0025-326X(98)00045-9
Have Arctic Marine Mammals Adapted to High Cadmium Levels? R. DIETZ*, J. NORGAARDt and J. C. HANSEN$ *Department of Arctic Environment, National Environmental Research Institute, Copenhagen, Denmark tAnatomical Institute, University of Aarhus, Aarhus, Denmark $Centre of Arctic Environmental Medicine, University of Aarhus, Aarhus, Denmark Over the last two decades, many heavy metal data have become available from the Arctic regions. These data have recently been assessed as part of the Arctic Monitoring and Assessment Programme (Dietz et al., 1996, 1997; Nilsson, 1997; Dietz et al., in press). Among the conclusions of this assessment is the fact that elevated cadmium levels are found in Arctic marine mammals and birds, and these levels may often be much higher than in animals from temperate regions. Within the Arctic, some of the highest cadmium levels have been found in marine mammals from the Northwest Greenland and eastern Canadian High Arctic (for example, Dietz et al., 1996a, b; Wagemann et al., 1996; Dietz et al., 1997). The cadmium levels in kidneys of some ringed seals from Northwest Greenland are higher than the critical concentration of 200 lag g-1 wet weight, a level associated with kidney damage in mammals including humans (WHO, 1992). A recent review for the risk assessment of cadmium in humans by Elinder and Jfirup (1996) stated, however, that this is a serious overestimation of the critical concentration of cadmium in the kidney. Both environmentally exposed human populations in general, and elderly persons, have displayed evidence of cadmium-induced renal dysfunction at a urinary excretion of the order of 490
> 3 nmol cadmium per mmol creatinine. This level corresponds to kidney cortex concentrations of cadmium of about 50 gg g - ~ wet weight, i.e. four times lower than the previously accepted critical concentration. As no pathological effect studies had been carried out previously on Arctic marine mammals exposed to high cadmium levels, a pilot study was initiated on ringed seals (Phoca hispida) from Northwest Greenland collected during the mid-1980s. The samples were selected among 462 ringed seals previously analysed for cadmium in kidneys, livers and muscles (Dietz et al., 1996). The cadmium concentrations in kidneys of these seals are shown in Fig. 1. Among these, fifteen kidney samples were selected for microscopic examination from three concentration ranges, these being 1.63-5.19, 86.5-91.3 and 259-581 lagg-i wet weight respectively (Table 1). The analysis had been carried out on whole kidneys, which means that the concentrations in the cortex would be approximately 25% higher than the values cited here. The most contaminated kidney cortex would hence correspond to a concentration of 726 lag g-1 Cd wet weight (such cortex values are normally referred to when discussing critical concentrations). A quite high incidence of renal tubular proteinurea could be expected at this level, as incidences of 10% and 50% corresponding to 200 and 300lagCdg -1 respectively have been observed in workers exposed to cadmium (Elinder and Jfirup, 1996). Samples of the kidneys were removed from the storage freezer (-20°C) and placed in 4% buffered formaldehyde at 4°C. After thawing, the kidney surface was examined for pathological changes. From all kidneys, a series of 2 ram-thick slices each containing 2-3 lobuli (renuli) were cut vertically through the kidney surface and postfixed in formaldehyde for 4 days. After dehydration and embedding in paraffin, 5 ~tm thick slices were cut and stained v~ith hematoxylin and eosin, as well as with Van Gieson for collagenous fibers. Macroscopic examination of the kidneys revealed a preserved and normal-appearing multilobular (renular) structure. Light microscopy showed that tissue preservation was sub-optimal, but the renal cortical and medullary zones appeared normal in all three groups, resembling typical seal kidneys as previously decribed by Dragert et al. (1975). No increase in interstitial connective tissue due to proximal tubular cellular damage or necrosis was observed, either in the cortical labyrinth or the medullary rays, and the major glomerular architecture was preserved. No differences in renal
Volume 36/Number6/June 1998 morphology could be observed between the experimental groups. These preliminary investigations indicate that marine mammals appear able to maintain considerable concentrations of cadmium without showing renal damage. Cadmium levels have always been high in the Greenland Arctic regions, as indicated by the lack of obvious temporal trends in sediment cores, as well as historic hair samples from the 15th century from both seals and Inuits (Hansen et al., 1989; Loring and Asmund, 1996). Ringed seals may therefore have habituated to the naturally high cadmium levels in their diet. High levels of other heavy metals such as mercury have also been observed in marine mammals (for example, Law, 1996). The half-time of methyl
mercury in marine mammals is 5-10 times longer than in humans, but there are several indications that the mercury in livers of marine mammals is detoxified and stored, as the inert mercury-selenium complex (tiemannite), in metallothioneins, or in non-degradable granules of the hepatocytes (Andr6 et al., 1990). Marine mammals placed at the top of the marine trophic network may have adapted to tolerate high heavy metal levels, but further studies are needed to consider potential effects or detoxifiying mechanisms of this animal group. Funding has now been allocated to look further into this aspect within the next year, using a larger number of animals and improved sampling techniques for the pathological examinations. Information on how marine l a l , r l l l , i I
600
500
~,
400
n
.~
3o0
e~
.~,
•
•
Kidney damage level (WHO. 1992) •"=
0
200
O
*| 100
I *e
IO ]OOiii~•!|~tlil,.,.O"OOO' 0•OOI• 800• O0 . iI 18O• " l0ottOOO0 Oi•Kldneydamagel t :iI~oOO OO0 • •. • evel Oi • i•(Elm ~derandJ"ru•p'199~, t .... 0
5
10
15
20
25
30
35
40
A g e (years)
Fig. 1 Cadmiumlevelsin kidneysof ringed seals fromGreenland.
TABLE 1 Mean (range) of cadmium concentrations (gg g 1 wet weight) and age information for the three groups of ringed seals from Northwest Greenland that were selected for microscopic examination
Group
Kidney(whole)
Liver
Muscle
Age
N
Low Intermediate High
3.13 (1.63-5.19) 88.1 (86.5-91.3) 399 (259-581)
0.684 (0.400-1.36) 30.8 (19.5-52.7) 58.1 (27.1-109)
0.023 (0.007-0.070) 0.303 (0.112-0.611) 1.58 (0.800-3.00)
0.6 (0-1) 4.0 (2-7) 7.8 (4-15)
5 5 5 491
Marine Pollution Bulletin
mammals deal with high cadmium burdens may have significance for human medical treatment of cadmiuminduced renal degradation. Andr6, J.M., Ribeyre, F. and Boudou, A. (1990) Mercury contamination levels and distribution in tissues and organs of delphinids (Stenella attenuata) from the eastern tropical Pacific, in relation to biological and ecological factors. Marine Environmental Research, 30, 43-72. Dietz, R., Riget, F. and Johansen, P. (1996) Lead, cadmium, mercury and selenium in Greenland marine animals. The Science of the Total Environment, 186, 67-93. Dietz, R., Johansen, P., Riget, F. and Asmund, G. (1997) Heavy metals in the Greenland Marine Environment, National Assessment, ln: AMAP Greenland 1994-96, Arctic Monitoring and Assessment Programme (AMAP). Danish Environmental Protection Agency, Environmental Project, 356, 119-245. Dietz, R., Pacyna, J. and Thomas, D. J. (in press). Heavy metals. AMAP International Assessment, Arctic Monitoring and Assessment Programme, Oslo, Norway. Dragert, J., Corey, S. and Ronald, K. (1975) Anatomical aspects of the kidney of the harp seal Pagophilus groenlandicus (Erxleben, 1777). Rapport Process verbeaux R~union International Exploration de la Mer, 169, 133-140.
Marine PollutionBulletin, Vol. 36, No. 6, pp. 492-500, 1998 © 1998 Published by Elsevier Science Ltd. All rights reserved. Printed in Great Britain 0025-326X/98 $19.00+0.00
PII: 0025-326X(98)00029-0
Polychlorinated Biphenyls and Cyclic Pesticides in Sediments and Macro-invertebrates from the Coastal Zone and Continental Slope of Kenya J. M. EVERAARTS, E. M. VAN WEERLEE, C. V. FISCHERM and TH. J. HILLEBRAND Department of Marine Biogeochemistry and Toxicology, Netherlands Institute for Sea Research, PO Box 59, I 790 AB Den Burg, Texel, The Netherlands Over 70% of the Earth's surface consists of oceans, coastal seas and estuarine zones. The importance of marine ecosystems is also illustrated by the fact that the coastal area is inhabited by about 60% of the world's population. Thus, in particular, estuarine and coastal systems, showing considerable biological activity, are exposed to a high degree of contamination. The load of anthropogenic compounds induces impairment of various physiological functions of individual organisms and affects the ecological quality of ecosystems. Polychlorinated biphenyls (PCBs) and chlorinated pesticides (e.g. DDTs, dieldrin) show a global distribution. They are ubiquitous toxic contaminants, due to their bioaccumulative capacity and persistence and specific physico-chemical properties. Technical PCB mixtures or the individual CB congeners and pesticides accumulate in biota of all trophic levels and 492
Elinder, C.-G. and Jfirup, L. (1996) Cadmium exposure and health risks: recent findings. Ambio, 25, 370-373. Hansen, J.C., Toribara, T.Y. and Muhs, A.G. (1989) Trace metals in human and animal hair from the 15th century graves at Qilakitsoq compared with recent samples. Meddelelser om GrOnland, Man and Society, 12, 161-167. Law, R. J. (1996) Metals in marine mammals. In Environmental Contaminants in Wildlife. Interpreting Tissue Concentration, eds. W. N. Beyer, G. H. Heinz and A. W. Redmon-Norwood, pp. 357-376. SETAC Special Publication Series. CRC Press Inc., Lewis Publishers Inc., Boca Raton, FL. Loring, D.H. and Astound, G. (1996) Geochemical factors controlling accumulation of major and trace elements in Greenland coastal and fjord sediments. Environmental Geology, 28, 2-11. Nilsson, A. (1996) Arctic pollution issues: a state of the Arctic environment report. Arctic Monitoring and Assessment Programme, Oslo, Norway. Wagemann, R., Innins, S. and Richard, P. (1996) Overview and regional and temporal differences of heavy metals in Arctic and ringed seals in the Canadian Arctic. The Science of the Total Environment, 186, 41-66. WHO (1992) Cadmium. Environmental Health Criteria, Vol. 134. World Health Organization, Geneva.
residues are reported in environmental compartments from all geographical latitudes (Preston, 1988; Everaarts et al., 1993). However, from certain regions such as the South Pacific and the western Indian Ocean, contaminant levels in various environmental compartments were neither extensively investigated nor well reported. Only recently, data from these areas were published, indicating low levels of PCBs and DDTs in water and fish from an estuary on the east coast of South Africa (Grobler et al., 1996). Levels of PCBs and a wide variety of pesticides were determined just above their detection limit in sediments and shellfish from Vanuatu and Tonga (Harrison et al., 1996). Concentrations of a wide variety of organic compounds in the estuarine and coastal environment of the Fiji Islands were also found to be low (<10 ng g-1 dry weight), and it was suggested that organochlorine pesticides had undergone conversion reactions, particularly enhanced due to the tropical climatic conditions (Morrison et al., 1996). Research on marine pollution is a priority area within the research and monitoring programs of the Kenyan Marine Fisheries Institutes, and necessary for pollution management and decision making (Anon, 1991). Pollution studies in the marine environment of Kenya mainly focused on the estuarine and coastal zone in the vicinity of Mombasa (T. Williams et al., 1997). However, other coastal areas, such as the Sabaki and Tana river mouths are even more impacted by freshwater run-offs or riverine influences. To the author's knowledge, only one publication reports on residues of organochlorine pesticides in fish from the estuarine environment of Kenya (Mugachia et al., 1992), which were considered to be low. The present study contributes to knowledge on the status of the marine ecosystems along the coast of