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Mercury, selenium, arsenic and zinc in waders from the Dutch Wadden Sea
Environmental Pollution (Series A) 37 (1985) 287-309
Mercury, Selenium, Arsenic and Zinc in Waders from The Dutch Wadden Sea
A. A. G o e d e Research Institute for Nature Management, Texel, The Netherlands
ABSTRACT In the Dutch Wadden Sea, a major post-nuptial moulting area for waders, three wader species were investigated )br metal contamination using mainly the feathers as monitoring tissue. All four elements--mercury, arsenic, selenium and zinc--were detected at sometimes highly elevated levels. The implications are discussed.
INTRODUCTION In the years 1964-1966 high mortality among several bird species made it painfully clear that the river Rhine (and Meuse) does not end where it meets the North Sea. Part of it continues as a 'coastal river' and deposits a considerable amount of its load in a large estuarine area, 100-150 km to the n o r t h - - t h e Wadden Sea. In those years the pesticides telodrin and dieldrin were discharged into the river: as a result, in the Dutch Wadden Sea the sandwich tern Sterna sandvicensis came close to extinction (Koeman, 1971). Also, other pollutants carried by the rivers--heavy metals and PCBs--give cause for concern. Although the discharge of some heavy metals has been reduced in the last 10-15 years, it has not ended. The long-term effects of chronic low exposures to these discharges on the estuarine ecosystems are unknown. Recently, elevated levels of 287
Environ. Pollut. Ser. A. 0143-1471/85/$03-30 © Elsevier Applied Science Publishers Ltd, England, 1985. Printed in Great Britain
288
A. A. Goede
mercury have been reported in two vertebrate species in the Wadden Sea: the harbour seal Phoca vitulina (Reijnders, 1980) and the eelpout Zoarces viviparus (Essink, 1980). Regarding PCBs, it is suspected that the high concentrations found in the harbour seals from the Dutch Wadden Sea correlate with the seal's strongly decreased reproductive success (Reijnders, 1980). It has become clear, particularly in the last decade, that the Wadden Sea has a very important function as a moulting area for many bird species, especially for large numbers of waders at the time of the postnuptial moult (Boere, 1976). Large percentages of the world population of some wader species are dependent on the Wadden Sea in this respect (Smit & Wolff, 1981). These waders are at the end of a food chain. Because of this, it is of the utmost importance to know to what extent these birds are exposed to pollution in this area. Therefore, an investigation into the metal and PCB contamination of waders during the post-nuptial moult in the Dutch Wadden Sea has been initiated. This paper gives the results concerning mercury, selenium, arsenic and zinc.
MATERIALS AND METHODS The metal contamination of waders in the Dutch Wadden Sea was investigated using the primaries formed in this area as a monitoring tissue. During post-nuptial moult the adult waders renew the whole plumage; the first calender year birds (from now on called juveniles) retain the primaries formed on the breeding grounds. The breeding grounds of the investigated species are remote: the knot Calidris canutus population moulting in the Wadden Sea breeds in Greenland and NE Canada; the bar-tailed godwit Limosa lapponica on the Taymyr peninsula in Siberia and the Icelandic redshank Tringa totanus robusta on Iceland (Boere & Smit, 1981). It may be assumed that the exposure to metal pollution is negligible in these areas. The concentrations of metals in juvenile primaries formed on the breeding grounds, together with concentrations in primaries from museum specimens (1900-1930 and 1960-1970 collections) and a primary from a knot sampled in Morocco in the spring of 1982, were used to compare concentrations in recently formed primaries in the Dutch Wadden Sea.
289
Metal in waders
Sampling The juvenile primaries, as well as newly formed adult No. 8 primaries, were collected in the autumns of 1979-1982. The birds were trapped by mist-netting in the eastern part of the Dutch Wadden Sea, near the island of Schiermonnikoog, and in the western part, near the island of Vlieland (Fig. l). On Schiermonnikoog it was possible to collect enough adult redshank and male bar-tailed godwit feathers to compare different years. Primaries No. 8 from specimens were obtained from the collection of the Zoological Museum, Amsterdam, the preserved skins having been treated with an arsenic compound. These birds had been collected in, or near, the Dutch Wadden Sea; however, some collection dates were in May Danish Wadden
Gefrnor1"-_ Dutchi
Fig. 1. Location of the Dutch Wadden Sea (1, mouth of the river Rhine; 2, island of Vlieland; 3, island of Schiermonnikoog).
290
A. A, Goede
(spring migration). In these cases it is uncertain where the primaries had been formed the previous autumn. The godwits were all collected in May; hence their feathers had been formed on the west coast of Africa or in NW Europe. Three of the five adult knots were also collected in May. According to the biometrical measurements one probably belonged to the Greenland/Canada breeding population moulting in NW Europe with the Wadden Sea as the most important area, the other two to the Siberian breeding population mainly (post-nuptial) moulting in Africa (Dick, 1975; Dick et al., 1976). Their concentrations will be given separately in the 'Results' section, the latter being referred to as 'Siberian' knot. To avoid contamination surgical gloves were worn when the feathers were pulled out and individually put into labelled plastic bags. As described by Goede & de Bruin (1984) the following feather parts were used as a monitoring tissue: the vane for Zn and Se and the shaft for Hg and As. When vanes are to be used as tissue indicating exposure of the bird to Se, the time since the formation of the feather has to be known since the vane accumulates Se with time (Goede & de Bruin, 1984). While collecting the feathers it was observed that primary No. 8 is fully grown (no blood in the end of the quill) when primary No. 10 is at the growing stage 4, i.e. when the total primary moult score was 49 (according to Ashmole, 1962). In the 'Results' section the time since completion of No. 8 is given as the time since primary moult score 49 (Boere, 1976). The feather needs 1 to 1.5 months to grow. In addition, some birds which recently completed the growth of the primary No. 8 were sacrificed (suffocated in ether), to determine liver and kidney concentrations (godwits, 0-2 weeks and redshanks, 2-4 weeks after completion). Having initially been stored at - 1 8 °C, they were eventually stored at - 6 0 °C in the laboratory.
Sample analysis All laboratory material involved in handling and storage of the samples was rinsed once with 1:1 concentrated HNO 3 and four times with deionized water. Prior to analysis the feathers were shaken in deionized water for 1 min to remove superficial contamination and dried at 60 °C for 30 min. The vane was clipped from the shaft with stainless steel scissors. The metal concentrations were measured by means of instrumental neutron activation analysis, using the IRI system for routine analysis,
Metal in waders
291
described in detail elsewhere (de Bruin & Korthoven, 1972; de Bruin et al., 1982; Goede & de Bruin, 1984). Prior to analysis, livers and kidneys were freeze-dried for 70 h. A part of the liver was lipid extracted by repeated washing with hexane for 2 h in a Soxhlet apparatus. The loss of weight of the sample was considered to be the lipid content. Percentages of water in these organs and fat content of the liver are given in Table 1. TABLE 1 Percentages o f W a t e r a n d F a t in Liver a n d Kidney
Godwit Redshank
Weight % H20 liver
Weight % H20 kidney
Weight % fat dry liver
n
71"34 +_ 0'78 71.07 + 0-59
75'91 _ 1.07 75.51 +_ 0.29
9"96 _ 3"04 6-73 + 1.33
10 3
Metal concentrations of the liver are given in mg kg- 1 lean dry weight and kidney concentrations in mg kg-1 dry weight. In the 'Results' section mean values are given, together with standard deviations.
RESULTS
Mercury--shaft (Table 2) All juveniles, both museum specimens and trapped birds, had low Hg concentrations in the shaft; godwits significantly lower than knots and redshanks (Wilcoxon-two-tailed test, p < 0.01). Adult godwits from the museum collections, 'Siberian' knots from museum collections and a knot from 1930 had comparable levels. Compared with them, all recent adults, both from Schiermonnikoog and Vlieland, had elevated Hg levels in the shaft, most pronounced in the redshanks from Vlieland. The two adult knots from the 1960s also had elevated levels, comparable with those found in recent years. The redshank from Schiermonnikoog had significantly higher concentrations in 1979 (7.84 ___1.14mg kg-1, n = 10) than in 1980-1981
TABLE 2
20 2
3.12 __+0-06 0.38 + 0-14
D e t e c t i o n limit
2 1 2
0-57 ___0.31 0-41 5.01 + 1.75 5.76 + 1.68
4 27
0.69 + 0.25 0.94 _ 0.48
n
Adults, 1979-1982, Schiermonnikoog Vlieland
Juveniles, 1927 1969 Juveniles, 1979-1982 A d u l t B-t godwit, 1904-1963 A d u l t Sib. k n o t , 1931-1982 A d u l t , 1930 A d u l t s , 1964 ( M a y bird) - 1 9 6 9
Knot
7
--
--
1 ---
-6
nND
10.26 ___3.78
6.54 + 1.88
1-07 ± 0.35
Redshank
5
20
10
n
--
--
nND
10 19 5 3
4.89 + 0.97 0.14 + 0-09
4 4
n
1-96 + 0-41 2.50 __+0.95 3-67 + 2.00
0.29 + 0.20 0.43 + 0.23
Bar-tailed godwit
-7
----
6 1
nND
~/3'
~_/~
M e r c u r y C o n c e n t r a t i o n s in F e a t h e r S h a f t s o f W a d e r s (in m g kg 1 ; n, n u m b e r w i t h d e t e c t a b l e c o n c e n t r a t i o n s ; n N D , n u m b e r with n o d e t e c t a b l e c o n c e n t r a t i o n s ; n + N D , t o t a l s a m p l e size)
e~
Metal in waders
293
(5.23+ 1.54mgkg -1, n = 10) (p<0-01). Male godwits from Schiermonnikoog did not differ significantly in the subsequent years, 1980 and 1981. Redshanks and female godwits from Vlieland had significantly higher Hg levels than their congeners from Schiermonnikoog (p <0.02); the male godwits showed the same trend. On Schiermonnikoog redshanks and knots had significantly higher Hg concentrations in the shaft than godwits (p < 0.02). In 1979 redshanks also had significantly higher concentrations than knots (p < 0.01). Also on Vlieland, redshanks had significant higher levels than godwits (p < 0.02). The male godwits did not differ significantly from the females.
Arsenic
shaft (Table 3)
All but one juvenile had no detectable amounts of As in the shaft. Compared with them, the adults from the Wadden Sea had elevated levels. Significant differences in concentrations in the different sampling years were found in redshanks and male godwits from Schiermonnikoog, concentrations being higher in the earlier years. The redshanks had higher concentrations in 1979 than in 1980-1981 (p < 0.01), those from 1980 and 1981 did not differ from each other; the male godwits had higher concentrations in 1980 than in 1981 (4 out of 9 having no detectable concentrations, p < 0-02). Female godwits from Vlieland had higher As shaft concentrations than those from Schiermonnikoog (only a weak significance: p < 0.10, since one Vlieland bird had an undetectable concentration--however, its detection limit was relatively high, 1.01 mg kg-1). The redshank data from Vlieland were scattered. Knots from Schiermonnikoog in 1979 had significantly lower As concentrations in the shaft than the redshanks from the same year and location. No significant differences were found between female and male godwits.
Selenium--vane (Table 4) After arrival in the Wadden Sea, juvenile knots (Goede & de Bruin, 1984) and redshanks (Fig. 2) rapidly accumulated Se in the vane. Concentrations in the juvenile feathers from museum specimens did not
TABLE
3
0"49 + 0-07 0'18 + 0"29
Detection limit
--
1"03_+0.59
Juveniles, 1979-1982 Adults, Schiermonnikoog 1979 1980 (1980-1981 R e d s h a n k ) 1981 Vlieland, 1979-1982
Knot
17
n
17
14 3
nND
0"15_+0.21
5
9
0-60__+0-23 1 ' 6 3 + 1.07
1 10
n
0"78 1.46 __+0"37
Redshank
9
--
1
8 -
nND
0-56 __+0-26 0-51 ___0"10 0-47+0.17 3-17+0.93 0"87 ___0'48 0.11 + 0 " 2 4
--
Bar-tailed godwit
Arsenic C o n c e n t r a t i o n s in F e a t h e r Shafts o f W a d e r s (Definitions as in Table 2)
9 10 5 4 3
--
n
1 -4 1 -16
10
nND
3
~/(3
~/~
¢3
D e t e c t i o n limit
2-4 weeks
0-2 weeks after a r r i v a l in t h e W a d d e n Sea A d u l t B-t godwit, 1904 1963 6-7 months A d u l t Sib. k n o t . 1930 1982 5-7 months Adult, 1930-1969 1-4 months A d u l t , 1964 7 months Adults, 1979-1982 0-2 weeks Schiermonnikoog 2-4 weeks Vlieland 0-2 weeks
Juveniles, 1927-1982
Time since completion o f the feather
3 2 1 20
2
4.33 + 0.97 2 1 . 2 3 + 1.18 53.96 15.72_+_5.32
18.33+2.90
1-80 + 0.97
8
n
3 . 6 8 _ 1.02
Knot
14
--
-----
14
nND
13-82 + 3.06
12.94+__4.11 8 - 7 4 + 1.51
3-43 + 1.02
Redshank
3
18 2
4
n
--
---
--
nND
0.81 +- 0.15
5.65___ 1-98 7-24 _+ 0.94
7.45 + 1.62 9 . 5 9 + 1"79
-5.38 _ 3.82
Bar-tailed godwit
TABLE 4 S e l e n i u m C o n c e n t r a t i o n s in F e a t h e r V a n e s o f W a d e r s ( D e f i n i t i o n s as in T a b l e 2)
5 3
10 19
-5
n
6
---
---
6 --
nND
2/ff
~-/~
L~
2
296
A. A. Goede rag. kg "1 Se Vane
30KNOT 2520 15. 10-
• ° o
5-
ND aug
'
sept
OCt
nov
rag. k g ' l Se
20 -
REDSHANK
Vane
15_ 10_ 5-
ND i
aug
sept
oct
nov
®museum feathers 1927-1928 o museum feathers 1966-1969
Fig. 2.
Selenium concentrations in the vanes of juvenile knots and redshanks with time (ND, vane with concentration below the detection limit).
differ from those found in juvenile feathers from recent times (Fig. 2). No increase in concentrations was found in juvenile godwit vanes (at the end of September all were below the detection limit (n = 6), as at the beginning of November (n = 4). However, very little is known about their migration. It is not unlikely that the November birds belonged to a group arriving later, while the first ones had left for the African wintering grounds, as do a large percentage of the adults (Boere & Smit, 1981). Just after arrival of the juveniles in the Wadden Sea relatively low or undetectable concentrations were found in vanes formed on the breeding grounds. Also relatively low concentrations were found in the vanes of the Siberian knots, even many months after the formation was completed. In contrast, feathers formed in the Wadden Sea had elevated levels in only a few weeks after formation. The knot feather from a bird collected in November 1930 on Schiermonnikoog also had an elevated level shortly after its formation.
297
Metal in waders
No yearly differences were found in recent feathers. On Schiermonnikoog the female godwits had a significantly lower level than the males (p < 0.01), the same trend being seen on Vlieland. Clearly, the knot had the most contaminated feather vanes. Zinc--vane (Fig. 3) In all juveniles from past and present samples, the range of vane Zn concentrations amounted to 100-400 mg kg-1 (one extreme value in the redshank: 686 mg kg- 1). The adult knot from Morocco, and all the adults from the past, had concentrations within this range. Compared with them, 30 % of the adult knots, 31 ~o of the godwits from Schiermonnikoog and 12.5% of the godwits from Vlieland had elevated Zn concentrations--up to 977 mg kg -1. No yearly differences could be detected in the feathers from recent years. juveniles
adults
n 20" KNOT
12.
4,
OU~IT
:1 ~J~ 100
REDsANK
, t"l 500
I
100
~
500 900 rag. kg "1 Zn vane
Schi ermonn i koog Vlie~and Morocco museum feathers
Fig. 3. Zinc concentrations in vanes of waders from the Dutch Wadden Sea.
rag. kg-1 As kidney
11 x 9
7
5
3
5
7
9
I'I
1'3
I'5 mg.kg "1 As liver
mg.kg-1 Se kidney
,o
.
j/
3O 10
I'O
3'o
~o
~o
9b
• bar-tailed o redshank × knot
1% "rag. kg-1 Se ,ive,
godwit
Fig. 4. Relationship between liver and kidney concentrations of arsenic and selenium.
mg. kg-1 Se
100-
liver
80-
6040-
x
20-
o I
2
4
=
i
6
8 rag. kg -1 Hg liver
Fig. 5. Relationship between mercury and selenium concentrations in liver (,-o, detection limit of x-co-ordinate; its actual concentration is below this detection limit).
299
Metal in waders
Neither the godwits nor the redshanks from Vlieland and Schiermonnikoog differed significantly from each other with respect to Zn concentrations in the vane. In contrast to the knot and godwit none of the adult redshanks had elevated Zn levels in the vane. On Schiermonnikoog the knot did not differ from the godwit, nor the female from the male godwits.
Organs Liver and kidney concentrations are given in Figs. 4 to 6. In these organs significant positive correlations were found in general (all species involved) between As concentrations in the kidney (Y) and As concentrations in liver (X): Y = 0 . 5 1 X + I . l l (r=0.91; p < 0 . 0 1 ) . Similarly, Se concentration in kidney (Y) was related to Se concentrations in the liver as Y = 0-79X + 0-09 (r = 0.96;p < 0.01) (Fig. 4) and a negative correlation was found between concentrations of Se (Y) liver and Hg liver concentrations (X): Y = - 12.18X + 96.86 (r = 0.82; p < 0-01) (Fig. 5). In calculating the latter equation, Hg concentrations found to be below rag, k 9 -1 Hg shaft
J
~2
q
6
8
rag. kg'lHg
~o
~o
7~
9'o
~.. ~g-~ s..iver
liver
rag. kg-1 Se 15vane
10.
Fig. 6.
Relationship between shaft and liver concentrations of mercury in waders and vane and liver selenium concentrations in the bar-tailed godwit.
300
A..4. Goede
the detection limit were taken as concentrations equal to the detection limit ( = maximum possible concentration). Correlations with feather concentrations were only found in general between Hg shaft (Y) and Hg liver (X) concentrations: Y = 0.64X + 0-87 (r = 0.72; p _<0.02) and for the godwit between Se vane (Y) and Se liver (X) concentrations: Y= 0.09X+ 2-53 (r --- 0-84, p < 0"05) (Fig. 6).
DISCUSSION Feathers/organs
Elevated levels of Hg in feathers were found in adult waders from the Dutch Wadden Sea. In one of the most severe cases of Hg poisoning in birds in history--due to the use of alkyloHg compounds as seed dressings in Sweden--10-20-fold increases in feathershaft concentrations, compared with the natural level, have been reported (Berg et al., 1966). A cautious estimate for knots and redshanks from Schiermonnikoog gives at least a 5-fold--and for the redshanks from Vlieland a 10fold---elevation in concentration. Also, compared with data on Hg concentrations in feathers of other aquatic species, concentrations in some waders from the Dutch Wadden Sea are high. The great crested grebe and the osprey in Sweden have a natural level ofc. 4.5 mg kg- 1 but, during the period of seed dressings use mentioned above, concentrations increased 3-4 fold (Jensen et al., 1972). Levels in breast feathers of some seabirds in Peru did not exceed 2 mg kg- 1 (Gochfeld, 1980). Puffin, manx shearwater and fulmar in Britain had 7-94+0.80, 1.15 +0-06 and 3.34 + 1.49 mg kg- 1, respectively in whole primaries (Osborn et al., 1979) and oystercatcher, herring gull and great skua in Britain, 1.92 + 0.83, 2-84 _+ 0.51 and 6-38 _+ 1.22 mg kg- 1, respectively in whole primaries (Hutton, 1981). No natural levels are provided in these studies. For comparison, the mean whole primary level in the redshank from Vlieland amounted to 11.48 + 4-31 mg kg- 1 Hg concentration in the liver is subject to seasonal fluctuations (Parslow, 1973; Ward, 1978; Osborn, 1979; Evans & Moon, 1981), being highest just prior to moult and lowest just after moult. These authors suggested that uptake and excretion parallels the yearly cycle of the essential element Zn. Bfihler & Norheim (1982) suggested that the deposition of Hg into growing feathers causes a significant reduction of
Metal in waders
301
the Hg content in the body of the bird. Further evidence that incorporation in the feathers is an important way of excretion is provided by Stickel et al. (1977). Results given here are in agreement with this: although feather concentrations are high, liver and kidney concentrations are relatively low just after moult. Hg liver levels of bar-tailed godwits are comparable with those found in waders from Britain sampled in the same season (Parslow, 1973; Evans & Moon, 1981). Those in redshanks are higher. Very little is known about As in birds. Blus et al. (1977) and White et al. (1980) give tissue concentrations. The latter authors reported liver concentrations for wintering shorebirds in industrialized bays in the range 0.02 to 1-20mg kg-1 wet weight, the average being lower than 0.10mgkg -1. Blus et al. (1977) reported similar levels in livers of the brown pelican. In comparison, the liver concentrations reported here are markedly higher, especially in the redshanks. After a diet with 8 mg kg- 1 Se added during 64 weeks, the highest tissue Se concentrations in chickens were found in the feathers: 3-5 mg kg-1 (Arnold et al., 1973). These concentrations are not high compared with those found in waders but the chickens could deposit Se continuously in their eggs. These authors suggest that the feathers may be an important route of excretion for excesses of Se. However, Goede & de Bruin (1984) postulate that the feathers indirectly indicate exposure to Se, by contamination with Se excreted in the feather oils. This will be further investigated. Se organ concentrations reported in the literature are, for livers, 12.8 + 1-3 mg kg- 1 dry weight (oystercatcher), 7.9 + 0.3 mg kg- 1 dry weight (herring gull), 19.7 + 3.1 mg kg-1 dry weight (great skua) (Hutton, 1981); 3.5 +__1.1mg kg -~ wet weight (guillemot)and 3.6mg kg- ~ wet weight (razorbill) (Koeman et al., 1975). Van der Molen et al. (1982) reported similar levels in grey herons and Blus et al. (1977) in brown pelicans. Kidney concentrations reported by Hutton (1981) for the oystercatcher are equal to, and for the other two species twice, the liver concentrations. White et al. (1980) reported 1-3-10.2 mg kg- ~wet weight kidney concentrations in wintering shorebirds. Compared with these data, the liver and kidney Se concentrations of the bar-tailed godwits are extremely high. Data provided here give a negative correlation between Hg and Se in concentrations in the liver. So far, only positive correlations or no correlation have been reported in livers of birds and mammals (Koeman et al., 1975; Martin et al., 1976; Reijnders, 1980; Hutton, 1981 ; Van der
302
A. A. Goede
Molen et al., 1982). Redistribution of Se in the body after moult might be responsible for this relationship: Owing to moulting time differences, the redshanks were sampled two weeks later than the godwits and had much lower Se liver--but, on the other hand, higher Se vane--concentrations. This indicates that Se might have been excreted via the feather oils which contaminated the feathers. In an extensive study into the mineral composition in primaries of geese, Hanson & Jones (1976) reported mean vane Zn concentrations in an average range of 93-164 mg kg-1, the highest concentration reported being 330mg kg -1. Zn concentrations in whole primaries have been frequently reported (Kelsall & Calaprice, 1972; Kellsall et al., 1975a,b; Kellsall & Pannekoek, 1976; Ranta et al., 1978; .Osborn et al., 1979; Scanlon et al., 1979; Hutton, 1981; Howarth et al., 1981, 1982). On average, these concentrations range from c. 80 to 175 mg kg- 1(the lowest being 60 mg kg- 1 (Hutton, 1981), the highest 169 + 15 mg kg- 1 (Kellsall et al., 1975b)), a small range. In comparison, the waders with elevated vane concentrations (>400mg kg -1) have whole primary Zn concentrations of 244 + 26 mg kg- 1 (knot) and 228 + 42 mg kg- 1 (godwit, Schiermonnikoog). These concentrations are still elevated compared with those mentioned above, but confirm the statement of Goede & de Bruin (1984) that, due to the fixed Zn levels in the shaft, whole primaries should not be used as a monitoring tissue, since the portion of the shaft in the featherweight is relatively large, and differences in vane concentrations will thus easily remain undetected.
Toxicological significance Within a relatively short time, waders become heavily contaminated with Hg in the Dutch Wadden Sea. A well known effect of Hg poisoning in birds is decreased reproduction; clutch size, hatchability and mortality of hatchlings are affected (Ljunggren, 1968; Fimreite, 1974; Heinz, 1974; Bednarek et al., 1975; Finley & Stendell, 1978). In spring many waders moult into summer plumage in the Dutch Wadden Sea (Hg might again be excreted via the growing feathers), and accumulate fat before departure to the breeding grounds. Hg concentrations affecting reproduction might be accumulated at this time. Indeed, high Hg levels were found by Lindberg & Odsj6 (1983) in two wader (Tringa) species collected in the summer in N Sweden. They suggest that most of the Hg is picked up during migration and while the birds are wintering in polluted
Metal in waders
303
estuaries in northwestern and southern Europe. Overwintering waders will also accumulate Hg since elimination is slow when the metal cannot be deposited in growing feathers (Stickel et al., 1977). During bad conditions this might prove to be fatal as in the case of grey herons (van der Molen et al., 1982). However, the presence of Se might (partly) neutralize the toxicity of Hg (Ganther et al., 1973). Background As levels in tissues of normal animals are considered to be less than 0-5rag kg -1. Animals dying from acute or subacute As poisoning with tissue levels of 2-10 mg kg- ~ and levels higher than 10 mg kg- 1, all on a wet weight basis, would be considered to be cases which confirm As poisoning. Normal hair values are less than 1 mg kg- 1, those in cases of chronic poisoning, 5 mg kg- ~ and in acute poisoning, 10-30mg kg -1 (Buck, 1978). One of the first symptoms of acute As poisoning in swine is lack of co-ordination of movements (Ledet & Buck, 1978). Compared with these data, godwits have high--and redshanks and knot very high--organ concentrations. Also regarding these data it is suspected that a knot found to be drowned in the nets, and having a liver concentration of 100.5 mg kg- 1 dry weight and a vane concentration of 21.0mgkg -1, died (indirectly--problems of locomotion) due to As poisoning. Se poisoning severely affects reproduction. Laying hens fed 5-9 mg kg-1 for 16 weeks accumulated, on average, 2-3 mg kg-1 in liver and kidney while controls averaged less than 1 mg kg-~. Reproduction was affected; significant decreases occurred in egg weight, egg production and hatchability (Ort & Latshaw, 1978). Arnold et al. (1973) reported similar results. Liver and kidney concentrations in waders exceed 2-3 mg kg- 1; when there is no adaptation to these high concentrations, effects on reproduction might be expected. Selenosis in mammals affects tissues, causing loss of hair and nails and cracked hooves (Harr, 1978). However, malformations in the feathers were not observed in this investigation. Most animal species are tolerant to excessive intake of Zn. Poultry is able to tolerate levels of 1000-2000 mg kg-1 without adverse effects (Ewan, 1978). Therefore, the elevated levels found are not alarming with regard to toxicological effects.
Inter-species differences There are marked differences in prey items taken by the different wader species and between the sexes in the godwit. In the Dutch Wadden Sea
304
A. A. Goede
knot feed mainly on small molluscs, of which Macoma baltica is most common. The redshank feeds on a wider range of invertebrate species, including the polychaete Nereis, small molluscs like Macoma and small crustaceans (amphipods). The bar-tailed godwit's main prey items are large polychaetes, Nereis and Arenicola, the female taking larger specimens than the male (Smit & Wolff, 1981). These differences in diet probably account for the differences in metal contamination. However, the factors involved are complex. For example, in some species of polychaetes, smaller specimens accumulate higher amounts of metals per unit weight than the larger ones (Bryan & Hummerstone, 1973; Ray et al., 1980; Evans & Moon, 1981 (all Nereis), Packer et al. (1980) (Arenicola)); this might explain why the godwits, in particular the females, have the lowest Hg concentrations. Age-related As accumulation does not occur in the polychaete Tharyx marioni: both juvenile and adult worms accumulate remarkable amounts. Whole body concentrations usually exceed 2000 mg kg-1 dry weight (Gibbs et al., 1983). N e r d s also absorbs As, but to different extents in different circumstances (Bryan, 1974). Even short exposure to low concentrations of Hg in the water causes decreased, or even inhibited, burrowing activities in small Macoma, recovery being poor (Eldon et al., 1980); this means higher exposure for Hgoaffected specimens to predators eating the smaller Macoma species. McGreer (1979) reported similar results. And the availability of Zn to Macoma varies with the type of sediment (Luoma & Jenne, 1977); accordingly, exposure to Zn via this prey item will vary with the foraging areas of the wader. Hence, sampling only water, sediment and invertebrates is quite insufficient to assess the impact of pollution in an estuary with an important function in the life cycle of waders. Wadden Sea/river Rhine The trace metal concentrations (in sediments) in the Dutch Wadden Sea decrease in an easterly direction, apparently through the diminishing influence of the river Rhine (Salomons & De Groot, 1978). In some wader species this gradient is also reflected in their Hg and As contamination. For Zn the reverse is found and no explanation can be given for this phenomenon. Discharge of Hg and As decreased in the river Rhine during the last one or two decades, and accordingly As concentrations in the river Rhine sediment have decreased since 1958 to the level which occurred at
Metal in waders
305
the beginning of this century; Hg concentrations, on the other hand, have decreased since 1973 to the level of the middle of this century (Salomons & Eysink, 1981). In 1979-1982 highly elevated levels of these elements in waders from the Dutch Wadden Sea were still measured; the effects of pollution apparently remained detectable for a long time. Zinc levels in the sediment of the Rhine have only decreased slightly in the last decade after an approximately six-fold increase since the beginning of the century (Salomons & Eysink, 1981). Data on Se are not available. ACKNOWLEDGEMENTS I am grateful to Dr E. Nieboer, who loaned the bird trapping facilities of the Vrije Universiteit, Amsterdam on Schiermonnikoog. The Rijks Universiteit, Groningen, is thanked for providing lodging on Schiermonnikoog. Skilful field assistants were W. Tamis, P. M. Zegers, D. Tensen and T. M. van der Have. Feathers from skins were kindly provided by Dr Wattel, Zoological Museum, University of Amsterdam, from Vlieland by Dr G. C. Boere, P. M. Zegers and the Institute for Environmental Studies and from Morocco by the members of the Netherlands Morocco Expedition (1982). The Institute for Environmental Studies, Vrije Universiteit, Amsterdam, offered laboratory facilities and the Interuniversity Reactor Institute, Delft, made the analysis possible, thanks to the assistance of Dr ir. M. de Bruin and A. Dijkstra. Dr W. J. Wolff and Drs P. de Voogt made helpful comments on the manuscript, LASOM financed the project. Without all these valuable contributions, this study would not have been possible. REFERENCES Arnold, R. L., Olson, O. E. & Carlson, C. W. (1973). Dietary selenium and arsenic additions and their effects on tissue and egg selenium. Poultry Sci., 52, 847-54. Ashmole, N. P. (1962). The black noddy Anous tenuirostris on Ascension Island. Ibis, 103b, 235-319. Bednarek, W., Hausdorf, W., J6rissen, U., Schulte, E. & Wegener, H. (1975). Uber die Auswirkungen der chemischen Umweltbelastung auf Greifv6gel in zwei Probefl~ichen Westfalens J. Orn., 116, 181-94. Berg, W., Johnels, A., Sj6strand, B. & Westermark, T. (1966). Mercury content in feathers of Swedish birds from the past 100 years. Oikos, 17, 71-83.
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Blus, L. J., Neely, B. S., Lamont, T. G. & Mulhern, B. (1977). Residues of organochlorines and heavy metals in tissues and eggs of brown pelicans, 1969-73. Pestic. Monit. J., 11, 40-53. Boere, G. C. (1976). The significance of the Dutch Waddenzee in the annual life cycle of arctic, subarctic and boreal waders Part 1. The function as a moulting area. Ardea, 64, 210-91. Boere, G. C. & Smit, C. J. (1981). Knot. Bar-tailed godwit, Redshank. In Birds of the WaddenSea, ed. byC. J. Smit and W. J. Wolff, 136-45, 170-9, 195-206. Rotterdam, Balkema. Bryan, G. W. (1974). Adaptation of an estuarine polychaete to sediments containing high concentrations of heavy metals. In Pollution and physiology of marine organisms, ed. by F. J. Vernberg and W. B. Vernberg, 123-35, New York, Academic Press. Bryan, G. W. & Hummerstone, L. G. (1973). Adaptation of the polychaete Nereis diversicolor to estuarine sediments containing high concentrations of zinc and cadmium. J. mar. biol. Ass. UK, 53, 839-57. Buck, W. B. (1978). Toxicity of inorganic and aliphatic organic arsenicals. In Toxicity of heavy metals in the environment, ed. by F. W. Oehme, Part 1, 357-74. New York, M. Dekker. Biihler, U. & Norheim, G. (1982). The mercury content in feathers of the sparrowhawk Accipiter nisus in Norway. Fauna norv. Ser. C. Cinclus, 5, 43-6. de Bruin, M. & Korthoven, P. J. M. (1972). Computer oriented system for nondestructive neutron activation analysis. Analyt. Chem. 44, 2382-5. de Bruin, M., Korthoven, P. J. M. & Bode, P. (1982). Evaluation of a system for routine instrumental neutron activation analysis. J. Radiat. analyt. Chem. 70(1-2), 497-512. Dick, W. J. A. (ed.) (1975). Oxjord and Cambridge Mauretanian expedition, 1973. Report. Cambridge, W. J. A. Dick. Dick, W. J. A., Pienkowski, M. W., Waltner, M. & Minton, C. D. T. (1976). Distribution and geographical origins of knot Calidris canutus wintering in Europe and Africa. Ardea, 64, 22-47. Eldon, J., Pekkarinen, M. & Kristoffersson, R. (1980). Effects of low concentrations of heavy metals on the bivalve Macoma baltica. Ann. Zool. Fennici, 17, 233-42. Essink, K. (1980). Mercury pollution in the Ems estuary. Helgol. Wiss. Meeresunters., 33, 111-21. Evans, P. R. & Moon, S. J. (1981). Heavy metals in shore birds and their prey. In Heavy metals in Northern England." Em, ironmental and biological aspects. ed. by P. J. Say and B. A. Whitton, 181-90. University of Durham. Ewan, R. C. (1978). Toxicology and adverse effects of mineral imbalance with emphasis on selenium and other minerals. In Toxicity of heavy metals in the environment, ed. by F. W. Oehme, Part 1,445-89. New York, M. Dekker. Fimreite, N. (1974). Mercury contamination of aquatic birds in northwestern Ontario. J. Wildl. Mgmt, 38, 120-31. Finley, M. T. & Stendell, R. C. (1978). Survival and reproductive success of black ducks fed methyl mercury. Environ. Pollut., 16, 51 64.
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Ganther, H. E., Wagner, P. A., Sunde, M. L. & Hoekstra, W. G. (1973). Protective effects of selenium against heavy metal toxicities. In Trace substances in environmental health, ed. by D.D. Hemphill, 247-52. Columbia, University of Missouri. Gibbs, P. E., Langston, W. J., Burt, G. R. & Pascoe, P. L. (1983). Tharyx marioni (Polychaeta): A remarkable accumulator of arsenic. J. mar. biol. Ass. UK, 63, 313-25. Gochfeld, M. (1980). Mercury levels in some seabirds of the Humboldt current, Peru. Era,iron. Pollut. (Ser. A), 22, 197-205. Goede, A. A. & de Bruin, M. (1984). The use of bird feather parts as a monitor for metal pollution. Environ. Pollut., Set. B, 8(4), 281-98. Hanson, H. C. & Jones, R. L. (1976). The biogeochemistry of blue, snow and Ross' geese. Spec. Pubis Illinois Nat. Hist. Surv., no. 1. Urbana, Illinois. Harr, J. R. (1978). Biological effects of selenium. In Toxicity of heavy metals in the environment, ed. by F. W. Oehme, Part 1, 393-426. New York, M. Dekker. Heinz, G. (1974). Effects of low dietary levels of methyl mercury on mallard reproduction. Bull. environ. Contain & Toxicol., 11, 386-92. Howarth, D. M., Hulbert, A. J. &Horning, D. (1981). A comparative study of heavy metal accumulation in tissues of the crested tern, Sterna bergii, breeding near industrialized and non-industrialized areas. Austr. Wildl. Res., 8, 665-72. Howarth, D. M., Grant, T. R. & Hulbert, A. J. (1982). A comparative study of heavy metal accumulation in tissues of the crested tern, Sterna bergii, breeding near an industrial port before and after harbour dredging and ocean dumping. Austr. Wildl. Res., 9, 571-7. Hutton, M. (1981). Accumulation of heavy metals and selenium in three seabird species from the United Kingdom. Era,iron. Pollut. (Ser. A), 26, 129-45. Jensen, S., Johnels, A. G., Olsson, M. & Westermark, T. (1972). The avifauna of Sweden as indicators of environmental contamination with mercury and chlorinated hydrocarbons. In Proc. int. Orn. Congr., 15th, Leiden, 455-65. Kelsall, J. P. & Calaprice, J. R. (1972). Chemical content of waterfowl plumage as a potential diagnostic tool. J. Wildl. Mgmt., 36, 1088-97. Kelsall, J. P., Pannekoek, W. J. (1976). The mineral profile of plumage in captive lesser snow geese. Can. J. Zool., 54, 301-5. Kelsall, J. P., Pannekoek, W. J. & Burton, R. (1975a). Chemical variability in plumage of wild lesser snow geese. Can. J. Zool., 53, 1369-75. Kelsall, J. P., Pannekoek, W. J. & Burton, R. (1975b). Variability in the chemical content of waterfowl plumage. Can. J. Zool., 53, 1379-86. Koeman, J. H. (1971). Het voorkomen en de toxicologische betekenis van enkele chloorkoolwaterstoffen aan de Nederlandse kust in de periode van 1965-1970. Ph.D thesis, Utrecht University. Koeman, J. H., van de Ven, W. S. M., Goeij, J. J. M., Tjioe, P. S. & van Haaften, J. L. (1975). Mercury and selenium in marine mammals and birds. Sci. Total. Environ., 3, 279-87. Ledet, A. E. & Buck, W. B. (1978). Toxicity of organic arsenicals in feedstuffs. In
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Toxicity of heavy metals in the environment, ed. by F. W. Oehme, Part 1, 375-92. New York, M. Dekker. Lindberg, P. & Odsj6, T. (1983). Mercury levels in feathers of peregrine falcon Falco peregrinus compared with total mercury content in some of its prey species in Sweden. Environ. Pollut. (Ser. B), 5, 297-318. Ljunggren, L. (1968). The influence of mercury poisoning on the reproduction and general health of wood pigeons. Viltrevy, 5, 423-31. Luoma, S. N. & Jenne, E. A. (1977). The availability of sediment-bound cobalt silver and zinc to a deposit-feeding clam. In Biological implications of metals in the environment. Proc. Ann. Hanford Life Sci. Symp., 15th, ed. by H. Drucker and R. E. Wildung. Martin, J. H., Elliott, P. D., Andenlini, V. C., Girvin, D., Jacobs, S. A., Risebrough, R. W., Delong, R. L. & Gilmartin, W. G. (1976). Mercury-selenium-bromine imbalance in premature parturient California sea lions. Mar. Biol., 35, 91-104. McGreer, E. R. (1979). Sublethal effects of heavy metal contaminated sediments on the bivalve Macoma baltiea (L.). Mar. Pollut. Bull., 10, 259-62. Ort, J. F. & Latshaw, J. D. (1978). The toxic level of sodium selenite in the diet of laying chickens. J. Nutr., 108, 1114-20. Osborn, D. (1979). Seasonal changes in the fat, protein and metal content of the liver of the starling Sturnus vulgaris. Environ. Pollut., 19, 145-55. Osborn, D., Harris, M. P. & Nicholson, J. K. (1979). Comparative tissue distribution of mercury, cadmium and zinc in three species of pelagic seabirds. Comp. Biochem. Physiol., 64C, 61-7. Packer, D. M., Ireland, M. P. & Wootton, R. J. (1980). Cadmium, copper, lead, zinc and manganese in the polychaete Arenicola marina from sediments around the coast of Wales. Environ. Pollut. (Set. A), 22, 309-21. Parslow, J. L. F. (1973). Mercury in waders from the Wash. Environ. Pollut., 5, 295-304. Ranta, W. B., Tomassini, F. D. & Nieboer, E. (1978). Elevation of copper and nickel levels in primaries from black and mallard ducks collected in the Sudbury district, Ontario. Can. J. Zool., 56, 581-6. Ray, S., McLeese, D. & Pezzack, D. (1980). Accumulation of cadmium by Nereis virens. Arch. environ. Contam. & Toxicol., 9, 1-8. Reijnders, P. J. H. (1980). Organochlorine and heavy metal residues in harbour seals from the Wadden Sea and their possible effects on reproduction. Neth. J. Sea Res., 14, 30-65. Salomons. W. & de Groot, A. J. (1978). Pollution history of trace metals in sediments, as affected by the Rhine river. In Environmental biogeochemistry and geomicrobiology, ed. by W.E. Krumbein, 1, 140-64. Ann Arbor, Ann Arbor Science. Salomons, W. & Eysink, W. D. (1981). Pathways of mud and particulate metals from rivers to the southern North Sea. In Biogeochemical and hydrodynamic processes affecting heavy metals in rivers, lakes and estuaries. Pubis Delft Hydraulics Laboratory, no. 253. Scanlon, P. F., O'Brien, T. G., Schauer, N. L., Coggin, J. L. & Steffen, D. E.
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(1979). Heavy metal levels in feathers of wild turkeys from Virginia. Bull: environ. Contam. & Toxicol., 21, 591-5. Smit, C. & Wolff, W. J. (eds.) (1981). Birds of the Wadden Sea. Rotterdam, Balkema. Stickel, L. F., Stickel, W. H., McLane, M. A. R. & Bruns, M. (1977). Prolonged retention of methyl mercury by mallard drakes. Bull. environ. Contain. & Toxicol., 18, 393-400. van der Molen, E. J., Blok, A. A. de Graaf, G. J. (1982). Winter starvation and mercury intoxication in grey herons (Ardea cinerea) in the Netherlands. Ardea, 70, 173-84. Ward, P. (1978). Heavy metals in waders. ITE report 56-57. Cambridge, Institute of Terrestrial Ecology. White, D. H., King, K. A. & Prouty, R. M. (1980). Significance of organochlorine and heavy metal residues in wintering shore birds at Corpus Christi, Texas, 1976-77. Pestic. Monit. J. 14, 58-63.
Mercury, Selenium, Arsenic and Zinc in Waders from The Dutch Wadden Sea
A. A. G o e d e Research Institute for Nature Management, Texel, The Netherlands
ABSTRACT In the Dutch Wadden Sea, a major post-nuptial moulting area for waders, three wader species were investigated )br metal contamination using mainly the feathers as monitoring tissue. All four elements--mercury, arsenic, selenium and zinc--were detected at sometimes highly elevated levels. The implications are discussed.
INTRODUCTION In the years 1964-1966 high mortality among several bird species made it painfully clear that the river Rhine (and Meuse) does not end where it meets the North Sea. Part of it continues as a 'coastal river' and deposits a considerable amount of its load in a large estuarine area, 100-150 km to the n o r t h - - t h e Wadden Sea. In those years the pesticides telodrin and dieldrin were discharged into the river: as a result, in the Dutch Wadden Sea the sandwich tern Sterna sandvicensis came close to extinction (Koeman, 1971). Also, other pollutants carried by the rivers--heavy metals and PCBs--give cause for concern. Although the discharge of some heavy metals has been reduced in the last 10-15 years, it has not ended. The long-term effects of chronic low exposures to these discharges on the estuarine ecosystems are unknown. Recently, elevated levels of 287
Environ. Pollut. Ser. A. 0143-1471/85/$03-30 © Elsevier Applied Science Publishers Ltd, England, 1985. Printed in Great Britain
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mercury have been reported in two vertebrate species in the Wadden Sea: the harbour seal Phoca vitulina (Reijnders, 1980) and the eelpout Zoarces viviparus (Essink, 1980). Regarding PCBs, it is suspected that the high concentrations found in the harbour seals from the Dutch Wadden Sea correlate with the seal's strongly decreased reproductive success (Reijnders, 1980). It has become clear, particularly in the last decade, that the Wadden Sea has a very important function as a moulting area for many bird species, especially for large numbers of waders at the time of the postnuptial moult (Boere, 1976). Large percentages of the world population of some wader species are dependent on the Wadden Sea in this respect (Smit & Wolff, 1981). These waders are at the end of a food chain. Because of this, it is of the utmost importance to know to what extent these birds are exposed to pollution in this area. Therefore, an investigation into the metal and PCB contamination of waders during the post-nuptial moult in the Dutch Wadden Sea has been initiated. This paper gives the results concerning mercury, selenium, arsenic and zinc.
MATERIALS AND METHODS The metal contamination of waders in the Dutch Wadden Sea was investigated using the primaries formed in this area as a monitoring tissue. During post-nuptial moult the adult waders renew the whole plumage; the first calender year birds (from now on called juveniles) retain the primaries formed on the breeding grounds. The breeding grounds of the investigated species are remote: the knot Calidris canutus population moulting in the Wadden Sea breeds in Greenland and NE Canada; the bar-tailed godwit Limosa lapponica on the Taymyr peninsula in Siberia and the Icelandic redshank Tringa totanus robusta on Iceland (Boere & Smit, 1981). It may be assumed that the exposure to metal pollution is negligible in these areas. The concentrations of metals in juvenile primaries formed on the breeding grounds, together with concentrations in primaries from museum specimens (1900-1930 and 1960-1970 collections) and a primary from a knot sampled in Morocco in the spring of 1982, were used to compare concentrations in recently formed primaries in the Dutch Wadden Sea.
289
Metal in waders
Sampling The juvenile primaries, as well as newly formed adult No. 8 primaries, were collected in the autumns of 1979-1982. The birds were trapped by mist-netting in the eastern part of the Dutch Wadden Sea, near the island of Schiermonnikoog, and in the western part, near the island of Vlieland (Fig. l). On Schiermonnikoog it was possible to collect enough adult redshank and male bar-tailed godwit feathers to compare different years. Primaries No. 8 from specimens were obtained from the collection of the Zoological Museum, Amsterdam, the preserved skins having been treated with an arsenic compound. These birds had been collected in, or near, the Dutch Wadden Sea; however, some collection dates were in May Danish Wadden
Gefrnor1"-_ Dutchi
Fig. 1. Location of the Dutch Wadden Sea (1, mouth of the river Rhine; 2, island of Vlieland; 3, island of Schiermonnikoog).
290
A. A, Goede
(spring migration). In these cases it is uncertain where the primaries had been formed the previous autumn. The godwits were all collected in May; hence their feathers had been formed on the west coast of Africa or in NW Europe. Three of the five adult knots were also collected in May. According to the biometrical measurements one probably belonged to the Greenland/Canada breeding population moulting in NW Europe with the Wadden Sea as the most important area, the other two to the Siberian breeding population mainly (post-nuptial) moulting in Africa (Dick, 1975; Dick et al., 1976). Their concentrations will be given separately in the 'Results' section, the latter being referred to as 'Siberian' knot. To avoid contamination surgical gloves were worn when the feathers were pulled out and individually put into labelled plastic bags. As described by Goede & de Bruin (1984) the following feather parts were used as a monitoring tissue: the vane for Zn and Se and the shaft for Hg and As. When vanes are to be used as tissue indicating exposure of the bird to Se, the time since the formation of the feather has to be known since the vane accumulates Se with time (Goede & de Bruin, 1984). While collecting the feathers it was observed that primary No. 8 is fully grown (no blood in the end of the quill) when primary No. 10 is at the growing stage 4, i.e. when the total primary moult score was 49 (according to Ashmole, 1962). In the 'Results' section the time since completion of No. 8 is given as the time since primary moult score 49 (Boere, 1976). The feather needs 1 to 1.5 months to grow. In addition, some birds which recently completed the growth of the primary No. 8 were sacrificed (suffocated in ether), to determine liver and kidney concentrations (godwits, 0-2 weeks and redshanks, 2-4 weeks after completion). Having initially been stored at - 1 8 °C, they were eventually stored at - 6 0 °C in the laboratory.
Sample analysis All laboratory material involved in handling and storage of the samples was rinsed once with 1:1 concentrated HNO 3 and four times with deionized water. Prior to analysis the feathers were shaken in deionized water for 1 min to remove superficial contamination and dried at 60 °C for 30 min. The vane was clipped from the shaft with stainless steel scissors. The metal concentrations were measured by means of instrumental neutron activation analysis, using the IRI system for routine analysis,
Metal in waders
291
described in detail elsewhere (de Bruin & Korthoven, 1972; de Bruin et al., 1982; Goede & de Bruin, 1984). Prior to analysis, livers and kidneys were freeze-dried for 70 h. A part of the liver was lipid extracted by repeated washing with hexane for 2 h in a Soxhlet apparatus. The loss of weight of the sample was considered to be the lipid content. Percentages of water in these organs and fat content of the liver are given in Table 1. TABLE 1 Percentages o f W a t e r a n d F a t in Liver a n d Kidney
Godwit Redshank
Weight % H20 liver
Weight % H20 kidney
Weight % fat dry liver
n
71"34 +_ 0'78 71.07 + 0-59
75'91 _ 1.07 75.51 +_ 0.29
9"96 _ 3"04 6-73 + 1.33
10 3
Metal concentrations of the liver are given in mg kg- 1 lean dry weight and kidney concentrations in mg kg-1 dry weight. In the 'Results' section mean values are given, together with standard deviations.
RESULTS
Mercury--shaft (Table 2) All juveniles, both museum specimens and trapped birds, had low Hg concentrations in the shaft; godwits significantly lower than knots and redshanks (Wilcoxon-two-tailed test, p < 0.01). Adult godwits from the museum collections, 'Siberian' knots from museum collections and a knot from 1930 had comparable levels. Compared with them, all recent adults, both from Schiermonnikoog and Vlieland, had elevated Hg levels in the shaft, most pronounced in the redshanks from Vlieland. The two adult knots from the 1960s also had elevated levels, comparable with those found in recent years. The redshank from Schiermonnikoog had significantly higher concentrations in 1979 (7.84 ___1.14mg kg-1, n = 10) than in 1980-1981
TABLE 2
20 2
3.12 __+0-06 0.38 + 0-14
D e t e c t i o n limit
2 1 2
0-57 ___0.31 0-41 5.01 + 1.75 5.76 + 1.68
4 27
0.69 + 0.25 0.94 _ 0.48
n
Adults, 1979-1982, Schiermonnikoog Vlieland
Juveniles, 1927 1969 Juveniles, 1979-1982 A d u l t B-t godwit, 1904-1963 A d u l t Sib. k n o t , 1931-1982 A d u l t , 1930 A d u l t s , 1964 ( M a y bird) - 1 9 6 9
Knot
7
--
--
1 ---
-6
nND
10.26 ___3.78
6.54 + 1.88
1-07 ± 0.35
Redshank
5
20
10
n
--
--
nND
10 19 5 3
4.89 + 0.97 0.14 + 0-09
4 4
n
1-96 + 0-41 2.50 __+0.95 3-67 + 2.00
0.29 + 0.20 0.43 + 0.23
Bar-tailed godwit
-7
----
6 1
nND
~/3'
~_/~
M e r c u r y C o n c e n t r a t i o n s in F e a t h e r S h a f t s o f W a d e r s (in m g kg 1 ; n, n u m b e r w i t h d e t e c t a b l e c o n c e n t r a t i o n s ; n N D , n u m b e r with n o d e t e c t a b l e c o n c e n t r a t i o n s ; n + N D , t o t a l s a m p l e size)
e~
Metal in waders
293
(5.23+ 1.54mgkg -1, n = 10) (p<0-01). Male godwits from Schiermonnikoog did not differ significantly in the subsequent years, 1980 and 1981. Redshanks and female godwits from Vlieland had significantly higher Hg levels than their congeners from Schiermonnikoog (p <0.02); the male godwits showed the same trend. On Schiermonnikoog redshanks and knots had significantly higher Hg concentrations in the shaft than godwits (p < 0.02). In 1979 redshanks also had significantly higher concentrations than knots (p < 0.01). Also on Vlieland, redshanks had significant higher levels than godwits (p < 0.02). The male godwits did not differ significantly from the females.
Arsenic
shaft (Table 3)
All but one juvenile had no detectable amounts of As in the shaft. Compared with them, the adults from the Wadden Sea had elevated levels. Significant differences in concentrations in the different sampling years were found in redshanks and male godwits from Schiermonnikoog, concentrations being higher in the earlier years. The redshanks had higher concentrations in 1979 than in 1980-1981 (p < 0.01), those from 1980 and 1981 did not differ from each other; the male godwits had higher concentrations in 1980 than in 1981 (4 out of 9 having no detectable concentrations, p < 0-02). Female godwits from Vlieland had higher As shaft concentrations than those from Schiermonnikoog (only a weak significance: p < 0.10, since one Vlieland bird had an undetectable concentration--however, its detection limit was relatively high, 1.01 mg kg-1). The redshank data from Vlieland were scattered. Knots from Schiermonnikoog in 1979 had significantly lower As concentrations in the shaft than the redshanks from the same year and location. No significant differences were found between female and male godwits.
Selenium--vane (Table 4) After arrival in the Wadden Sea, juvenile knots (Goede & de Bruin, 1984) and redshanks (Fig. 2) rapidly accumulated Se in the vane. Concentrations in the juvenile feathers from museum specimens did not
TABLE
3
0"49 + 0-07 0'18 + 0"29
Detection limit
--
1"03_+0.59
Juveniles, 1979-1982 Adults, Schiermonnikoog 1979 1980 (1980-1981 R e d s h a n k ) 1981 Vlieland, 1979-1982
Knot
17
n
17
14 3
nND
0"15_+0.21
5
9
0-60__+0-23 1 ' 6 3 + 1.07
1 10
n
0"78 1.46 __+0"37
Redshank
9
--
1
8 -
nND
0-56 __+0-26 0-51 ___0"10 0-47+0.17 3-17+0.93 0"87 ___0'48 0.11 + 0 " 2 4
--
Bar-tailed godwit
Arsenic C o n c e n t r a t i o n s in F e a t h e r Shafts o f W a d e r s (Definitions as in Table 2)
9 10 5 4 3
--
n
1 -4 1 -16
10
nND
3
~/(3
~/~
¢3
D e t e c t i o n limit
2-4 weeks
0-2 weeks after a r r i v a l in t h e W a d d e n Sea A d u l t B-t godwit, 1904 1963 6-7 months A d u l t Sib. k n o t . 1930 1982 5-7 months Adult, 1930-1969 1-4 months A d u l t , 1964 7 months Adults, 1979-1982 0-2 weeks Schiermonnikoog 2-4 weeks Vlieland 0-2 weeks
Juveniles, 1927-1982
Time since completion o f the feather
3 2 1 20
2
4.33 + 0.97 2 1 . 2 3 + 1.18 53.96 15.72_+_5.32
18.33+2.90
1-80 + 0.97
8
n
3 . 6 8 _ 1.02
Knot
14
--
-----
14
nND
13-82 + 3.06
12.94+__4.11 8 - 7 4 + 1.51
3-43 + 1.02
Redshank
3
18 2
4
n
--
---
--
nND
0.81 +- 0.15
5.65___ 1-98 7-24 _+ 0.94
7.45 + 1.62 9 . 5 9 + 1"79
-5.38 _ 3.82
Bar-tailed godwit
TABLE 4 S e l e n i u m C o n c e n t r a t i o n s in F e a t h e r V a n e s o f W a d e r s ( D e f i n i t i o n s as in T a b l e 2)
5 3
10 19
-5
n
6
---
---
6 --
nND
2/ff
~-/~
L~
2
296
A. A. Goede rag. kg "1 Se Vane
30KNOT 2520 15. 10-
• ° o
5-
ND aug
'
sept
OCt
nov
rag. k g ' l Se
20 -
REDSHANK
Vane
15_ 10_ 5-
ND i
aug
sept
oct
nov
®museum feathers 1927-1928 o museum feathers 1966-1969
Fig. 2.
Selenium concentrations in the vanes of juvenile knots and redshanks with time (ND, vane with concentration below the detection limit).
differ from those found in juvenile feathers from recent times (Fig. 2). No increase in concentrations was found in juvenile godwit vanes (at the end of September all were below the detection limit (n = 6), as at the beginning of November (n = 4). However, very little is known about their migration. It is not unlikely that the November birds belonged to a group arriving later, while the first ones had left for the African wintering grounds, as do a large percentage of the adults (Boere & Smit, 1981). Just after arrival of the juveniles in the Wadden Sea relatively low or undetectable concentrations were found in vanes formed on the breeding grounds. Also relatively low concentrations were found in the vanes of the Siberian knots, even many months after the formation was completed. In contrast, feathers formed in the Wadden Sea had elevated levels in only a few weeks after formation. The knot feather from a bird collected in November 1930 on Schiermonnikoog also had an elevated level shortly after its formation.
297
Metal in waders
No yearly differences were found in recent feathers. On Schiermonnikoog the female godwits had a significantly lower level than the males (p < 0.01), the same trend being seen on Vlieland. Clearly, the knot had the most contaminated feather vanes. Zinc--vane (Fig. 3) In all juveniles from past and present samples, the range of vane Zn concentrations amounted to 100-400 mg kg-1 (one extreme value in the redshank: 686 mg kg- 1). The adult knot from Morocco, and all the adults from the past, had concentrations within this range. Compared with them, 30 % of the adult knots, 31 ~o of the godwits from Schiermonnikoog and 12.5% of the godwits from Vlieland had elevated Zn concentrations--up to 977 mg kg -1. No yearly differences could be detected in the feathers from recent years. juveniles
adults
n 20" KNOT
12.
4,
OU~IT
:1 ~J~ 100
REDsANK
, t"l 500
I
100
~
500 900 rag. kg "1 Zn vane
Schi ermonn i koog Vlie~and Morocco museum feathers
Fig. 3. Zinc concentrations in vanes of waders from the Dutch Wadden Sea.
rag. kg-1 As kidney
11 x 9
7
5
3
5
7
9
I'I
1'3
I'5 mg.kg "1 As liver
mg.kg-1 Se kidney
,o
.
j/
3O 10
I'O
3'o
~o
~o
9b
• bar-tailed o redshank × knot
1% "rag. kg-1 Se ,ive,
godwit
Fig. 4. Relationship between liver and kidney concentrations of arsenic and selenium.
mg. kg-1 Se
100-
liver
80-
6040-
x
20-
o I
2
4
=
i
6
8 rag. kg -1 Hg liver
Fig. 5. Relationship between mercury and selenium concentrations in liver (,-o, detection limit of x-co-ordinate; its actual concentration is below this detection limit).
299
Metal in waders
Neither the godwits nor the redshanks from Vlieland and Schiermonnikoog differed significantly from each other with respect to Zn concentrations in the vane. In contrast to the knot and godwit none of the adult redshanks had elevated Zn levels in the vane. On Schiermonnikoog the knot did not differ from the godwit, nor the female from the male godwits.
Organs Liver and kidney concentrations are given in Figs. 4 to 6. In these organs significant positive correlations were found in general (all species involved) between As concentrations in the kidney (Y) and As concentrations in liver (X): Y = 0 . 5 1 X + I . l l (r=0.91; p < 0 . 0 1 ) . Similarly, Se concentration in kidney (Y) was related to Se concentrations in the liver as Y = 0-79X + 0-09 (r = 0.96;p < 0.01) (Fig. 4) and a negative correlation was found between concentrations of Se (Y) liver and Hg liver concentrations (X): Y = - 12.18X + 96.86 (r = 0.82; p < 0-01) (Fig. 5). In calculating the latter equation, Hg concentrations found to be below rag, k 9 -1 Hg shaft
J
~2
q
6
8
rag. kg'lHg
~o
~o
7~
9'o
~.. ~g-~ s..iver
liver
rag. kg-1 Se 15vane
10.
Fig. 6.
Relationship between shaft and liver concentrations of mercury in waders and vane and liver selenium concentrations in the bar-tailed godwit.
300
A..4. Goede
the detection limit were taken as concentrations equal to the detection limit ( = maximum possible concentration). Correlations with feather concentrations were only found in general between Hg shaft (Y) and Hg liver (X) concentrations: Y = 0.64X + 0-87 (r = 0.72; p _<0.02) and for the godwit between Se vane (Y) and Se liver (X) concentrations: Y= 0.09X+ 2-53 (r --- 0-84, p < 0"05) (Fig. 6).
DISCUSSION Feathers/organs
Elevated levels of Hg in feathers were found in adult waders from the Dutch Wadden Sea. In one of the most severe cases of Hg poisoning in birds in history--due to the use of alkyloHg compounds as seed dressings in Sweden--10-20-fold increases in feathershaft concentrations, compared with the natural level, have been reported (Berg et al., 1966). A cautious estimate for knots and redshanks from Schiermonnikoog gives at least a 5-fold--and for the redshanks from Vlieland a 10fold---elevation in concentration. Also, compared with data on Hg concentrations in feathers of other aquatic species, concentrations in some waders from the Dutch Wadden Sea are high. The great crested grebe and the osprey in Sweden have a natural level ofc. 4.5 mg kg- 1 but, during the period of seed dressings use mentioned above, concentrations increased 3-4 fold (Jensen et al., 1972). Levels in breast feathers of some seabirds in Peru did not exceed 2 mg kg- 1 (Gochfeld, 1980). Puffin, manx shearwater and fulmar in Britain had 7-94+0.80, 1.15 +0-06 and 3.34 + 1.49 mg kg- 1, respectively in whole primaries (Osborn et al., 1979) and oystercatcher, herring gull and great skua in Britain, 1.92 + 0.83, 2-84 _+ 0.51 and 6-38 _+ 1.22 mg kg- 1, respectively in whole primaries (Hutton, 1981). No natural levels are provided in these studies. For comparison, the mean whole primary level in the redshank from Vlieland amounted to 11.48 + 4-31 mg kg- 1 Hg concentration in the liver is subject to seasonal fluctuations (Parslow, 1973; Ward, 1978; Osborn, 1979; Evans & Moon, 1981), being highest just prior to moult and lowest just after moult. These authors suggested that uptake and excretion parallels the yearly cycle of the essential element Zn. Bfihler & Norheim (1982) suggested that the deposition of Hg into growing feathers causes a significant reduction of
Metal in waders
301
the Hg content in the body of the bird. Further evidence that incorporation in the feathers is an important way of excretion is provided by Stickel et al. (1977). Results given here are in agreement with this: although feather concentrations are high, liver and kidney concentrations are relatively low just after moult. Hg liver levels of bar-tailed godwits are comparable with those found in waders from Britain sampled in the same season (Parslow, 1973; Evans & Moon, 1981). Those in redshanks are higher. Very little is known about As in birds. Blus et al. (1977) and White et al. (1980) give tissue concentrations. The latter authors reported liver concentrations for wintering shorebirds in industrialized bays in the range 0.02 to 1-20mg kg-1 wet weight, the average being lower than 0.10mgkg -1. Blus et al. (1977) reported similar levels in livers of the brown pelican. In comparison, the liver concentrations reported here are markedly higher, especially in the redshanks. After a diet with 8 mg kg- 1 Se added during 64 weeks, the highest tissue Se concentrations in chickens were found in the feathers: 3-5 mg kg-1 (Arnold et al., 1973). These concentrations are not high compared with those found in waders but the chickens could deposit Se continuously in their eggs. These authors suggest that the feathers may be an important route of excretion for excesses of Se. However, Goede & de Bruin (1984) postulate that the feathers indirectly indicate exposure to Se, by contamination with Se excreted in the feather oils. This will be further investigated. Se organ concentrations reported in the literature are, for livers, 12.8 + 1-3 mg kg- 1 dry weight (oystercatcher), 7.9 + 0.3 mg kg- 1 dry weight (herring gull), 19.7 + 3.1 mg kg-1 dry weight (great skua) (Hutton, 1981); 3.5 +__1.1mg kg -~ wet weight (guillemot)and 3.6mg kg- ~ wet weight (razorbill) (Koeman et al., 1975). Van der Molen et al. (1982) reported similar levels in grey herons and Blus et al. (1977) in brown pelicans. Kidney concentrations reported by Hutton (1981) for the oystercatcher are equal to, and for the other two species twice, the liver concentrations. White et al. (1980) reported 1-3-10.2 mg kg- ~wet weight kidney concentrations in wintering shorebirds. Compared with these data, the liver and kidney Se concentrations of the bar-tailed godwits are extremely high. Data provided here give a negative correlation between Hg and Se in concentrations in the liver. So far, only positive correlations or no correlation have been reported in livers of birds and mammals (Koeman et al., 1975; Martin et al., 1976; Reijnders, 1980; Hutton, 1981 ; Van der
302
A. A. Goede
Molen et al., 1982). Redistribution of Se in the body after moult might be responsible for this relationship: Owing to moulting time differences, the redshanks were sampled two weeks later than the godwits and had much lower Se liver--but, on the other hand, higher Se vane--concentrations. This indicates that Se might have been excreted via the feather oils which contaminated the feathers. In an extensive study into the mineral composition in primaries of geese, Hanson & Jones (1976) reported mean vane Zn concentrations in an average range of 93-164 mg kg-1, the highest concentration reported being 330mg kg -1. Zn concentrations in whole primaries have been frequently reported (Kelsall & Calaprice, 1972; Kellsall et al., 1975a,b; Kellsall & Pannekoek, 1976; Ranta et al., 1978; .Osborn et al., 1979; Scanlon et al., 1979; Hutton, 1981; Howarth et al., 1981, 1982). On average, these concentrations range from c. 80 to 175 mg kg- 1(the lowest being 60 mg kg- 1 (Hutton, 1981), the highest 169 + 15 mg kg- 1 (Kellsall et al., 1975b)), a small range. In comparison, the waders with elevated vane concentrations (>400mg kg -1) have whole primary Zn concentrations of 244 + 26 mg kg- 1 (knot) and 228 + 42 mg kg- 1 (godwit, Schiermonnikoog). These concentrations are still elevated compared with those mentioned above, but confirm the statement of Goede & de Bruin (1984) that, due to the fixed Zn levels in the shaft, whole primaries should not be used as a monitoring tissue, since the portion of the shaft in the featherweight is relatively large, and differences in vane concentrations will thus easily remain undetected.
Toxicological significance Within a relatively short time, waders become heavily contaminated with Hg in the Dutch Wadden Sea. A well known effect of Hg poisoning in birds is decreased reproduction; clutch size, hatchability and mortality of hatchlings are affected (Ljunggren, 1968; Fimreite, 1974; Heinz, 1974; Bednarek et al., 1975; Finley & Stendell, 1978). In spring many waders moult into summer plumage in the Dutch Wadden Sea (Hg might again be excreted via the growing feathers), and accumulate fat before departure to the breeding grounds. Hg concentrations affecting reproduction might be accumulated at this time. Indeed, high Hg levels were found by Lindberg & Odsj6 (1983) in two wader (Tringa) species collected in the summer in N Sweden. They suggest that most of the Hg is picked up during migration and while the birds are wintering in polluted
Metal in waders
303
estuaries in northwestern and southern Europe. Overwintering waders will also accumulate Hg since elimination is slow when the metal cannot be deposited in growing feathers (Stickel et al., 1977). During bad conditions this might prove to be fatal as in the case of grey herons (van der Molen et al., 1982). However, the presence of Se might (partly) neutralize the toxicity of Hg (Ganther et al., 1973). Background As levels in tissues of normal animals are considered to be less than 0-5rag kg -1. Animals dying from acute or subacute As poisoning with tissue levels of 2-10 mg kg- ~ and levels higher than 10 mg kg- 1, all on a wet weight basis, would be considered to be cases which confirm As poisoning. Normal hair values are less than 1 mg kg- 1, those in cases of chronic poisoning, 5 mg kg- ~ and in acute poisoning, 10-30mg kg -1 (Buck, 1978). One of the first symptoms of acute As poisoning in swine is lack of co-ordination of movements (Ledet & Buck, 1978). Compared with these data, godwits have high--and redshanks and knot very high--organ concentrations. Also regarding these data it is suspected that a knot found to be drowned in the nets, and having a liver concentration of 100.5 mg kg- 1 dry weight and a vane concentration of 21.0mgkg -1, died (indirectly--problems of locomotion) due to As poisoning. Se poisoning severely affects reproduction. Laying hens fed 5-9 mg kg-1 for 16 weeks accumulated, on average, 2-3 mg kg-1 in liver and kidney while controls averaged less than 1 mg kg-~. Reproduction was affected; significant decreases occurred in egg weight, egg production and hatchability (Ort & Latshaw, 1978). Arnold et al. (1973) reported similar results. Liver and kidney concentrations in waders exceed 2-3 mg kg- 1; when there is no adaptation to these high concentrations, effects on reproduction might be expected. Selenosis in mammals affects tissues, causing loss of hair and nails and cracked hooves (Harr, 1978). However, malformations in the feathers were not observed in this investigation. Most animal species are tolerant to excessive intake of Zn. Poultry is able to tolerate levels of 1000-2000 mg kg-1 without adverse effects (Ewan, 1978). Therefore, the elevated levels found are not alarming with regard to toxicological effects.
Inter-species differences There are marked differences in prey items taken by the different wader species and between the sexes in the godwit. In the Dutch Wadden Sea
304
A. A. Goede
knot feed mainly on small molluscs, of which Macoma baltica is most common. The redshank feeds on a wider range of invertebrate species, including the polychaete Nereis, small molluscs like Macoma and small crustaceans (amphipods). The bar-tailed godwit's main prey items are large polychaetes, Nereis and Arenicola, the female taking larger specimens than the male (Smit & Wolff, 1981). These differences in diet probably account for the differences in metal contamination. However, the factors involved are complex. For example, in some species of polychaetes, smaller specimens accumulate higher amounts of metals per unit weight than the larger ones (Bryan & Hummerstone, 1973; Ray et al., 1980; Evans & Moon, 1981 (all Nereis), Packer et al. (1980) (Arenicola)); this might explain why the godwits, in particular the females, have the lowest Hg concentrations. Age-related As accumulation does not occur in the polychaete Tharyx marioni: both juvenile and adult worms accumulate remarkable amounts. Whole body concentrations usually exceed 2000 mg kg-1 dry weight (Gibbs et al., 1983). N e r d s also absorbs As, but to different extents in different circumstances (Bryan, 1974). Even short exposure to low concentrations of Hg in the water causes decreased, or even inhibited, burrowing activities in small Macoma, recovery being poor (Eldon et al., 1980); this means higher exposure for Hgoaffected specimens to predators eating the smaller Macoma species. McGreer (1979) reported similar results. And the availability of Zn to Macoma varies with the type of sediment (Luoma & Jenne, 1977); accordingly, exposure to Zn via this prey item will vary with the foraging areas of the wader. Hence, sampling only water, sediment and invertebrates is quite insufficient to assess the impact of pollution in an estuary with an important function in the life cycle of waders. Wadden Sea/river Rhine The trace metal concentrations (in sediments) in the Dutch Wadden Sea decrease in an easterly direction, apparently through the diminishing influence of the river Rhine (Salomons & De Groot, 1978). In some wader species this gradient is also reflected in their Hg and As contamination. For Zn the reverse is found and no explanation can be given for this phenomenon. Discharge of Hg and As decreased in the river Rhine during the last one or two decades, and accordingly As concentrations in the river Rhine sediment have decreased since 1958 to the level which occurred at
Metal in waders
305
the beginning of this century; Hg concentrations, on the other hand, have decreased since 1973 to the level of the middle of this century (Salomons & Eysink, 1981). In 1979-1982 highly elevated levels of these elements in waders from the Dutch Wadden Sea were still measured; the effects of pollution apparently remained detectable for a long time. Zinc levels in the sediment of the Rhine have only decreased slightly in the last decade after an approximately six-fold increase since the beginning of the century (Salomons & Eysink, 1981). Data on Se are not available. ACKNOWLEDGEMENTS I am grateful to Dr E. Nieboer, who loaned the bird trapping facilities of the Vrije Universiteit, Amsterdam on Schiermonnikoog. The Rijks Universiteit, Groningen, is thanked for providing lodging on Schiermonnikoog. Skilful field assistants were W. Tamis, P. M. Zegers, D. Tensen and T. M. van der Have. Feathers from skins were kindly provided by Dr Wattel, Zoological Museum, University of Amsterdam, from Vlieland by Dr G. C. Boere, P. M. Zegers and the Institute for Environmental Studies and from Morocco by the members of the Netherlands Morocco Expedition (1982). The Institute for Environmental Studies, Vrije Universiteit, Amsterdam, offered laboratory facilities and the Interuniversity Reactor Institute, Delft, made the analysis possible, thanks to the assistance of Dr ir. M. de Bruin and A. Dijkstra. Dr W. J. Wolff and Drs P. de Voogt made helpful comments on the manuscript, LASOM financed the project. Without all these valuable contributions, this study would not have been possible. REFERENCES Arnold, R. L., Olson, O. E. & Carlson, C. W. (1973). Dietary selenium and arsenic additions and their effects on tissue and egg selenium. Poultry Sci., 52, 847-54. Ashmole, N. P. (1962). The black noddy Anous tenuirostris on Ascension Island. Ibis, 103b, 235-319. Bednarek, W., Hausdorf, W., J6rissen, U., Schulte, E. & Wegener, H. (1975). Uber die Auswirkungen der chemischen Umweltbelastung auf Greifv6gel in zwei Probefl~ichen Westfalens J. Orn., 116, 181-94. Berg, W., Johnels, A., Sj6strand, B. & Westermark, T. (1966). Mercury content in feathers of Swedish birds from the past 100 years. Oikos, 17, 71-83.
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A. A. Goede
Blus, L. J., Neely, B. S., Lamont, T. G. & Mulhern, B. (1977). Residues of organochlorines and heavy metals in tissues and eggs of brown pelicans, 1969-73. Pestic. Monit. J., 11, 40-53. Boere, G. C. (1976). The significance of the Dutch Waddenzee in the annual life cycle of arctic, subarctic and boreal waders Part 1. The function as a moulting area. Ardea, 64, 210-91. Boere, G. C. & Smit, C. J. (1981). Knot. Bar-tailed godwit, Redshank. In Birds of the WaddenSea, ed. byC. J. Smit and W. J. Wolff, 136-45, 170-9, 195-206. Rotterdam, Balkema. Bryan, G. W. (1974). Adaptation of an estuarine polychaete to sediments containing high concentrations of heavy metals. In Pollution and physiology of marine organisms, ed. by F. J. Vernberg and W. B. Vernberg, 123-35, New York, Academic Press. Bryan, G. W. & Hummerstone, L. G. (1973). Adaptation of the polychaete Nereis diversicolor to estuarine sediments containing high concentrations of zinc and cadmium. J. mar. biol. Ass. UK, 53, 839-57. Buck, W. B. (1978). Toxicity of inorganic and aliphatic organic arsenicals. In Toxicity of heavy metals in the environment, ed. by F. W. Oehme, Part 1, 357-74. New York, M. Dekker. Biihler, U. & Norheim, G. (1982). The mercury content in feathers of the sparrowhawk Accipiter nisus in Norway. Fauna norv. Ser. C. Cinclus, 5, 43-6. de Bruin, M. & Korthoven, P. J. M. (1972). Computer oriented system for nondestructive neutron activation analysis. Analyt. Chem. 44, 2382-5. de Bruin, M., Korthoven, P. J. M. & Bode, P. (1982). Evaluation of a system for routine instrumental neutron activation analysis. J. Radiat. analyt. Chem. 70(1-2), 497-512. Dick, W. J. A. (ed.) (1975). Oxjord and Cambridge Mauretanian expedition, 1973. Report. Cambridge, W. J. A. Dick. Dick, W. J. A., Pienkowski, M. W., Waltner, M. & Minton, C. D. T. (1976). Distribution and geographical origins of knot Calidris canutus wintering in Europe and Africa. Ardea, 64, 22-47. Eldon, J., Pekkarinen, M. & Kristoffersson, R. (1980). Effects of low concentrations of heavy metals on the bivalve Macoma baltica. Ann. Zool. Fennici, 17, 233-42. Essink, K. (1980). Mercury pollution in the Ems estuary. Helgol. Wiss. Meeresunters., 33, 111-21. Evans, P. R. & Moon, S. J. (1981). Heavy metals in shore birds and their prey. In Heavy metals in Northern England." Em, ironmental and biological aspects. ed. by P. J. Say and B. A. Whitton, 181-90. University of Durham. Ewan, R. C. (1978). Toxicology and adverse effects of mineral imbalance with emphasis on selenium and other minerals. In Toxicity of heavy metals in the environment, ed. by F. W. Oehme, Part 1,445-89. New York, M. Dekker. Fimreite, N. (1974). Mercury contamination of aquatic birds in northwestern Ontario. J. Wildl. Mgmt, 38, 120-31. Finley, M. T. & Stendell, R. C. (1978). Survival and reproductive success of black ducks fed methyl mercury. Environ. Pollut., 16, 51 64.
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Toxicity of heavy metals in the environment, ed. by F. W. Oehme, Part 1, 375-92. New York, M. Dekker. Lindberg, P. & Odsj6, T. (1983). Mercury levels in feathers of peregrine falcon Falco peregrinus compared with total mercury content in some of its prey species in Sweden. Environ. Pollut. (Ser. B), 5, 297-318. Ljunggren, L. (1968). The influence of mercury poisoning on the reproduction and general health of wood pigeons. Viltrevy, 5, 423-31. Luoma, S. N. & Jenne, E. A. (1977). The availability of sediment-bound cobalt silver and zinc to a deposit-feeding clam. In Biological implications of metals in the environment. Proc. Ann. Hanford Life Sci. Symp., 15th, ed. by H. Drucker and R. E. Wildung. Martin, J. H., Elliott, P. D., Andenlini, V. C., Girvin, D., Jacobs, S. A., Risebrough, R. W., Delong, R. L. & Gilmartin, W. G. (1976). Mercury-selenium-bromine imbalance in premature parturient California sea lions. Mar. Biol., 35, 91-104. McGreer, E. R. (1979). Sublethal effects of heavy metal contaminated sediments on the bivalve Macoma baltiea (L.). Mar. Pollut. Bull., 10, 259-62. Ort, J. F. & Latshaw, J. D. (1978). The toxic level of sodium selenite in the diet of laying chickens. J. Nutr., 108, 1114-20. Osborn, D. (1979). Seasonal changes in the fat, protein and metal content of the liver of the starling Sturnus vulgaris. Environ. Pollut., 19, 145-55. Osborn, D., Harris, M. P. & Nicholson, J. K. (1979). Comparative tissue distribution of mercury, cadmium and zinc in three species of pelagic seabirds. Comp. Biochem. Physiol., 64C, 61-7. Packer, D. M., Ireland, M. P. & Wootton, R. J. (1980). Cadmium, copper, lead, zinc and manganese in the polychaete Arenicola marina from sediments around the coast of Wales. Environ. Pollut. (Set. A), 22, 309-21. Parslow, J. L. F. (1973). Mercury in waders from the Wash. Environ. Pollut., 5, 295-304. Ranta, W. B., Tomassini, F. D. & Nieboer, E. (1978). Elevation of copper and nickel levels in primaries from black and mallard ducks collected in the Sudbury district, Ontario. Can. J. Zool., 56, 581-6. Ray, S., McLeese, D. & Pezzack, D. (1980). Accumulation of cadmium by Nereis virens. Arch. environ. Contam. & Toxicol., 9, 1-8. Reijnders, P. J. H. (1980). Organochlorine and heavy metal residues in harbour seals from the Wadden Sea and their possible effects on reproduction. Neth. J. Sea Res., 14, 30-65. Salomons. W. & de Groot, A. J. (1978). Pollution history of trace metals in sediments, as affected by the Rhine river. In Environmental biogeochemistry and geomicrobiology, ed. by W.E. Krumbein, 1, 140-64. Ann Arbor, Ann Arbor Science. Salomons, W. & Eysink, W. D. (1981). Pathways of mud and particulate metals from rivers to the southern North Sea. In Biogeochemical and hydrodynamic processes affecting heavy metals in rivers, lakes and estuaries. Pubis Delft Hydraulics Laboratory, no. 253. Scanlon, P. F., O'Brien, T. G., Schauer, N. L., Coggin, J. L. & Steffen, D. E.
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