THE
USE OF BIRD
HEAVY
FEATHERS
METAL
FOR INDICATING
POLLUTION
A. A. GOEDE
Research Institute f o r Nature Management, Texel, the Netherlands and M. DE BRUIN
lnteruniversity Reactor Institute, Delft, the Netherlands
Abstract. Feather material has been investigated as a suitable indicating tissue for heavy metal pollution. At least three different routes are described through which trace metal content in the feathers can increase: internal deposition during growth, contamination by the bird's secretion and outside contamination. As mercury is only deposited during feather growth, the feather burden reflects the internal contamination of the bird. Internal deposition of zinc appears to be well regulated in the shaft but concentrations differ widely in the vanes. No external contamination of the vanes could be demonstrated, so these levels reflect contamination from inside. Selenium and lead contamination can be deposited by the birds secretion. W h e n the time elapsed after feather formation is accounted for, the feather can give indirectly an indication of the birds exp6~ure to these elements.
1. Introduction
To study the extent of pollution, there is a growing need for materials to indicate a n d / o r monitor the occurrence of pollutants. Biological indicators and monitors may be of interest if they provide information on transport and accumulation in ecosystems. The use of the feather as such a tissue has several advantages. It is known that heavy metals can be present in the feathers in concentrations that make reliable analysis possible. Moreover, feathers can be obtained without killing the bird, which makes large-scaled and repeated sampling possible. However, attention should be given to how these pollutants reach the feathers and in which way the tissue burden reflects the presence and level of a pollutant in the bird's environment. It was found only recently that feathers can get contaminated externally with Cu, Fe and Ni with time after the feather was formed (Rose and Parker, 1982). When the feather is used as an indicating or monitoring tissue, it is therefore essential to know the underlying mechanisms determining the feather concentrations. For uptake of metals in the feather, three routes can be distinguished (Figure 1): (a) uptake through the food and incorporation during feather growth; (b) contamination through preening: heavy metals present in secretion products o f salt- a n d / o r preen glands contaminate the feathers; (c) contamination through direct contact with the environment (water, air, mud etc.). We have investigated these routes along which heavy metals accumulate in feathers Environmental Monitoring and Assessment 7 (1986) 249-256. 9 1986 by D. Reidel Publishing Company.
250
Fig. 1.
A. A. GOEDE AND M. DE BRUIN
Three different routes through which the feather might get enrichted with heavy metals (see text).
of waders during their stay in the Dutch Wadden Sea. This estuarine area is of great significance in the life cycle of waders as a post-nuptial moulting ground (Smit and Wolff, 1981; Boere, 1976). In autumn wading birds from subarctic and arctic breeding grounds migrate to this area where the adult birds moult all their feathers and the juvelines their small feathers only, retaining the flight feathers formed on the breeding grounds. However the Wadden Sea area is subject to pollution by various sources, a.o. the rivers Rhine and Scheldt. The breeding grounds of the knot (Cah'dris canutus) and bar-tailed godwit (Limosa lapponica) are arctic and it is assumed that the exposure to metal pollution is negligible in these areas. Therefore, the juveniles when arriving in the Wadden Sea are regarded 'claen'. Adult feathers grown during the bird's stay in the polluted Wadden Sea might reflect internal and external deposition of contaminants, in contrast to juvenile feathers which will only reflect external deposition. 2. Methods
Primaries of both age classes have been collected, and thr vanes and shafts have been analysed separately for Hg, Zn, and Se by means of neutron activiation analysis using the system developed at the Interuniversity Reactor Institute for routine analysis (de
THE USE OF BIRD FEATHERS
FOR INDICATING
HEAVY
METAL
POLLUTION
251
Bruin and Korthoven, 1972; de Bruin et al., 1982). Pb was measured by means of atomic absorption spectrometry (Goede and de Voogt, 1985). Prior to analysis the feathers were shaken in deionized water for one minute to remove superficial contamination. - Feathers o f juvenile knots were sampled f r o m the m o m e n t of arrival in the Wadden Sea (end of August) until departure about two months later. After formation, the feathers lose vascular and nervous connections and hence become physiologically isolated f r o m the rest o f the bird. Therefore, any change in concentration in the juvenile feathers formed on the breeding grounds, is due to external contamination or leaching. - Adult feathers were sampled 0--4 weeks after completion of growth (the growth covers 1-1.5 weeks) and checked for correlations between vane and shaft concentrations (strong correlations mean that no changes in concentration have taken place since the firtst contamination). - Clean juvenile feathers were exposed intensively - up to 60 h - to the water and mud o f the environment to detect direct uptake. Adult feathers were washed out in artificial seawater to determine leaching. It is presumed that salt- a n d / o r preenglands play an essential role in the transport o f Se from the environment into the feather. This called for additional experiments. The role of preening was investigated in the dunlin (Calidris alpina). On their migration f r o m the breeding grounds to the Wadden Sea, some adult dunlins were captured and collected in Sweden. Others were sampled shortly after arrival in the Wadden Sea, in the middle of August and this has been repeated every month until until December. Se-concentrations of the glands and feather vanes could thus be correlated over time. 3. Results and Discussion
3.1. MERCURY Hg concentrations in the feather did neither change with time nor after 60 h exposure to the environment or washing. A very strong positive correlation ( p < 0 . 0 0 1 ) was found between vane and shaft concentrations (Figure 2). Therefore it can be concluded that Hg-concentration o f the feather does reflect the internal deposition of mercury during formation of the feather. Recently this has been confirmed by results of experiments reported by Appelquist et al. (1984). The influence of ultra-violet light, heating, freezing and weathering on the Hg concentration in primaties was investigated and it was concluded that even after 8 months of intensive exposure, variation in concentrations was less than 10%. 3.2. ZtNC Markedly different were the results with the Zn concentrations in shafts and vanes. Shaft concentrations did not change with time or after environmental exposure and
252
A.
mg.kg -I Hg
A.
GOEDE
AND
M.
DE
BRUIN
vane
16
14
12 0
0
0
10
O o
8
o
0
o
6
0
o. 9o
o,
o knot 9 bar-tailed
%~ *
.~""
2
i
I
2
i
i
4
i
w
I
6
8
mg.kg Fig. 2.
godwit
i
i
1
i
I0
Hg s h a f t
Relation between Hg vane and shaft concentration in adult knots and bar-tailed godwits.
washing, but they were found to vary over a very narrow range (Figure 3). Adult and juvenile shaft concentrations of various waderspecies all fell within this range. It can be concluded that the shaft concentration of Zn does reflect internal deposition during feather formation, but that the deposition is well regulated and therefore does not reflect the birds exposure to Zn. Vane concentrations of Zn did not change with time or after exposure to the environment. But after 24 h of washing, about 25% o f Zn concentration in the vanes
THE USE OF BIRD FEATHERS
mg.kg
1
FOR INDICATING
HEAVY
METAL
POLLUTION
253
Zn vane
1000
800 o
600 o o
400 0
0 0
o
200
9
o knot 9 bar-tailed
o
9....o..:.~o o
!
80
Fig. 3.
o
"~ ~o :.. c,
I
100
'
I
120
godwit
i
mg.kg
1 Zn s h a f t
Relation between Zo vane and shaft concentration in adult knots and bar-tailed godwits.
was lost. In contrast to the shaft concentrations of Zn, vane concentrations vary widely (Figure 3). If Zn deposition on the vane during formation is strictly controlled too, the conclusion must be drawn that leaching is well as heavy external contamination can occur within a short time. However, such contamination was not observed in the juvenile feathers even after a stay of these birds for two months in the area, or after intensive exposure of the feathers to the environment. The loss of Zn from the vane by washing m a y be due to a weak binding with the keratine. Hence, the results are inconclusive if the assumption is that vane concentrations of Zn are regulated like in the shaft. However, if such a strong regulation does not exist, the variable vane concentrations reflect only immediately after feather formation, the variable exposures of the birds to Zn. 3.3. LEAD AND SELENIUM Vane concentrations of PJ0 and Se increased considerably with time (Figure 4). Shaft concentrations increased far less pronouncedly. Evidently the feathers got externally contaminated. However, no direct contamination was observed after exposure to the environment. Apparently the feathers got contaminated by the secretion products of the bird itself. Indeed, preliminary results of analyses of some preen glands showed widely varying but sometimes high Se concentrations. Furthermore it is known that
254
A. A. GOEDE
AND
M. DE BRUIN
rag. k g
9f 32,7
Pb vane 20
18 juvenile
knot 14
I0
0 Q
OO
61 o
:
o:!I o,
N.D.i !
aug
!
sept
I
oct
nov 9 Schiermonnikoog o Vlieland
Fig. 4. Lead concentrations in the feather vanes of juvenile knots with time (ND: concentration below the detection limit; O, O: eastern, resp. western Dutch Wadden Sea). From Goede and de Voogt (1985).
Pb accumulates in the salt glands (Buggiani and Rindi, 1980; Howarth et al., 1981; Howarth et aL, 1982). The relation between Se concentrations in preen glands and feather vanes was further investigated in the dunlin. Before arrival of these birds in the Wadden Sea, the gland Se concentrations were relatively low (Figure 5a), but concentrations in the one year-old primary vanes were high and differed widely (Figure 5b). Shortly after arrival in the Wadden Sea, in the middle o f August, preen gland Se concentrations were already significantly elevated (p < 0.0005). This increase continued for about two months, then levelled off, indicating that an equilibrium had been reached between accumulation and secretion (the high variability in preen gland concentration from October is due to one exceptionally high concentration of 46.6 Ixg g - 1). Primary vane concentrations were markedly lower in the new grown feathers, but started to increase rapidly with time (Figure 5b). These results give the first evidence that the feathers indeed got contaminated by secretion products of the preen gland. Se could be washed out of the vane: in 24 h 40~ was lost. Obviously Se did not bind firmly to the keratine. 4. Conclusions
It can be concluded from this study that the feather can be used at least as an indicator
THE USE OF BIRD FEATHERS FOR INDICATING HEAVY METAL POLLUTION -1
mg. kg
255
Se
4O
A
30
20
1
10-
(, 0
i
i
i
I
,
S
70-
50"
T
30.
I0AGg Fig. 5.
Sebt
Okt
N~)v
S e l e n i u m c o n c e n t r a t i o n s (with s.d.) in A) p r e e n g l a n d s a n d B) p r i m a r y v a n e s o f a d u l t d u n l i n s in the D u t c h W a d d e n Sea, w i t h t i m e (S: birds f r o m Sweden).
for the presence or absence of Hg, Zn, Pb, and Se in the ecosystem the bird is part of. For Zn, the feather vanes can be used in this way only shortly after completion of the feather and when using Se and Pb vane concentrations, one has to account for effects occurring in the time elapsed since feather formation. A follow up study of Hg and Se (Goede, 1985; Goede and de Bruin, 1985) will show a close relationship between the body burden and the feather concentration of the bird.
256
A. A. GOEDE AND M. DE BRUIN
Acknowledgements We are indebted to Drs. P. de Voogt of the Institute for Environmental Studies of the Free University, Amsterdam, who provided the dunlins for the investigation on Se and who made Pb analysis possible.
References Appelquist, H., Asbirk, S. and Drabaek, 1.: 1984, 'Mercury Monitoring: Mercury Stability in Bird Feathers', Mar. Pollut. Bull. 15, 22-24. Boere, G. C.: 1976, 'The Significance of the Dutch Waddenzee in the Annual Life Cycle of Arctic, Subarctis and Boreal Waders', Ardea 64, 210-291. Bruin, M. de and Korthoven, P. J. M.: 1972, 'Computer Oriented System for Non-Destructive Neutron Activation Analysis', Analyt. Chem. 44, 2382-2385. Bruin, M. de, Korthoven, P. J. M., and Bode, P.: 1982, 'Evaluation of a System for Routine Instrumental Neutron Activation Analysis', J. Radiat. analyt. Chem. 70, 497-512. Buggiona, S. S. and Rindi, S.: 1980, 'Lead Toxicosis and Salt Glands in Domestic Ducks', Bull. environ. Contain. & Toxicol. 24, 152-155. Goede, A. A.: 1985, 'Mercury, Selenium, Arsenic and Zinc in Waders from the Dutch Wadden Sea', Environ. Pollut. 37, 287-309. Goede, A. A. and Bruin, M. de: 1985, 'Selenium in the wader Dunlin (Calidris alpina) from the Dutch Wadden Sea', Mar. Pollut. Bull. 16, 115-117. Goede, A. A. and Voogt, P. de: 'Lead and Cadmium in Waders from the Dutch Wadden Sea', Environ. Pollut. 37, 311-322. Howarth, D. M., Hulbert, A. J., and Horning, D.: 1981, 'A comparative Study of Heavy Metal Accumulation in Tissues of the Crested Tern, Sterna bergii, Breeding near Industrialized and NonIndustrialized Areas', Austr. Wildl. Res. 8, 665-672. Howarth, D. M., Grant, T. R., and Hulbert, A. J.: 1982, 'A Comparative Study of Heavy Metal Accumulation in Tissues of the Crested Tern, Sterne bergii, Breeding near an Industrial Port Before and After Harbour Dredging and Ocean Dumping', Austr. Wildl. Res. 9, 571-577. Rose, G. A. and Parker, G. H.: 1982, 'Effects of Smelter Emissions on Metal Levels in the Plumage of Ruffed Grouse near Sudbury, Ontario, Canada', Can. J. ZooL, 60, 2659-2667. Smit, C. and Wolff, W. J. (eds.): 1981, 'Birds o f the Wadden Sea', Rotterdam, Balkema.
USE OF BIRD
HEAVY
FEATHERS
METAL
FOR INDICATING
POLLUTION
A. A. GOEDE
Research Institute f o r Nature Management, Texel, the Netherlands and M. DE BRUIN
lnteruniversity Reactor Institute, Delft, the Netherlands
Abstract. Feather material has been investigated as a suitable indicating tissue for heavy metal pollution. At least three different routes are described through which trace metal content in the feathers can increase: internal deposition during growth, contamination by the bird's secretion and outside contamination. As mercury is only deposited during feather growth, the feather burden reflects the internal contamination of the bird. Internal deposition of zinc appears to be well regulated in the shaft but concentrations differ widely in the vanes. No external contamination of the vanes could be demonstrated, so these levels reflect contamination from inside. Selenium and lead contamination can be deposited by the birds secretion. W h e n the time elapsed after feather formation is accounted for, the feather can give indirectly an indication of the birds exp6~ure to these elements.
1. Introduction
To study the extent of pollution, there is a growing need for materials to indicate a n d / o r monitor the occurrence of pollutants. Biological indicators and monitors may be of interest if they provide information on transport and accumulation in ecosystems. The use of the feather as such a tissue has several advantages. It is known that heavy metals can be present in the feathers in concentrations that make reliable analysis possible. Moreover, feathers can be obtained without killing the bird, which makes large-scaled and repeated sampling possible. However, attention should be given to how these pollutants reach the feathers and in which way the tissue burden reflects the presence and level of a pollutant in the bird's environment. It was found only recently that feathers can get contaminated externally with Cu, Fe and Ni with time after the feather was formed (Rose and Parker, 1982). When the feather is used as an indicating or monitoring tissue, it is therefore essential to know the underlying mechanisms determining the feather concentrations. For uptake of metals in the feather, three routes can be distinguished (Figure 1): (a) uptake through the food and incorporation during feather growth; (b) contamination through preening: heavy metals present in secretion products o f salt- a n d / o r preen glands contaminate the feathers; (c) contamination through direct contact with the environment (water, air, mud etc.). We have investigated these routes along which heavy metals accumulate in feathers Environmental Monitoring and Assessment 7 (1986) 249-256. 9 1986 by D. Reidel Publishing Company.
250
Fig. 1.
A. A. GOEDE AND M. DE BRUIN
Three different routes through which the feather might get enrichted with heavy metals (see text).
of waders during their stay in the Dutch Wadden Sea. This estuarine area is of great significance in the life cycle of waders as a post-nuptial moulting ground (Smit and Wolff, 1981; Boere, 1976). In autumn wading birds from subarctic and arctic breeding grounds migrate to this area where the adult birds moult all their feathers and the juvelines their small feathers only, retaining the flight feathers formed on the breeding grounds. However the Wadden Sea area is subject to pollution by various sources, a.o. the rivers Rhine and Scheldt. The breeding grounds of the knot (Cah'dris canutus) and bar-tailed godwit (Limosa lapponica) are arctic and it is assumed that the exposure to metal pollution is negligible in these areas. Therefore, the juveniles when arriving in the Wadden Sea are regarded 'claen'. Adult feathers grown during the bird's stay in the polluted Wadden Sea might reflect internal and external deposition of contaminants, in contrast to juvenile feathers which will only reflect external deposition. 2. Methods
Primaries of both age classes have been collected, and thr vanes and shafts have been analysed separately for Hg, Zn, and Se by means of neutron activiation analysis using the system developed at the Interuniversity Reactor Institute for routine analysis (de
THE USE OF BIRD FEATHERS
FOR INDICATING
HEAVY
METAL
POLLUTION
251
Bruin and Korthoven, 1972; de Bruin et al., 1982). Pb was measured by means of atomic absorption spectrometry (Goede and de Voogt, 1985). Prior to analysis the feathers were shaken in deionized water for one minute to remove superficial contamination. - Feathers o f juvenile knots were sampled f r o m the m o m e n t of arrival in the Wadden Sea (end of August) until departure about two months later. After formation, the feathers lose vascular and nervous connections and hence become physiologically isolated f r o m the rest o f the bird. Therefore, any change in concentration in the juvenile feathers formed on the breeding grounds, is due to external contamination or leaching. - Adult feathers were sampled 0--4 weeks after completion of growth (the growth covers 1-1.5 weeks) and checked for correlations between vane and shaft concentrations (strong correlations mean that no changes in concentration have taken place since the firtst contamination). - Clean juvenile feathers were exposed intensively - up to 60 h - to the water and mud o f the environment to detect direct uptake. Adult feathers were washed out in artificial seawater to determine leaching. It is presumed that salt- a n d / o r preenglands play an essential role in the transport o f Se from the environment into the feather. This called for additional experiments. The role of preening was investigated in the dunlin (Calidris alpina). On their migration f r o m the breeding grounds to the Wadden Sea, some adult dunlins were captured and collected in Sweden. Others were sampled shortly after arrival in the Wadden Sea, in the middle of August and this has been repeated every month until until December. Se-concentrations of the glands and feather vanes could thus be correlated over time. 3. Results and Discussion
3.1. MERCURY Hg concentrations in the feather did neither change with time nor after 60 h exposure to the environment or washing. A very strong positive correlation ( p < 0 . 0 0 1 ) was found between vane and shaft concentrations (Figure 2). Therefore it can be concluded that Hg-concentration o f the feather does reflect the internal deposition of mercury during formation of the feather. Recently this has been confirmed by results of experiments reported by Appelquist et al. (1984). The influence of ultra-violet light, heating, freezing and weathering on the Hg concentration in primaties was investigated and it was concluded that even after 8 months of intensive exposure, variation in concentrations was less than 10%. 3.2. ZtNC Markedly different were the results with the Zn concentrations in shafts and vanes. Shaft concentrations did not change with time or after environmental exposure and
252
A.
mg.kg -I Hg
A.
GOEDE
AND
M.
DE
BRUIN
vane
16
14
12 0
0
0
10
O o
8
o
0
o
6
0
o. 9o
o,
o knot 9 bar-tailed
%~ *
.~""
2
i
I
2
i
i
4
i
w
I
6
8
mg.kg Fig. 2.
godwit
i
i
1
i
I0
Hg s h a f t
Relation between Hg vane and shaft concentration in adult knots and bar-tailed godwits.
washing, but they were found to vary over a very narrow range (Figure 3). Adult and juvenile shaft concentrations of various waderspecies all fell within this range. It can be concluded that the shaft concentration of Zn does reflect internal deposition during feather formation, but that the deposition is well regulated and therefore does not reflect the birds exposure to Zn. Vane concentrations of Zn did not change with time or after exposure to the environment. But after 24 h of washing, about 25% o f Zn concentration in the vanes
THE USE OF BIRD FEATHERS
mg.kg
1
FOR INDICATING
HEAVY
METAL
POLLUTION
253
Zn vane
1000
800 o
600 o o
400 0
0 0
o
200
9
o knot 9 bar-tailed
o
9....o..:.~o o
!
80
Fig. 3.
o
"~ ~o :.. c,
I
100
'
I
120
godwit
i
mg.kg
1 Zn s h a f t
Relation between Zo vane and shaft concentration in adult knots and bar-tailed godwits.
was lost. In contrast to the shaft concentrations of Zn, vane concentrations vary widely (Figure 3). If Zn deposition on the vane during formation is strictly controlled too, the conclusion must be drawn that leaching is well as heavy external contamination can occur within a short time. However, such contamination was not observed in the juvenile feathers even after a stay of these birds for two months in the area, or after intensive exposure of the feathers to the environment. The loss of Zn from the vane by washing m a y be due to a weak binding with the keratine. Hence, the results are inconclusive if the assumption is that vane concentrations of Zn are regulated like in the shaft. However, if such a strong regulation does not exist, the variable vane concentrations reflect only immediately after feather formation, the variable exposures of the birds to Zn. 3.3. LEAD AND SELENIUM Vane concentrations of PJ0 and Se increased considerably with time (Figure 4). Shaft concentrations increased far less pronouncedly. Evidently the feathers got externally contaminated. However, no direct contamination was observed after exposure to the environment. Apparently the feathers got contaminated by the secretion products of the bird itself. Indeed, preliminary results of analyses of some preen glands showed widely varying but sometimes high Se concentrations. Furthermore it is known that
254
A. A. GOEDE
AND
M. DE BRUIN
rag. k g
9f 32,7
Pb vane 20
18 juvenile
knot 14
I0
0 Q
OO
61 o
:
o:!I o,
N.D.i !
aug
!
sept
I
oct
nov 9 Schiermonnikoog o Vlieland
Fig. 4. Lead concentrations in the feather vanes of juvenile knots with time (ND: concentration below the detection limit; O, O: eastern, resp. western Dutch Wadden Sea). From Goede and de Voogt (1985).
Pb accumulates in the salt glands (Buggiani and Rindi, 1980; Howarth et al., 1981; Howarth et aL, 1982). The relation between Se concentrations in preen glands and feather vanes was further investigated in the dunlin. Before arrival of these birds in the Wadden Sea, the gland Se concentrations were relatively low (Figure 5a), but concentrations in the one year-old primary vanes were high and differed widely (Figure 5b). Shortly after arrival in the Wadden Sea, in the middle o f August, preen gland Se concentrations were already significantly elevated (p < 0.0005). This increase continued for about two months, then levelled off, indicating that an equilibrium had been reached between accumulation and secretion (the high variability in preen gland concentration from October is due to one exceptionally high concentration of 46.6 Ixg g - 1). Primary vane concentrations were markedly lower in the new grown feathers, but started to increase rapidly with time (Figure 5b). These results give the first evidence that the feathers indeed got contaminated by secretion products of the preen gland. Se could be washed out of the vane: in 24 h 40~ was lost. Obviously Se did not bind firmly to the keratine. 4. Conclusions
It can be concluded from this study that the feather can be used at least as an indicator
THE USE OF BIRD FEATHERS FOR INDICATING HEAVY METAL POLLUTION -1
mg. kg
255
Se
4O
A
30
20
1
10-
(, 0
i
i
i
I
,
S
70-
50"
T
30.
I0AGg Fig. 5.
Sebt
Okt
N~)v
S e l e n i u m c o n c e n t r a t i o n s (with s.d.) in A) p r e e n g l a n d s a n d B) p r i m a r y v a n e s o f a d u l t d u n l i n s in the D u t c h W a d d e n Sea, w i t h t i m e (S: birds f r o m Sweden).
for the presence or absence of Hg, Zn, Pb, and Se in the ecosystem the bird is part of. For Zn, the feather vanes can be used in this way only shortly after completion of the feather and when using Se and Pb vane concentrations, one has to account for effects occurring in the time elapsed since feather formation. A follow up study of Hg and Se (Goede, 1985; Goede and de Bruin, 1985) will show a close relationship between the body burden and the feather concentration of the bird.
256
A. A. GOEDE AND M. DE BRUIN
Acknowledgements We are indebted to Drs. P. de Voogt of the Institute for Environmental Studies of the Free University, Amsterdam, who provided the dunlins for the investigation on Se and who made Pb analysis possible.
References Appelquist, H., Asbirk, S. and Drabaek, 1.: 1984, 'Mercury Monitoring: Mercury Stability in Bird Feathers', Mar. Pollut. Bull. 15, 22-24. Boere, G. C.: 1976, 'The Significance of the Dutch Waddenzee in the Annual Life Cycle of Arctic, Subarctis and Boreal Waders', Ardea 64, 210-291. Bruin, M. de and Korthoven, P. J. M.: 1972, 'Computer Oriented System for Non-Destructive Neutron Activation Analysis', Analyt. Chem. 44, 2382-2385. Bruin, M. de, Korthoven, P. J. M., and Bode, P.: 1982, 'Evaluation of a System for Routine Instrumental Neutron Activation Analysis', J. Radiat. analyt. Chem. 70, 497-512. Buggiona, S. S. and Rindi, S.: 1980, 'Lead Toxicosis and Salt Glands in Domestic Ducks', Bull. environ. Contain. & Toxicol. 24, 152-155. Goede, A. A.: 1985, 'Mercury, Selenium, Arsenic and Zinc in Waders from the Dutch Wadden Sea', Environ. Pollut. 37, 287-309. Goede, A. A. and Bruin, M. de: 1985, 'Selenium in the wader Dunlin (Calidris alpina) from the Dutch Wadden Sea', Mar. Pollut. Bull. 16, 115-117. Goede, A. A. and Voogt, P. de: 'Lead and Cadmium in Waders from the Dutch Wadden Sea', Environ. Pollut. 37, 311-322. Howarth, D. M., Hulbert, A. J., and Horning, D.: 1981, 'A comparative Study of Heavy Metal Accumulation in Tissues of the Crested Tern, Sterna bergii, Breeding near Industrialized and NonIndustrialized Areas', Austr. Wildl. Res. 8, 665-672. Howarth, D. M., Grant, T. R., and Hulbert, A. J.: 1982, 'A Comparative Study of Heavy Metal Accumulation in Tissues of the Crested Tern, Sterne bergii, Breeding near an Industrial Port Before and After Harbour Dredging and Ocean Dumping', Austr. Wildl. Res. 9, 571-577. Rose, G. A. and Parker, G. H.: 1982, 'Effects of Smelter Emissions on Metal Levels in the Plumage of Ruffed Grouse near Sudbury, Ontario, Canada', Can. J. ZooL, 60, 2659-2667. Smit, C. and Wolff, W. J. (eds.): 1981, 'Birds o f the Wadden Sea', Rotterdam, Balkema.
