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Organochlorine contaminants and eggshell thinning in grebes from prairie Canada
Environmental Pollution 85 (1994) 51-58
ORGANOCHLORINE CONTAMINANTS AND EGGSHELL T H I N N I N G IN GREBES F R O M PRAIRIE C A N A D A D.J. Forsyth a, P.A. Martin a, K.D.
De Smet b
& M.E.
Riske C
a Canadian Wildlife Service, 115 Perimeter Road, Saskatoon, Saskatchewan, S7N OX4, Canada b Manitoba Department of Natural Resources, Southwest Conservation Centre, Box 520, Melita, Manitoba ROM 1LO, Canada c R.R. #1 Camrose, Alberta T4V2M9, Canada
(Received 28 October 1992; accepted 19 March 1993)
organochlorine contaminants, including polychlorinated biphenyls (PCBs), have also been associated with reproductive impairment (Risebrough, 1986). Low reproductive success of northern gannets (Sula bassanus) in Quebec during the late 1960s was associated with a 17% reduction in mean shell thickness and DDE levels of 18.5 mg kg-~ wet weight (Elliott et al., 1988). Reductions in breeding success and increased incidence of cracked eggs of black-crowned night herons (Nycticorax nycticorax) in the western United States during the late 1970s were correlated with DDE levels and eggshell thinning (Henny et al., 1984). Effects became particularly severe at DDE concentrations above 8 mg kg j wet weight with mean reductions in shell-thickness of 13% (Henny et al., 1984). Banning the use of DDT and most other organochlorine pesticides in North America during the early 1970s resulted in reductions of residues in the eggs of most aquatic species, recovery of shell thickness to values typical of the pre-DDT era, and concomitant improvements in breeding success (Fleming et al., 1983; King et al., 1985; Fox & Weseloh, 1987). Organochlorine concentrations sufficient to cause reproductive impairment persisted in many avian populations, nonetheless (Fleming et al., 1983; Henny et al., 1985). Grebes (family Podicipedidae) occupy the upper trophic levels of inland aquatic ecosystems, feeding primarily on fish and large invertebrates (Wetmore, 1924; Munro, 1941). In recent years there has been some concern about the stability of North American grebe populations (Tate, 1981; Koonz & Rakowski, 1985; Tate, 1986). Western grebes (Aechmophorus occidentalis) in Utah with mean egg concentrations of DDE of about 5.4 mg kg I and 2.3% shell-thinning appeared to be experiencing reduced productivity in comparison to normally producing birds (Rudd & Herman, 1972; Lindvall & Low, 1980). De Smet (1987) attributed extremely low egg viability and reduced fledging success in a southwestern Manitoba population of red-necked grebes (Podiceps grisegena) in 1981, in part, to elevated mean concentrations of DDE and PCBs of 6.68 and 17.53 mg kg-1 wet weight, respectively, and associated shell-thinning of 6.5%. The purpose of this study was to determine, through a broad-scale monitoring effort, if the contaminant levels
Abstract
Eggs of five species of grebe were collected from Manitoba, Saskatchewan and Alberta during 1982-1987: red-necked (Podiceps grisegena), horned (P. auritus), eared (P. caspicus), western (Aechmophorus occidentalis) and pied-billed (Podilymbus podiceps). DDE and PCBs were present in all samples analyzed, whereas dieldrin, mirex and oxychlordane were occasionally present at low levels. Mercury was present at low levels in all samples for which it was analyzed. Red-necked grebes nesting in Manitoba had the highest contaminant levels and, assuming that contaminant burdens were accumulated principally on the wintering grounds, the mean P C B : D D E ratio (3.1) indicated that these birds and those from sites in central and eastern Saskatchewan probably wintered on the Atlantic coast. Overall low contaminant levels and a low mean P C B : D D E ratio (1.4) in the eggs of red-necked grebes breeding in Alberta and western Saskatchewan suggested that these birds wintered on the Pacific coast. A similar pattern was apparent in horned and eared grebes. Concentrations of D D E and PCB were both significantly correlated with Ratcliffe index (shell thickness), and were strongly correlated with each other. Ratcliffe indices were determined for historical collections of red-necked grebe eggs. Eggshell thickness of grebes nesting in Manitoba declined significantly during the years following the introduction of D D T (post-1947) and has only recovered partially since it was banned in 1972. The Alberta-breeding population did not appear to have undergone any significant decrease in shell thickness. INTRODUCTION
The association between shell thickness and organochlorine contamination of eggs has been documented in many aquatic bird species (Anderson & Hickey, 1972; Faber & Hickey, 1973). Their position at the top of the food web predisposes fish-eating species to accumulate lipophilic contaminants from their diet. DDE, the major metabolite of the insecticide DDT, is the contaminant most clearly correlated with shell-thinning of eggs and the resultant breakage, although other Environ. Pollut. 0269-7491/94/$07.00 © 1994 Elsevier Science Limited, England. Printed in Great Britain
51
D . J . Forsyth, P. A. Martin, K. D. De Smet, M. E. Riske
52
1-12 nests (clutches o f two o r m o r e eggs) per b r e e d i n g a r e a d u r i n g M a y to July a n d p o o l e d b y a r e a for each species. Eggs were collected at v a r i o u s stages o f laying a n d incubation; a b o u t 5 - 1 0 % were a d d l e d . In 1982 a n d 1983 b u t n o t in 1986 a n d 1987, the length a n d width o f each egg was m e a s u r e d to the nearest 0.1 m m . Eggs were opened a n d the contents were e m p t i e d into acetonerinsed glass j a r s that were sealed with a l u m i n u m foillined lids, a n d frozen. Eggshells were rinsed with water, a i r - d r i e d for at least 3 m o n t h s , weighed to the nearest 0.01 g, a n d Ratcliffe indices (Ratcliffe, 1967) o f shell thickness were calculated. Eggs were frozen a n d stored intact in plastic bags in 1986 a n d 1987. All eggs were s h i p p e d to the N a t i o n a l Wildlife R e s e a r c h Centre (Hull, Quebec) where they were i n d i v i d u a l l y h o m o genized a n d frozen; a l i q u o t s f r o m h o m o g e n a t e s were s u b s e q u e n t l y used to o b t a i n p o o l e d samples. R e s i d u e analyses o f the 1982 a n d 1983 s a m p l e s were c o n d u c t e d by the O n t a r i o R e s e a r c h F o u n d a t i o n ( O R F ; Mississauga, Ontario); analyses o f the later collections were p e r f o r m e d by M a n i t o b a E n v i r o n m e n t (Winnipeg, M a n i t o b a ) . A n a l y s i s o f s t a n d a r d i z e d reference samples o f gull egg h o m o g e n a t e b y the two l a b o r a t o r i e s d e m o n strated t h a t their results were c o m p a r a b l e a n d generally fulfilled the quality assurance criteria (Turle et al., 1988). D D E values f r o m analyses o f 1986 a n d 1987 samples (Tables 1 a n d 2) were increased b y 20.7% to c o r r e c t for l a b o r a t o r y bias relative to the reference samples.
a n d c o n c o m i t a n t r e d u c t i o n s in shell thickness o f r e d - n e c k e d grebe eggs r e p o r t e d by D e Smet (1987) in M a n i t o b a were p r e v a l e n t in grebes t h r o u g h o u t the C a n a d i a n prairies. Specific objectives were (1) to o b t a i n egg samples o f all five species o f p r a i r i e - n e s t i n g grebe for residue analysis; (2) to d e t e r m i n e the r e l a t i o n s h i p s a m o n g o r g a n o c h l o r i n e residues a n d eggshell-thinning, focusing on the r e d - n e c k e d grebe; (3) to e x a m i n e historical c h a n g e s in shell thickness o f r e d - n e c k e d grebe eggs.
METHODS
Sample collection Eggs were collected f r o m r e d - n e c k e d grebes across the prairie p r o v i n c e s o f M a n i t o b a , S a s k a t c h e w a n a n d A l b e r t a ; f r o m e a r e d grebes (Podiceps caspicus) in S a s k a t c h e w a n a n d M a n i t o b a ; a n d from western, h o r n e d (Podiceps auritus) a n d pied-billed (Podilymbus podiceps) grebes in M a n i t o b a only (Fig. 1). Collections were m a d e in 1982, 1983, 1986 a n d 1987. A b r e e d i n g a r e a was c o n s i d e r e d to be a lake, m a r s h o r g r o u p o f small w e t l a n d s in close g e o g r a p h i c p r o x i m i t y . S o m e collections m a d e in 1986 a n d 1987 were divided into samples a, b o r c (Tables 1 a n d 2), representing different l o c a t i o n s within the a r e a or s a m p l i n g dates 1 m o n t h apart. Single eggs were collected at r a n d o m from each o f
Table 1. Organochlorine and mercury concentrations (mg kg-I, wet weight) in pooled samples of red-necked grebe eggs from Manitoba, Saskatchewan and Alberta collected between 1982 and 1986 Province Breeding area
Year Number eggs
DDD
DDT
DDE
Dieldrin
12 4 3 5 3 10 6 10 1 1 2
0-01 <0-03 <0-03 0-01 <0.03 <0.03 <0-03 <0.03 <0.03 <0.03 <0-03
0-02 <0-04 <0-04 0-02 <0-04 <0.04 <0-04 <0.04 <0.04 <0.04 <0-04
3.15 3.08 2.39 3.44 4.44 2.86 3-86 2-58 7.39 3.05 2.64
0.13 0.06 0.02 0.12 0-09 0.11 0-10 0-08 0.12 0-04 0-06
0-17 b -0.17 --
Shallow Lake Lone Island Lake Duck Bay Waterhen Lake
1983 1986a 1986b 1983 1986a 1986b 1986c 1986 1986 1986 1986
Saskatchewan 8. Prince Albert Park 9. Little Manito Lake 10. Minnow Lake 11. Reflex Lake 12. Moose Mountain Park
1982 1983 1983 1983 1983
5 10 5 10 10
0.11 <0.01 <0.01 <0.01 0.01
<0-01 <0.01 <0.01 <0-01 0-01
1-62 1.20 0.42 0.26 3.63
0.02 0.01 <0.01 <0-01 0-06
Alberta 13. Lac Ste. Anne 14. Wizard Lake 15. Wabamum Lake 16. Woods Lake
1982 1982 1982 1983
10 10 9 10
0.06 0-01 0.07 <0.01 0.07 <0-01 <0.01 <0.01
0-33 0.49 0.44 0.59
<0-01 <0-01 <0-01 0.01
Manitoba 1. Turtle Mountain Park 23 May 26 June 2. North Shoal Lake 3. Sandy Lake area
4. 5. 6. 7.
OxyMirex PCB" Total Ratcliffe index chlordane (1:1) mercury mean (SD)
0-67 0.28 0-38 0.19 0.34 0.35 0-46 0.20 1.63 0.24 0.06
10-80 8.96 5-64 7.96 13.44 10.02 16.18 7.66 21-00 8.73 10-50
0-09 --0.11 --------
1.76 (0.14)
0.03 0.05 0.01 0.01 0.16
0.31 0.04 <0.01 <0.01 <0.01
5-98 1.47 0.46 0.29 6-58
0-11 0.08 0.07 0.21 0.09
1.71 1.85 1.85 1.81 1.81
<0.01 0.01 0.01 0.06
<0.01 <0.01 <0.01 0.03
0.16 0.62 0.32 1.85
0.07 0.15 0.10 0.09
1-80 (0-I1) 1.84 (0.13) 1.90 (0.15) 1.81 (0.10)
------
Samples designated a, b or c were collected 1 month apart or from different locations within the breeding area. "Single peak estimate of 1:1 Aroclors 1254:1260 (Turle et al., 1988). b 1986 samples not analyzed for oxychlordane or mercury and not measured for Ratcliffe index calculation.
-1.65 (0.13) -------(0.19) (0.16) (0.18) (0.09) (0.17)
53
Organochlorine contaminants and eggshell thinning in grebes
ALBERTA
SASKATCHEWAN /
/
MANITOBA
/ o
MONTANA
USA
l
• ~'-'-~MINNESOTA NORTHDAKOTA
Fig. 1. Locations of red-necked (filled circle), eared (filled triangle), horned (filled square), pied-billed (unfilled circle) and western (unfilled square) grebe egg collection areas in Manitoba, Saskatchewan and Alberta, Canada. Locations from which eggs of two species were collected are shown as filled circles. Numbers refer to areas listed in Tables 1 and 2. Red-necked grebe eggshells from private a n d museum collections were weighed a n d m e a s u r e d for calculations o f Ratcliffe indices. Eggshells were from A l b e r t a , S a s k a t c h e w a n , M a n i t o b a a n d the K e n o r a district in n o r t h e r n O n t a r i o (near the M a n i t o b a b o r d e r ) a n d collection dates ranged f r o m 1895 to 1984. Egg collection dates were divided into three time p e r i o d s for c o m p a r i s o n o f Ratcliffe indices: the p r e - D D T era, p r i o r to 1947: the p e r i o d o f D D T use, between 1948 a n d
1971; a n d the p e r i o d following the b a n n i n g o f D D T use in N o r t h A m e r i c a , 1972 1983.
Residue analysis P o l y c h l o r i n a t e d biphenyls (PCBs), D D T a n d its two m e t a b o l i t e s D D D a n d D D E (p,p' isomers), dieldrin, h e p t a c h l o r epoxide, the c h l o r d a n e - r e l a t e d c o m p o u n d s except o x y c h l o r d a n e , a n d mirex were d e t e r m i n e d every year. M e r c u r y a n d o x y c h l o r d a n e were m e a s u r e d only
Table 2. Organochlorine concentrations (mg kg=l, wet weight) in pooled samples of eared, horned, pied-billed and western grebe eggs from Manitoba and Saskatchewan, collected between 1982 and 1987 Species Breeding area
Year
Number eggs
DDD
DDT
DDE
Dieldrin
Mirex
PCB" ( 1:1 )
1982 1983 1986 1986 1986 1986 1986 1986
5 10 5 5 10 10 10 10
0.07 <0-01 <0-03 <0-03 <0.03 <0.03 <0.03 <0.03
0.01 <0.01 <0-04 <0.04 <0.04 <0-04 <0-04 <0-04
0.80 0-51 0.63 0.31 0.72 0.99 0.41 0.92
<0.01 <0.01 <0.02 <0-02 <0-02 <0.02 <0-02 <0-02
<0.01 <0.01 <0-05 <0.05 <0-05 <0.05 <0-05 <0.05
0.16 0.06 0-38 <0-01 <0.01 <0.01 <0.01 <0.01
Horned grebe 3. Sandy Lake area, Man. 7. Waterhen Lake, Man. 24. Southwestern Manitoba 25. Minnedosa, Man. 25. Minnedosa, Man.
1986 1986 1986 1986 1987
2 4 4 7 5
<0.03 <0-03 <0.03 <0-03 <0-03
<0.04 <0.04 <0.04 <0.04 <0.04
1.50 0.78 1-28 0.69 1.47
0-02 <0-02 <0.02 <0.02 0.02
<0-05 <0.05 <0.05 <0.05 <0.05
6.28 1.75 2.46 2.24 4.42
Pied-billed grebe 25. Minnedosa (a), Man. 25. Minnedosa (b), Man. 26. Gull Lake, Man.
1987 1987 1986
5 5 2
<0.03 <0.03 <0.03
<0.04 <0.04 <0-04
1-47 0.75 0.25
<0-02 <0-02 <0.02
<0-05 <0.05 <0.05
1.02 0.38 0.83
Western grebe 6. Duck Bay (a), Man. 6. Duck Bay (b), Man. 27. Ninette (a), Man., 26 June 27. Ninette (b), Man., 22 July
1986 1986 1986 1986
10 4 10 10
0.29 0-58 0-47 0-66
<0-04 <0.04 <0.04 <0.04
0.70 0.84 2.60 3-37
<0-02 <0.02 <0-02 <0.02
<0.05 <0.05 <0.05 <0-05
2.55 2.08 4.22 4-67
Eared 17. 18. 19. 19. 20. 21. 22. 23.
grebe Bradwell, Sask. Grave Lake, Sask. Proven Lake (a), Man. Proven Lake (b), Man. Oak Hammock, Man. Winnipegosis Lake, Man Dog Lake, Man. Plum Lake, Man.
Samples designated a and b were collected 1 month apart or from different locations within the breeding area. u Single peak estimate of 1:t ratio of Aroclors 1254:1260 (Turle et al., 1988).
54
D. J. Forsyth, P. A. Martin, K. D. De Smet, M. E. R&ke RESULTS
in 1982 and 1983. Analyses for organochlorines, by capillary column gas c h r o m a t o g r a p h y (GC), followed the procedures of Reynolds & Cooper (1975): detection limits were 0.01 mg kg ~ wet weight in 1982 and 1983. Detection limits for the 1986 and 1987 samples were 0.03, 0.04, 0.02 and 0.05 mg kg ~ for D D D , D D T , dieldrin and mirex, respectively. PCBs are expressed as a 1:1 ratio of Aroclors 1254:1260 (Turle et al., 1988) and detection limits in all years were 0.01 mg kg ~. These values are about 2-fold higher than those based on sums of PCB congeners, but can be compared to earlier studies (Turle et al., 1991). Mercury was analyzed by O R F using cold vapor atomic absorption following digestion of samples with sulphuric and nitric acids at 60°C. Potassium permanganate was used to oxidize organic material and the excess was reduced by the addition of hydroxylamine hydrochloride and, immediately prior to analysis, by stannous chloride. Residues were reported on a wet weight basis. We were unable to correct for moisture loss (Stickel et al., 1973) as moisture content was not measured in eggs from 1986 or 1987. Transformation (log~0) of the data for statistical analysis was effective in reducing the heterogeneity of variance that is typical of contaminant data. Residue values reported are means and 95% confidence intervals. For the calculation of means, concentrations below detection limits were arbitrarily given the value of zero. We used the General Linear Model Procedure of SAS (SAS Institute Inc., 1985) to perform analyses of variance (ANOVA) and Tukey's honestly significant difference (HSD) tests for means separation. The Stepwise Procedure was used to conduct a stepwise multiple regression of D D E , dieldrin and PCB concentrations in pooled rednecked grebe egg samples collected in 1982 and 1983 (n -- 11) on the mean Ratcliffe index of the eggs within those pools. We then determined Pearson's correlation coefficients among the variables using the Correlation Procedure. Significance was inferred at p < 0.05.
A total of 20 samples (18 pooled, 2 12 eggs each; 2 single eggs) of red-necked grebe eggs and eight samples (5-10 eggs each) of eared grebe eggs was collected between 1982 and 1987 (Tables 1 and 2). Four, five and three samples (2-10 eggs each) of western, horned and piedbilled grebe eggs, respectively, were collected during 1986 and 1987 only (Table 2). Significant D D E and PCB residues were detected in all samples (Tables 1 and 2), with the exception of most Manitoba eared grebe eggs, in which PCBs were below detection limits (Table 2). D D T and D D D were detected in one Saskatchewan eared grebe sample. All western grebe samples contained D D D (Table 2). Dieldrin and mirex were found primarily in eggs of Manitoba-nesting rednecked grebes, but also in two Saskatchewan samples and one Alberta sample (Table 1). These compounds were below detection limits in eared, homed, pied-billed and western grebe eggs (Table 2). The chlordane-related compounds and heptachlor epoxide were below detection limits in most samples; however low levels (< 0.2 mg kg ~) of oxychlordane were measured in the majority of red-necked grebe eggs collected in 1982 and 1983. Mercury was detected in all samples for which it was analyzed (red-necked grebe eggs, 1982 and 1983: Table 1) and concentrations were generally close to 0.1 mg kg Levels of D D E , PCBs, dieldrin and mirex as well as the ratio of PCB:DDE were compared among rednecked grebe eggs from the three provinces and with the other four species (Table 3). Concentrations of these compounds were significantly higher in the eggs of red-necked grebes from Manitoba than in those from Alberta and Saskatchewan, or in those of eared, horned and pied-billed grebes (Table 3). Western grebe eggs had levels of D D E that were intermediate between those of Manitoba red-necked grebe eggs and those of
Table 3. Comparisons of residues (mg kg-I, wet weight, geometric mean and 95% confidence intervals) of DDE, PCB, mirex and dieldrin and PCB:DDE ratios (arithmetic mean and SE) among the eggs of five species of prairie-nesting grebe
Species
Number
DDE
Red-necked (Manitoba) Red-necked (Saskatchewan) Red-necked (Alberta) Eared
11
3.20" (2.66-3.82) 1.09f' (0.15 2 . 8 0 ) 0.45 ~ (0.32 1.29) 0.64 ~ (0-49-0.81 ) 1.11 h (0.82-1.46) 0.75 t' (0.24-1.49) 1-65"t' (0.71 3.10)
5 4 8
Horned
5
Pied-billed
3
Western
4
PCB 9-96" (8-12 1 2 . 1 8 ) 1.46~'' (0-07-4.62) 0.62' (0-07 1.46) 0.19' (0.02-0-40) 3.14~ (1.89493) 0.72 h'' (0.37-1.17) 3.76h (2.55 5.40)
Mirex
Dieldrin
0.38" (0.20-0.59) 0.02 h
ND b
0.07" (0.05 0.10) 0.02 h (0-0.07) ND ~ ND h
ND h
ND b
ND h
ND h
ND h
ND h
0.02 b
PCB:DDE 3.1" (0.2) 1.8~ (0.1) 1.4t' (0.6) 0.1' (0.07) 2.9" (0.7) 1.6h (0-91) 2.3 ''h (0.5)
ND = residues below detection limits: equivalent to zero in statistical analysis. ..h., Means within a column sharing the same superscript are not significantly different (p > 0-05: ANOVA and Tukey's HSD test).
Organochlorine contaminants and eggshell thinning in grebes Table 4. Ratcliffe indices (mean __ SE, n) of red-necked grebe eggs from Manitoba, Saskatchewan and Alberta before, during and following the ban of DDT use in North America
Manitoba a Pre-1947h
1-80 + 0.02 Aa 33 1948 1971h 1.49_+0-05 Ab 10 1972-1983 ~ 1.70 + 0-03 Ac 31
Saskatchewan"
Albertaa
1-78+ 0-03 Aa 19 1.56+ 0.10 Ab 10 1.79_+0-02 Ba 46
1.82+ 0.03 Aa 29 1.85+ 0.01 Ba 253 1-84+ 0-02 Ba 77
"Means within a column sharing a lower case letter in common are not significantly different (p > 0.05: ANOVA and Tukey's HSD test). Means within a row sharing an upper case letter in common are not significantly different (p > 0.05: ANOVA and Tukey's HSD test). all other populations (Table 3). The ratio of PCB to D D E was highest in the Manitoba population of rednecked grebes and horned grebes, whereas eared grebes had significantly lower ratios than all other species (Table 3). In a multiple regression of DDE, dieldrin and PCBs on Ratcliffe index of red-necked grebe eggs from 1982 and 1983, PCBs accounted for the greatest variation in the relationship, having a partial R 2 of 0.60. The added contributions of D D E and dieldrin to the model were insignificant (DDE: partial R 2 -- 0.035, p -- 0.41; dieldrin: partial R z -- 0.074, p = 0.23); however, all three independent variables were highly intercorrelated (r values > 0.85), with PCBs and D D E having a correlation coefficient of 0.95. Correlation coefficients of DDE, dieldrin and PCBs with Ratcliffe index were high ( 0.67, 0.76 and 0.77, respectively). Considerable information is lost by regressing pooled sample contaminant concentrations against mean Ratcliffe indices, compared to a regression using data for individual eggs. The significant interaction, in a two-way ANOVA, between the effects of province and historical period on Ratcliffe indices of red-necked grebe eggs indicated that eggshell thickness changed over time differently among the three provinces. A subsequent one-way A N O V A revealed no differences a m o n g the provinces during the p r e - D D T era, and the overall mean Ratcliffe index was 1.80 (Table 4). During the period of D D T use (1948-1971) however, grebe eggs from Saskatchewan and Manitoba underwent significant reductions in Ratcliffe index (14 and 18%, respectively) while Alberta eggs remained unaffected (Table 4). In the years since the banning of D D T (post-1972) Saskatchewan grebe eggs returned to p r e - D D T levels, while the Ratcliffe index of Manitoba grebe eggs recovered slightly, to a mean level 8°/,, lower than the p r e - D D T mean (Table 4). DISCUSSION All eggs in our study were collected in areas remote from industrial pollution. The fact that some of the
55
highest concentrations of PCB were found in grebe eggs from inside or close to provincial and national
parks suggests strongly that most of the contaminant burden in these birds was accumulated during winter or spring migration. The high P C B : D D E ratio (3.1) in eggs of red-necked grebes from Manitoba is similar to the 3:1 ratio that is characteristic of birds wintering or staging on the Atlantic coast and the Great Lakes, where elevated levels of the industrial contaminant PCB predominate. In contrast, the overall low PCB levels and approximately 1:1 P C B : D D E ratio found in eggs of Alberta-nesting red-necked grebes is typical of birds wintering on the Pacific coast (Keith & Gruchy, 1972). Although red-necked grebes are known to winter on both coasts, the dividing line between eastern and western migrants is not known (Palmer, 1976). The elevated PCB levels and PCB:DDE ratios of 3.7 and 1.8 of eggs from the central and eastern Saskatchewan collection areas (Prince Albert Park and Moose Mountain Park, respectively; Fig. 1) suggest that birds breeding in these regions probably also wintered on the Atlantic coast. Fox et al. (1980) concluded that c o m m o n loons (Gavia #nmer), nesting in northeastern Saskatchewan, with eggs containing a mean PCB:DDE ratio of 2.4, wintered along the Atlantic coast, while Alberta-nesting populations with P C B : D D E ratios of 0.7, wintered along the Pacific coast. The presence of mirex at significant levels in all samples of Manitoba red-necked grebe eggs, as well as the Prince Albert sample, supports the hypothesis that these birds spent some time during migration on the lower Great Lakes, where mirex occurs consistently. Mirex concentrations ranging from 0.20 to 1.63 mg kg ~ in these samples are comparable to those in the eggs of resident herring gulls collected from Hamilton Harbour, Lake Ontario between 1981 and 1987 (annual means range from 0.58 to 2.35 nag kg t; Bishop et al., 1992). It is unlikely that the mirex in rednecked grebe eggs from Manitoba originated on either the Atlantic or Pacific coast because eggs of piscivorous birds from both coasts contained at least 10-fold lower concentrations of mirex during the 1980s than did our eggs (Elliott et al., 1989; Pearce et al., 1989). The generally lower organochlorine levels in eared, horned and pied-billed grebes in comparison to rednecked grebes, probably reflect the relatively high proportion of fish eaten by red-necked grebes (56%) compared to the other species (Wetmore, 1924; Munro, 1941). The very low P C B : D D E ratio found in eared grebe eggs is consistent with this species wintering on the Pacific coast, in large western inland water bodies and in Mexico (Palmer, 1962). Although horned grebes winter on both coasts, the Manitoba-nesting populations of this study probably migrate to the eastern coast, hence accumulating a proportionately greater burden of PCBs relative to DDE. Unlike the other species of grebe, the pied-billed grebe does not winter coastally, but prefers small inland ponds in the southern United States and throughout Central and South America (Palmer, 1976). The low PCB levels and intermediate P C B : D D E ratio (1.6) indeed suggest that these
56
D. J. Forsvth, P. A. Martin, K. D. De Smet, M. E. Riske
grebes are avoiding heavily industrialized Atlantic coastal regions, although our sample represents only two breeding areas. Western grebes are the most piscivorous of all North American grebes, with fish comprising up to 81% of the winter diet (Palmer, 1962) and contributing to their relatively high contaminant burden. Walker (1983) has shown, however, that fish-eating birds exhibit very low activity of hepatic mixed-function oxidases, the enzymes responsible for the metabolism of toxic substances including organochlorines. Toxicant metabolism generally decreases with increasing body mass, perhaps further explaining the high contaminant levels in western and red-necked grebes relative to the three smaller species (Walker, 1983). Western grebes are known to winter along the Pacific coast and inland through California and Mexico but not along the Atlantic coast (Palmer, 1962). Their PCB:DDE ratio (2.3) approaches that typical of Atlantic-wintering birds, nonetheless, suggesting that they may winter in bays receiving industrial, as opposed to agricultural, runoff (Henny et al., 1985). The fact that all samples contained DDD, a short-lived metabolite of DDT, is indicative of fairly recent exposure to DDT. The PCB, D D E and D D D levels were similar to those detected in a larger sample of western grebe eggs from the Klamath Basin, California in 1981 (Boellstorff et al., 1985). Mean DDE and PCB residues of the eastern-migrating population of red-necked grebes were somewhat lower in the current study in comparison to those measured in southwestern Manitoba in 1981 (De Smet, 1987). The two samples collected from Turtle Mountain Park in 1986 averaged 2.74 and 7.30 mg kg t for DDE and PCBs, respectively, compared to mean residues of 6.68 and 17.53 mg kg ', respectively, in samples collected from the same park in 1981 (De Smet, 1987). Eggs collected from other areas in Manitoba during 1986 contained residues similar to those of the 1981 sample mean, however, suggesting that overall, contamination had not declined appreciably between 1981 and 1986 in eastern-migrating red-necked grebes. Residues were nonetheless well below those of another eastern population (Wisconsin) measured during 1970 (54.5 and 62.8 mg kg ~, D D E and PCBs, respectively; Faber & Hickey, 1973). Concentrations of DDE reported in the literature are considered to be relatively reliable, regardless of advances in analytical methodology, but PCBs reported prior to 1974 are probably underestimated because of changes in methods of PCB quantitation based on Aroclor mixtures (Turle et al., 1988). Thus, any declines in PCB levels apparent by comparing our data with those from the earlier analyses are probably also underestimates. Concentrations of D D E in horned grebe eggs in our study (1.11 mg k g ' ) were substantially lower than the 5.13 mg k g ' found in samples collected from Saskatchewan during the late 1960s (Vermeer & Reynolds, 1970). D D E levels were also considerably lower than those in samples collected from Alberta in
1971 (2.56 mg kg i; Riske, 1976), although PCB levels were similar (3.14 versus 4.24 mg kg 1; Riske, 1976). A comparison of mean D D E residues in western grebe samples taken in 1986 (1.65 mg kg 1) to those taken from Alberta in 1969 and 1971 (7.76 and 4.88 mg kg 1 respectively) and Saskatchewan in 1969 (3.70 mg kg 1) reveals a similar decline (Vermeer & Reynolds, 1970; Riske, 1976). Reductions in D D E residues probably reflect the cessation of the usage of D D T in agricultural areas along the west coast wintering grounds of western grebes and probably of Alberta-nesting horned grebes. However, DDE levels in eared grebe eggs collected in Manitoba and Saskatchewan from 1982 to 1986 were similar to those in eggs analyzed in Saskatchewan in 1969 (0.55 mg kg ~) and in Alberta in 1976 (1.06 mg kg ') (Vermeer & Reynolds, 1970; Riske, 1976). No early data are available for contaminant levels in the eggs of pied-billed grebes nesting on the Canadian prairies: levels of DDE and PCBs in a Wisconsin-nesting population in 1970 were 10-fold greater than those of our samples (6.61 and 6.21 mg kg ~, respectively; Faber & Hickey, 1973), indicating either large population differences or a decline in contaminant levels over time. Analysis of historical red-necked grebe eggshell thickness data indicated that eastern populations (Manitoba-nesting; see Table 4) underwent reductions in shell thickness during the D D T era from which they had not yet completely recovered by 1983, whereas western populations (Alberta-nesting) maintained shell thickness throughout that time. Lack of information about the migratory routes and wintering grounds of Saskatchewan-nesting birds makes interpretation of shell thinning trends in that province difficult. The correlation between DDE and Ratcliffe index observed in rednecked grebe eggs has been demonstrated in many other species of inland aquatic birds (Fox et al., 1980; Lindvall & Low, 1980; Haseltine et al., 1981; McEwen et al., 1984). The existence of this relationship, in combination with the increase in shell thickness apparent since 1972 in eastern prairie populations of red-necked grebes, suggests that D D E levels were higher in these populations prior to the banning of DDT. Residue data for Manitoba-nesting red-necked grebes during the D D T era are not available, however, for comparison to our values and those of De Smet (1987). De Smet (1987) found high variability in shell thickness indices, and although the mean degree of shell thinning relative to pre-DDT shells was only 4.6% (compared to our Ratcliffe index value of 1.8 for prairie-nesting populations), shells of individual eggs were as much as 39% thinner. He found a high incidence of cracked eggs, and attributed the high rate of single egg disappearance between nest checks (8.3%) to cracking of thin-shelled eggs that were subsequently ejected from the nest by parents (De Smet, 1987). Shell thickness need not be significantly decreased for an overall loss in shell strength to occur. Both D D E and PCBs are known to cause a reduction in density of shell pores and mammillae resulting in decreased shell quality, although the relation-
Organochlorine contaminants and eggshell thinning in grebes
ship with PCBs is less well documented (reviewed in Risebrough, 1986). An Alberta colony of common terns (Sterna hirundo) with a mean egg D D E content of 3.98 mg kg ~ and almost undetectable PCB levels exhibited a strong positive correlation between shell pore and mammillae densities and egg success, whereas shell thickness was unrelated and not significantly lower than p r e - D D T thickness (Fox, 1976). Eggs of Manitoba red-necked grebes had similar D D E levels in 1986; thus, the egg-cracking observed by De Smet (1987) in 1981 may have been the result of decreased shell strength not apparent from the measurements used to derive the Ratcliffe index. Consistently low contaminant levels (from the early 1970s till 1983) and the unchanged shell thickness of Alberta-nesting red-necked grebes during the D D T era, suggest that the decline in reproductive success noted by Riske (1976) in that population was unlikely to have been caused by organochlorines and eggshell thinning. The effects of human recreational activities were most likely the major cause of the decline, as evidenced by the 3-fold greater hatching success experienced by pairs breeding on small, non-recreational ponds. Similar effects of human disturbance on the nesting success of c o m m o n loons were observed on northern lakes in Saskatchewan and Ontario (Rummel & Goetzinger, 1975; Fox et al., 1980). Nevertheless, Riske (1976) reported that three red-necked grebe eggs collected from one lake had D D E and PCB levels as high as 17.8 and 39.4 mg kg t respectively, with corresponding mean shell thickness reductions of 11.8°/o, perhaps indicating a local source of contamination. Concentrations of total mercury in red-necked grebes were similar across all three provinces, suggesting that wintering areas either do not provide the source of this element, or that the degree of contamination is similar along the Atlantic and Pacific coasts. Concentrations were slightly less than those measured in the eggs of c o m m o n loons in northern Saskatchewan during the mid-1970s (mean of 0.35 mg kg ~ wet weight: Fox et al., 1980) or those of red-breasted mergansers (Mergus serrator) in Lake Michigan (mean of 0.49 nag kg ~ wet weight; Heinz et al., 1983). Reproductive success was normal in both populations. Reproductive impairment in c o m m o n loons in northwestern Ontario was associated with egg mercury concentrations >1 mg kg ~ (Barr, 1986).
ACKNOWLEDGEMENTS The authors thank L. Cocks for collecting eggs in Alberta, and H. DeVogel, R. Friesen and L. Sperling for assisting with egg collections in Saskatchewan. J. Dyck and K. Roney allowed us access to the historical egg collections at the Ontario Museum and the Saskatchewan Museum of Natural History, respectively. G. Erickson of the Provincial Museum of Alberta kindly measured eggs for Ratcliffe indices. World Wildlife Fund C a n a d a (Wildlife Toxicology Fund) supported the project in 1986 and 1987.
57
REFERENCES Anderson, D.W. & Hickey, J.J. (1972). Eggshell changes in certain North American birds. In Proceedings of the 15th International Ornithological Congress, pp. 51440. Barr, J.F. (1986). Population dynamics of the Common loon (Gavia immer) associated with mercury-contaminated waters in northwestern Ontario. Canadian Wildlife Service, Occasional Paper No. 56, 23 pp. Bishop, C.A., Weseloh, D.V., Burgess, N.M., Struger, J., Norstrom, R.J., Turle, R. & Logan, K.A. (1992). An atlas of contaminants in eggs of fish-eating colonial birds of the Great Lakes (197(~1988), Volume II: Accounts by chemical. Canadian Wildlife Service, Tech. Rep. Series No. 153, 315 pp. Boellstorff, D.E., Ohlendorf, H.M., Anderson, D.W., O'Neill, E.J., Keith, J.O. & Prouty, R.M. (1985). Organochlorine chemical residues in white pelicans and western grebes from the Klamath Basin, California. Arch. Environ. Contain. Toxieol., 14, 485-93. De Smet, K.D. (1987). Organochlorines, predators and reproductive success of the red-necked grebe in southern Manitoba. Condor, 89, 460-7. Elliott, J.E., Norstrom, R.J. & Keith, J.A. (1988). Organochlorines and eggshell thinning in northern gannets (Sula bassanus) from eastern Canada, 1968-1984. Environ. Pollut., 52, 81-102. Elliott, J.E., Noble, D.G., Norstrom, R.J., & Whitehead, P.E. (1989). Organochlorine contaminants in seabird eggs from the Pacific coast of Canada, 1971 1986. Environ. Monitor. Assess., 12, 67-82. Faber, R.A. & Hickey, J.J. (1973). Eggshell thinning, chlorinated hydrocarbons, and mercury in inland aquatic bird eggs, 1969 and 1970. Pestic. Monit. J., 7, 27 36. Fleming, W.J., Clark, D.R., Jr. & Henny, C.J. (1983). Organochlorine pesticides and PCBs: a continuing problem for the 1980s. Trans. N. Amer. Wildl. Nat. Resour. Conf, 48, 18699. Fox, G.A. (19761. Eggshell quality: its ecological and physiological significance in a DDE-contaminated common tern population. Wilson Bull., 88, 459 77. Fox, G.A., Yonge, K.S. & Sealy, S.G. (1980). Breeding performance, pollutant burden and eggshell thinning in common loons Gavia immer nesting on a boreal forest lake. Ornis. Scand., 11,243 8. Fox, G.A. & Weseloh, D.V. (1987). Colonial waterbirds as bio-indicators of environmental contamination in the Great Lakes. In The Value of Birds, ed. A.W. Diamond & F.L. Filion. ICBP Technical Publication No. 6, pp. 209-16. Haseltine, S.D., Heinz, G.H., Reichel, W.L. & Moore, J.F. (1981). Organochlorine and metal residues in eggs of waterfowl nesting on islands in Lake Michigan off Door County, Wisconsin, 1977-78. Pestic. Monit. J., 15, 90~7. Heinz, G.H., Haseltine, S.D., Reichel, W.L. & Hensler, G.L. (1983). Relationships of environmental contaminants to reproductive success in red-breasted mergansers Mergus serrator from Lake Michigan. Environ. Pollut., 32, 211-32. Henny, C.J., Blus, L.J., Krynitsky, A.J. & Bunck, C,M. (1984). Current impact of DDE on black-crowned nightherons in the intermountain west. J. Wildl. Manage., 48, 1-13. Henny, C.J., Blus, L.J. & Hulse, C.S. (1985). Trends and effects of organochlorine residues on Oregon and Nevada wading birds, 1979-83. Colonial Waterbirds, 8, 117-28. Keith, J.A. & Gruchy, I.M. (1972). Residue levels of chemical pollutants in North American birdlife. In Proceedings of the 15th International Ornithological Congress, pp. 437-54. King, K.A., Blankinship, D.R., Payne, E., Krynitsky, A.J. & Hensler, G.L. (1985). Brown pelican populations and pollutants in Texas 1975-1981. Wilson Bull., 97, 201-14. Koonz, W.H. & Rakowski, P.W. (1985). Status of colonial waterbirds nesting in southern Manitoba. Can. Field-Nat., 99, 19-29.
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D . J . Forsyth, P. A. Martin, K. D. De Smet, M. E. Riske
Lindvall, M.L. & Low, J.B. (1980). Effects of DDE, TDE, and PCBs on shell thickness of western grebe eggs, Bear River Migratory Bird Refuge, Utah--1973-74. Pestic. Monit. J., 14, 108-11. McEwen, L.C., Stafford, C.J. & Hensler, G.L. (1984). Organochlorine residues in eggs of black-crowned nightherons from Colorado and Wyoming. Environ. Toxieol. Chem., 3, 367-76. Munro, J.A. (1941). The grebes: studies of waterfowl in British Columbia. British Columbia Prov. Mus. Occasional Paper No. 3. Palmer, R.S. (1962). Handbook of North American birds, Vol. 1, New Haven, Yale Univ. Press, New Haven, CT. Pearce, P.A., Elliott, J.E., Peakall, D.B., & Norstrom, R.J. (1989). Organochlorine contaminants in eggs of seabirds in the Northwest Atlantic, 1968 1984. Environ. Pollut., 56, 217-35. Ratcliffe, D.A. (1967). Decrease in eggshell weight in certain birds of prey. Nature, 215, 208 10. Reynolds, L.M. & Cooper, T. (1975). Analysis of organochlorine residues in fish. In Water Quality Parameters, ASTM STP 573, American Society for Testing and Materials, Philadelphia, pp. 196~205. Risebrough, R.W. (1986). Pesticides and bird populations. Current Ornithol., 3, 397427. Riske, M.E. (1976). Environmental and human impacts upon grebes breeding in central Alberta. PhD thesis, University of Calgary, Calgary, Alberta, 482 pp. Rudd, R.L. & Herman, S.G. (1972). Ecosystematic transferral of pesticide residues in an aquatic environment. In Environmental Toxicology of Pesticides, ed. F. Matsumura. G.
Boush & T. Misato. Academic Press, New York, pp. 471 85. Rummel, L. & Goetzinger, C. (1975). The communication of intraspecific aggression in the common loon. Auk, 92, 333-46. SAS Institute, Inc. (1985). SAS User's Guide: Statistics, Version 5 edition. Cary, N.C. Stickel, L.F., Wiemeyer, S.N. & Blus, L.J. (1973). Pesticide residues in eggs of wild birds: adjustment for loss of moisture and lipid. Bull. Environ. Contain. Toxicol., 9, 193 6. Tate, J., Jr. (1981). The blue list for 1981: the first decade. Amer. Birds, 35, 3-10. Tate, J., Jr. (1986). The blue list for 1986. Amer. Birds, 40, 227 36. Turle, R., Norstrom, R.J. & Won, H.T. (1988). Quality assurance as applied to long-term monitoring of chemical residues and specimen banking. In Progress in Environmental Spechnen Banking, ed. S.A. Wise, R. Zeisler & G.M. Goldstein. National Bureau of Standards (USA), Special Pub. 740, pp. 171 83. Turle, R., Norstrom, R.J. & Collins, B. (1991). Comparison of PCB quantitation methods: re-analysis of archived specimens of herring gull eggs from the Great Lakes. Chemosphere, 22, 201 13. Vermeer, K. & Reynolds, L.M. (1970). Organochlorine residues in aquatic birds in the Canadian prairie provinces. Can. Field-Nat., 84, 117-30. Walker, C.H. (1983) Pesticides and bird~mechanisms of selective toxicity. Agric. Ecosystems Environ., 9, 211 26. Wetmore, A. (1924). Food and economic relations of North American grebes. U.S. Dept. Agric., Bull. No. 1196.
ORGANOCHLORINE CONTAMINANTS AND EGGSHELL T H I N N I N G IN GREBES F R O M PRAIRIE C A N A D A D.J. Forsyth a, P.A. Martin a, K.D.
De Smet b
& M.E.
Riske C
a Canadian Wildlife Service, 115 Perimeter Road, Saskatoon, Saskatchewan, S7N OX4, Canada b Manitoba Department of Natural Resources, Southwest Conservation Centre, Box 520, Melita, Manitoba ROM 1LO, Canada c R.R. #1 Camrose, Alberta T4V2M9, Canada
(Received 28 October 1992; accepted 19 March 1993)
organochlorine contaminants, including polychlorinated biphenyls (PCBs), have also been associated with reproductive impairment (Risebrough, 1986). Low reproductive success of northern gannets (Sula bassanus) in Quebec during the late 1960s was associated with a 17% reduction in mean shell thickness and DDE levels of 18.5 mg kg-~ wet weight (Elliott et al., 1988). Reductions in breeding success and increased incidence of cracked eggs of black-crowned night herons (Nycticorax nycticorax) in the western United States during the late 1970s were correlated with DDE levels and eggshell thinning (Henny et al., 1984). Effects became particularly severe at DDE concentrations above 8 mg kg j wet weight with mean reductions in shell-thickness of 13% (Henny et al., 1984). Banning the use of DDT and most other organochlorine pesticides in North America during the early 1970s resulted in reductions of residues in the eggs of most aquatic species, recovery of shell thickness to values typical of the pre-DDT era, and concomitant improvements in breeding success (Fleming et al., 1983; King et al., 1985; Fox & Weseloh, 1987). Organochlorine concentrations sufficient to cause reproductive impairment persisted in many avian populations, nonetheless (Fleming et al., 1983; Henny et al., 1985). Grebes (family Podicipedidae) occupy the upper trophic levels of inland aquatic ecosystems, feeding primarily on fish and large invertebrates (Wetmore, 1924; Munro, 1941). In recent years there has been some concern about the stability of North American grebe populations (Tate, 1981; Koonz & Rakowski, 1985; Tate, 1986). Western grebes (Aechmophorus occidentalis) in Utah with mean egg concentrations of DDE of about 5.4 mg kg I and 2.3% shell-thinning appeared to be experiencing reduced productivity in comparison to normally producing birds (Rudd & Herman, 1972; Lindvall & Low, 1980). De Smet (1987) attributed extremely low egg viability and reduced fledging success in a southwestern Manitoba population of red-necked grebes (Podiceps grisegena) in 1981, in part, to elevated mean concentrations of DDE and PCBs of 6.68 and 17.53 mg kg-1 wet weight, respectively, and associated shell-thinning of 6.5%. The purpose of this study was to determine, through a broad-scale monitoring effort, if the contaminant levels
Abstract
Eggs of five species of grebe were collected from Manitoba, Saskatchewan and Alberta during 1982-1987: red-necked (Podiceps grisegena), horned (P. auritus), eared (P. caspicus), western (Aechmophorus occidentalis) and pied-billed (Podilymbus podiceps). DDE and PCBs were present in all samples analyzed, whereas dieldrin, mirex and oxychlordane were occasionally present at low levels. Mercury was present at low levels in all samples for which it was analyzed. Red-necked grebes nesting in Manitoba had the highest contaminant levels and, assuming that contaminant burdens were accumulated principally on the wintering grounds, the mean P C B : D D E ratio (3.1) indicated that these birds and those from sites in central and eastern Saskatchewan probably wintered on the Atlantic coast. Overall low contaminant levels and a low mean P C B : D D E ratio (1.4) in the eggs of red-necked grebes breeding in Alberta and western Saskatchewan suggested that these birds wintered on the Pacific coast. A similar pattern was apparent in horned and eared grebes. Concentrations of D D E and PCB were both significantly correlated with Ratcliffe index (shell thickness), and were strongly correlated with each other. Ratcliffe indices were determined for historical collections of red-necked grebe eggs. Eggshell thickness of grebes nesting in Manitoba declined significantly during the years following the introduction of D D T (post-1947) and has only recovered partially since it was banned in 1972. The Alberta-breeding population did not appear to have undergone any significant decrease in shell thickness. INTRODUCTION
The association between shell thickness and organochlorine contamination of eggs has been documented in many aquatic bird species (Anderson & Hickey, 1972; Faber & Hickey, 1973). Their position at the top of the food web predisposes fish-eating species to accumulate lipophilic contaminants from their diet. DDE, the major metabolite of the insecticide DDT, is the contaminant most clearly correlated with shell-thinning of eggs and the resultant breakage, although other Environ. Pollut. 0269-7491/94/$07.00 © 1994 Elsevier Science Limited, England. Printed in Great Britain
51
D . J . Forsyth, P. A. Martin, K. D. De Smet, M. E. Riske
52
1-12 nests (clutches o f two o r m o r e eggs) per b r e e d i n g a r e a d u r i n g M a y to July a n d p o o l e d b y a r e a for each species. Eggs were collected at v a r i o u s stages o f laying a n d incubation; a b o u t 5 - 1 0 % were a d d l e d . In 1982 a n d 1983 b u t n o t in 1986 a n d 1987, the length a n d width o f each egg was m e a s u r e d to the nearest 0.1 m m . Eggs were opened a n d the contents were e m p t i e d into acetonerinsed glass j a r s that were sealed with a l u m i n u m foillined lids, a n d frozen. Eggshells were rinsed with water, a i r - d r i e d for at least 3 m o n t h s , weighed to the nearest 0.01 g, a n d Ratcliffe indices (Ratcliffe, 1967) o f shell thickness were calculated. Eggs were frozen a n d stored intact in plastic bags in 1986 a n d 1987. All eggs were s h i p p e d to the N a t i o n a l Wildlife R e s e a r c h Centre (Hull, Quebec) where they were i n d i v i d u a l l y h o m o genized a n d frozen; a l i q u o t s f r o m h o m o g e n a t e s were s u b s e q u e n t l y used to o b t a i n p o o l e d samples. R e s i d u e analyses o f the 1982 a n d 1983 s a m p l e s were c o n d u c t e d by the O n t a r i o R e s e a r c h F o u n d a t i o n ( O R F ; Mississauga, Ontario); analyses o f the later collections were p e r f o r m e d by M a n i t o b a E n v i r o n m e n t (Winnipeg, M a n i t o b a ) . A n a l y s i s o f s t a n d a r d i z e d reference samples o f gull egg h o m o g e n a t e b y the two l a b o r a t o r i e s d e m o n strated t h a t their results were c o m p a r a b l e a n d generally fulfilled the quality assurance criteria (Turle et al., 1988). D D E values f r o m analyses o f 1986 a n d 1987 samples (Tables 1 a n d 2) were increased b y 20.7% to c o r r e c t for l a b o r a t o r y bias relative to the reference samples.
a n d c o n c o m i t a n t r e d u c t i o n s in shell thickness o f r e d - n e c k e d grebe eggs r e p o r t e d by D e Smet (1987) in M a n i t o b a were p r e v a l e n t in grebes t h r o u g h o u t the C a n a d i a n prairies. Specific objectives were (1) to o b t a i n egg samples o f all five species o f p r a i r i e - n e s t i n g grebe for residue analysis; (2) to d e t e r m i n e the r e l a t i o n s h i p s a m o n g o r g a n o c h l o r i n e residues a n d eggshell-thinning, focusing on the r e d - n e c k e d grebe; (3) to e x a m i n e historical c h a n g e s in shell thickness o f r e d - n e c k e d grebe eggs.
METHODS
Sample collection Eggs were collected f r o m r e d - n e c k e d grebes across the prairie p r o v i n c e s o f M a n i t o b a , S a s k a t c h e w a n a n d A l b e r t a ; f r o m e a r e d grebes (Podiceps caspicus) in S a s k a t c h e w a n a n d M a n i t o b a ; a n d from western, h o r n e d (Podiceps auritus) a n d pied-billed (Podilymbus podiceps) grebes in M a n i t o b a only (Fig. 1). Collections were m a d e in 1982, 1983, 1986 a n d 1987. A b r e e d i n g a r e a was c o n s i d e r e d to be a lake, m a r s h o r g r o u p o f small w e t l a n d s in close g e o g r a p h i c p r o x i m i t y . S o m e collections m a d e in 1986 a n d 1987 were divided into samples a, b o r c (Tables 1 a n d 2), representing different l o c a t i o n s within the a r e a or s a m p l i n g dates 1 m o n t h apart. Single eggs were collected at r a n d o m from each o f
Table 1. Organochlorine and mercury concentrations (mg kg-I, wet weight) in pooled samples of red-necked grebe eggs from Manitoba, Saskatchewan and Alberta collected between 1982 and 1986 Province Breeding area
Year Number eggs
DDD
DDT
DDE
Dieldrin
12 4 3 5 3 10 6 10 1 1 2
0-01 <0-03 <0-03 0-01 <0.03 <0.03 <0-03 <0.03 <0.03 <0.03 <0-03
0-02 <0-04 <0-04 0-02 <0-04 <0.04 <0-04 <0.04 <0.04 <0.04 <0-04
3.15 3.08 2.39 3.44 4.44 2.86 3-86 2-58 7.39 3.05 2.64
0.13 0.06 0.02 0.12 0-09 0.11 0-10 0-08 0.12 0-04 0-06
0-17 b -0.17 --
Shallow Lake Lone Island Lake Duck Bay Waterhen Lake
1983 1986a 1986b 1983 1986a 1986b 1986c 1986 1986 1986 1986
Saskatchewan 8. Prince Albert Park 9. Little Manito Lake 10. Minnow Lake 11. Reflex Lake 12. Moose Mountain Park
1982 1983 1983 1983 1983
5 10 5 10 10
0.11 <0.01 <0.01 <0.01 0.01
<0-01 <0.01 <0.01 <0-01 0-01
1-62 1.20 0.42 0.26 3.63
0.02 0.01 <0.01 <0-01 0-06
Alberta 13. Lac Ste. Anne 14. Wizard Lake 15. Wabamum Lake 16. Woods Lake
1982 1982 1982 1983
10 10 9 10
0.06 0-01 0.07 <0.01 0.07 <0-01 <0.01 <0.01
0-33 0.49 0.44 0.59
<0-01 <0-01 <0-01 0.01
Manitoba 1. Turtle Mountain Park 23 May 26 June 2. North Shoal Lake 3. Sandy Lake area
4. 5. 6. 7.
OxyMirex PCB" Total Ratcliffe index chlordane (1:1) mercury mean (SD)
0-67 0.28 0-38 0.19 0.34 0.35 0-46 0.20 1.63 0.24 0.06
10-80 8.96 5-64 7.96 13.44 10.02 16.18 7.66 21-00 8.73 10-50
0-09 --0.11 --------
1.76 (0.14)
0.03 0.05 0.01 0.01 0.16
0.31 0.04 <0.01 <0.01 <0.01
5-98 1.47 0.46 0.29 6-58
0-11 0.08 0.07 0.21 0.09
1.71 1.85 1.85 1.81 1.81
<0.01 0.01 0.01 0.06
<0.01 <0.01 <0.01 0.03
0.16 0.62 0.32 1.85
0.07 0.15 0.10 0.09
1-80 (0-I1) 1.84 (0.13) 1.90 (0.15) 1.81 (0.10)
------
Samples designated a, b or c were collected 1 month apart or from different locations within the breeding area. "Single peak estimate of 1:1 Aroclors 1254:1260 (Turle et al., 1988). b 1986 samples not analyzed for oxychlordane or mercury and not measured for Ratcliffe index calculation.
-1.65 (0.13) -------(0.19) (0.16) (0.18) (0.09) (0.17)
53
Organochlorine contaminants and eggshell thinning in grebes
ALBERTA
SASKATCHEWAN /
/
MANITOBA
/ o
MONTANA
USA
l
• ~'-'-~MINNESOTA NORTHDAKOTA
Fig. 1. Locations of red-necked (filled circle), eared (filled triangle), horned (filled square), pied-billed (unfilled circle) and western (unfilled square) grebe egg collection areas in Manitoba, Saskatchewan and Alberta, Canada. Locations from which eggs of two species were collected are shown as filled circles. Numbers refer to areas listed in Tables 1 and 2. Red-necked grebe eggshells from private a n d museum collections were weighed a n d m e a s u r e d for calculations o f Ratcliffe indices. Eggshells were from A l b e r t a , S a s k a t c h e w a n , M a n i t o b a a n d the K e n o r a district in n o r t h e r n O n t a r i o (near the M a n i t o b a b o r d e r ) a n d collection dates ranged f r o m 1895 to 1984. Egg collection dates were divided into three time p e r i o d s for c o m p a r i s o n o f Ratcliffe indices: the p r e - D D T era, p r i o r to 1947: the p e r i o d o f D D T use, between 1948 a n d
1971; a n d the p e r i o d following the b a n n i n g o f D D T use in N o r t h A m e r i c a , 1972 1983.
Residue analysis P o l y c h l o r i n a t e d biphenyls (PCBs), D D T a n d its two m e t a b o l i t e s D D D a n d D D E (p,p' isomers), dieldrin, h e p t a c h l o r epoxide, the c h l o r d a n e - r e l a t e d c o m p o u n d s except o x y c h l o r d a n e , a n d mirex were d e t e r m i n e d every year. M e r c u r y a n d o x y c h l o r d a n e were m e a s u r e d only
Table 2. Organochlorine concentrations (mg kg=l, wet weight) in pooled samples of eared, horned, pied-billed and western grebe eggs from Manitoba and Saskatchewan, collected between 1982 and 1987 Species Breeding area
Year
Number eggs
DDD
DDT
DDE
Dieldrin
Mirex
PCB" ( 1:1 )
1982 1983 1986 1986 1986 1986 1986 1986
5 10 5 5 10 10 10 10
0.07 <0-01 <0-03 <0-03 <0.03 <0.03 <0.03 <0.03
0.01 <0.01 <0-04 <0.04 <0.04 <0-04 <0-04 <0-04
0.80 0-51 0.63 0.31 0.72 0.99 0.41 0.92
<0.01 <0.01 <0.02 <0-02 <0-02 <0.02 <0-02 <0-02
<0.01 <0.01 <0-05 <0.05 <0-05 <0.05 <0-05 <0.05
0.16 0.06 0-38 <0-01 <0.01 <0.01 <0.01 <0.01
Horned grebe 3. Sandy Lake area, Man. 7. Waterhen Lake, Man. 24. Southwestern Manitoba 25. Minnedosa, Man. 25. Minnedosa, Man.
1986 1986 1986 1986 1987
2 4 4 7 5
<0.03 <0-03 <0.03 <0-03 <0-03
<0.04 <0.04 <0.04 <0.04 <0.04
1.50 0.78 1-28 0.69 1.47
0-02 <0-02 <0.02 <0.02 0.02
<0-05 <0.05 <0.05 <0.05 <0.05
6.28 1.75 2.46 2.24 4.42
Pied-billed grebe 25. Minnedosa (a), Man. 25. Minnedosa (b), Man. 26. Gull Lake, Man.
1987 1987 1986
5 5 2
<0.03 <0.03 <0.03
<0.04 <0.04 <0-04
1-47 0.75 0.25
<0-02 <0-02 <0.02
<0-05 <0.05 <0.05
1.02 0.38 0.83
Western grebe 6. Duck Bay (a), Man. 6. Duck Bay (b), Man. 27. Ninette (a), Man., 26 June 27. Ninette (b), Man., 22 July
1986 1986 1986 1986
10 4 10 10
0.29 0-58 0-47 0-66
<0-04 <0.04 <0.04 <0.04
0.70 0.84 2.60 3-37
<0-02 <0.02 <0-02 <0.02
<0.05 <0.05 <0.05 <0-05
2.55 2.08 4.22 4-67
Eared 17. 18. 19. 19. 20. 21. 22. 23.
grebe Bradwell, Sask. Grave Lake, Sask. Proven Lake (a), Man. Proven Lake (b), Man. Oak Hammock, Man. Winnipegosis Lake, Man Dog Lake, Man. Plum Lake, Man.
Samples designated a and b were collected 1 month apart or from different locations within the breeding area. u Single peak estimate of 1:t ratio of Aroclors 1254:1260 (Turle et al., 1988).
54
D. J. Forsyth, P. A. Martin, K. D. De Smet, M. E. R&ke RESULTS
in 1982 and 1983. Analyses for organochlorines, by capillary column gas c h r o m a t o g r a p h y (GC), followed the procedures of Reynolds & Cooper (1975): detection limits were 0.01 mg kg ~ wet weight in 1982 and 1983. Detection limits for the 1986 and 1987 samples were 0.03, 0.04, 0.02 and 0.05 mg kg ~ for D D D , D D T , dieldrin and mirex, respectively. PCBs are expressed as a 1:1 ratio of Aroclors 1254:1260 (Turle et al., 1988) and detection limits in all years were 0.01 mg kg ~. These values are about 2-fold higher than those based on sums of PCB congeners, but can be compared to earlier studies (Turle et al., 1991). Mercury was analyzed by O R F using cold vapor atomic absorption following digestion of samples with sulphuric and nitric acids at 60°C. Potassium permanganate was used to oxidize organic material and the excess was reduced by the addition of hydroxylamine hydrochloride and, immediately prior to analysis, by stannous chloride. Residues were reported on a wet weight basis. We were unable to correct for moisture loss (Stickel et al., 1973) as moisture content was not measured in eggs from 1986 or 1987. Transformation (log~0) of the data for statistical analysis was effective in reducing the heterogeneity of variance that is typical of contaminant data. Residue values reported are means and 95% confidence intervals. For the calculation of means, concentrations below detection limits were arbitrarily given the value of zero. We used the General Linear Model Procedure of SAS (SAS Institute Inc., 1985) to perform analyses of variance (ANOVA) and Tukey's honestly significant difference (HSD) tests for means separation. The Stepwise Procedure was used to conduct a stepwise multiple regression of D D E , dieldrin and PCB concentrations in pooled rednecked grebe egg samples collected in 1982 and 1983 (n -- 11) on the mean Ratcliffe index of the eggs within those pools. We then determined Pearson's correlation coefficients among the variables using the Correlation Procedure. Significance was inferred at p < 0.05.
A total of 20 samples (18 pooled, 2 12 eggs each; 2 single eggs) of red-necked grebe eggs and eight samples (5-10 eggs each) of eared grebe eggs was collected between 1982 and 1987 (Tables 1 and 2). Four, five and three samples (2-10 eggs each) of western, horned and piedbilled grebe eggs, respectively, were collected during 1986 and 1987 only (Table 2). Significant D D E and PCB residues were detected in all samples (Tables 1 and 2), with the exception of most Manitoba eared grebe eggs, in which PCBs were below detection limits (Table 2). D D T and D D D were detected in one Saskatchewan eared grebe sample. All western grebe samples contained D D D (Table 2). Dieldrin and mirex were found primarily in eggs of Manitoba-nesting rednecked grebes, but also in two Saskatchewan samples and one Alberta sample (Table 1). These compounds were below detection limits in eared, homed, pied-billed and western grebe eggs (Table 2). The chlordane-related compounds and heptachlor epoxide were below detection limits in most samples; however low levels (< 0.2 mg kg ~) of oxychlordane were measured in the majority of red-necked grebe eggs collected in 1982 and 1983. Mercury was detected in all samples for which it was analyzed (red-necked grebe eggs, 1982 and 1983: Table 1) and concentrations were generally close to 0.1 mg kg Levels of D D E , PCBs, dieldrin and mirex as well as the ratio of PCB:DDE were compared among rednecked grebe eggs from the three provinces and with the other four species (Table 3). Concentrations of these compounds were significantly higher in the eggs of red-necked grebes from Manitoba than in those from Alberta and Saskatchewan, or in those of eared, horned and pied-billed grebes (Table 3). Western grebe eggs had levels of D D E that were intermediate between those of Manitoba red-necked grebe eggs and those of
Table 3. Comparisons of residues (mg kg-I, wet weight, geometric mean and 95% confidence intervals) of DDE, PCB, mirex and dieldrin and PCB:DDE ratios (arithmetic mean and SE) among the eggs of five species of prairie-nesting grebe
Species
Number
DDE
Red-necked (Manitoba) Red-necked (Saskatchewan) Red-necked (Alberta) Eared
11
3.20" (2.66-3.82) 1.09f' (0.15 2 . 8 0 ) 0.45 ~ (0.32 1.29) 0.64 ~ (0-49-0.81 ) 1.11 h (0.82-1.46) 0.75 t' (0.24-1.49) 1-65"t' (0.71 3.10)
5 4 8
Horned
5
Pied-billed
3
Western
4
PCB 9-96" (8-12 1 2 . 1 8 ) 1.46~'' (0-07-4.62) 0.62' (0-07 1.46) 0.19' (0.02-0-40) 3.14~ (1.89493) 0.72 h'' (0.37-1.17) 3.76h (2.55 5.40)
Mirex
Dieldrin
0.38" (0.20-0.59) 0.02 h
ND b
0.07" (0.05 0.10) 0.02 h (0-0.07) ND ~ ND h
ND h
ND b
ND h
ND h
ND h
ND h
0.02 b
PCB:DDE 3.1" (0.2) 1.8~ (0.1) 1.4t' (0.6) 0.1' (0.07) 2.9" (0.7) 1.6h (0-91) 2.3 ''h (0.5)
ND = residues below detection limits: equivalent to zero in statistical analysis. ..h., Means within a column sharing the same superscript are not significantly different (p > 0-05: ANOVA and Tukey's HSD test).
Organochlorine contaminants and eggshell thinning in grebes Table 4. Ratcliffe indices (mean __ SE, n) of red-necked grebe eggs from Manitoba, Saskatchewan and Alberta before, during and following the ban of DDT use in North America
Manitoba a Pre-1947h
1-80 + 0.02 Aa 33 1948 1971h 1.49_+0-05 Ab 10 1972-1983 ~ 1.70 + 0-03 Ac 31
Saskatchewan"
Albertaa
1-78+ 0-03 Aa 19 1.56+ 0.10 Ab 10 1.79_+0-02 Ba 46
1.82+ 0.03 Aa 29 1.85+ 0.01 Ba 253 1-84+ 0-02 Ba 77
"Means within a column sharing a lower case letter in common are not significantly different (p > 0.05: ANOVA and Tukey's HSD test). Means within a row sharing an upper case letter in common are not significantly different (p > 0.05: ANOVA and Tukey's HSD test). all other populations (Table 3). The ratio of PCB to D D E was highest in the Manitoba population of rednecked grebes and horned grebes, whereas eared grebes had significantly lower ratios than all other species (Table 3). In a multiple regression of DDE, dieldrin and PCBs on Ratcliffe index of red-necked grebe eggs from 1982 and 1983, PCBs accounted for the greatest variation in the relationship, having a partial R 2 of 0.60. The added contributions of D D E and dieldrin to the model were insignificant (DDE: partial R 2 -- 0.035, p -- 0.41; dieldrin: partial R z -- 0.074, p = 0.23); however, all three independent variables were highly intercorrelated (r values > 0.85), with PCBs and D D E having a correlation coefficient of 0.95. Correlation coefficients of DDE, dieldrin and PCBs with Ratcliffe index were high ( 0.67, 0.76 and 0.77, respectively). Considerable information is lost by regressing pooled sample contaminant concentrations against mean Ratcliffe indices, compared to a regression using data for individual eggs. The significant interaction, in a two-way ANOVA, between the effects of province and historical period on Ratcliffe indices of red-necked grebe eggs indicated that eggshell thickness changed over time differently among the three provinces. A subsequent one-way A N O V A revealed no differences a m o n g the provinces during the p r e - D D T era, and the overall mean Ratcliffe index was 1.80 (Table 4). During the period of D D T use (1948-1971) however, grebe eggs from Saskatchewan and Manitoba underwent significant reductions in Ratcliffe index (14 and 18%, respectively) while Alberta eggs remained unaffected (Table 4). In the years since the banning of D D T (post-1972) Saskatchewan grebe eggs returned to p r e - D D T levels, while the Ratcliffe index of Manitoba grebe eggs recovered slightly, to a mean level 8°/,, lower than the p r e - D D T mean (Table 4). DISCUSSION All eggs in our study were collected in areas remote from industrial pollution. The fact that some of the
55
highest concentrations of PCB were found in grebe eggs from inside or close to provincial and national
parks suggests strongly that most of the contaminant burden in these birds was accumulated during winter or spring migration. The high P C B : D D E ratio (3.1) in eggs of red-necked grebes from Manitoba is similar to the 3:1 ratio that is characteristic of birds wintering or staging on the Atlantic coast and the Great Lakes, where elevated levels of the industrial contaminant PCB predominate. In contrast, the overall low PCB levels and approximately 1:1 P C B : D D E ratio found in eggs of Alberta-nesting red-necked grebes is typical of birds wintering on the Pacific coast (Keith & Gruchy, 1972). Although red-necked grebes are known to winter on both coasts, the dividing line between eastern and western migrants is not known (Palmer, 1976). The elevated PCB levels and PCB:DDE ratios of 3.7 and 1.8 of eggs from the central and eastern Saskatchewan collection areas (Prince Albert Park and Moose Mountain Park, respectively; Fig. 1) suggest that birds breeding in these regions probably also wintered on the Atlantic coast. Fox et al. (1980) concluded that c o m m o n loons (Gavia #nmer), nesting in northeastern Saskatchewan, with eggs containing a mean PCB:DDE ratio of 2.4, wintered along the Atlantic coast, while Alberta-nesting populations with P C B : D D E ratios of 0.7, wintered along the Pacific coast. The presence of mirex at significant levels in all samples of Manitoba red-necked grebe eggs, as well as the Prince Albert sample, supports the hypothesis that these birds spent some time during migration on the lower Great Lakes, where mirex occurs consistently. Mirex concentrations ranging from 0.20 to 1.63 mg kg ~ in these samples are comparable to those in the eggs of resident herring gulls collected from Hamilton Harbour, Lake Ontario between 1981 and 1987 (annual means range from 0.58 to 2.35 nag kg t; Bishop et al., 1992). It is unlikely that the mirex in rednecked grebe eggs from Manitoba originated on either the Atlantic or Pacific coast because eggs of piscivorous birds from both coasts contained at least 10-fold lower concentrations of mirex during the 1980s than did our eggs (Elliott et al., 1989; Pearce et al., 1989). The generally lower organochlorine levels in eared, horned and pied-billed grebes in comparison to rednecked grebes, probably reflect the relatively high proportion of fish eaten by red-necked grebes (56%) compared to the other species (Wetmore, 1924; Munro, 1941). The very low P C B : D D E ratio found in eared grebe eggs is consistent with this species wintering on the Pacific coast, in large western inland water bodies and in Mexico (Palmer, 1962). Although horned grebes winter on both coasts, the Manitoba-nesting populations of this study probably migrate to the eastern coast, hence accumulating a proportionately greater burden of PCBs relative to DDE. Unlike the other species of grebe, the pied-billed grebe does not winter coastally, but prefers small inland ponds in the southern United States and throughout Central and South America (Palmer, 1976). The low PCB levels and intermediate P C B : D D E ratio (1.6) indeed suggest that these
56
D. J. Forsvth, P. A. Martin, K. D. De Smet, M. E. Riske
grebes are avoiding heavily industrialized Atlantic coastal regions, although our sample represents only two breeding areas. Western grebes are the most piscivorous of all North American grebes, with fish comprising up to 81% of the winter diet (Palmer, 1962) and contributing to their relatively high contaminant burden. Walker (1983) has shown, however, that fish-eating birds exhibit very low activity of hepatic mixed-function oxidases, the enzymes responsible for the metabolism of toxic substances including organochlorines. Toxicant metabolism generally decreases with increasing body mass, perhaps further explaining the high contaminant levels in western and red-necked grebes relative to the three smaller species (Walker, 1983). Western grebes are known to winter along the Pacific coast and inland through California and Mexico but not along the Atlantic coast (Palmer, 1962). Their PCB:DDE ratio (2.3) approaches that typical of Atlantic-wintering birds, nonetheless, suggesting that they may winter in bays receiving industrial, as opposed to agricultural, runoff (Henny et al., 1985). The fact that all samples contained DDD, a short-lived metabolite of DDT, is indicative of fairly recent exposure to DDT. The PCB, D D E and D D D levels were similar to those detected in a larger sample of western grebe eggs from the Klamath Basin, California in 1981 (Boellstorff et al., 1985). Mean DDE and PCB residues of the eastern-migrating population of red-necked grebes were somewhat lower in the current study in comparison to those measured in southwestern Manitoba in 1981 (De Smet, 1987). The two samples collected from Turtle Mountain Park in 1986 averaged 2.74 and 7.30 mg kg t for DDE and PCBs, respectively, compared to mean residues of 6.68 and 17.53 mg kg ', respectively, in samples collected from the same park in 1981 (De Smet, 1987). Eggs collected from other areas in Manitoba during 1986 contained residues similar to those of the 1981 sample mean, however, suggesting that overall, contamination had not declined appreciably between 1981 and 1986 in eastern-migrating red-necked grebes. Residues were nonetheless well below those of another eastern population (Wisconsin) measured during 1970 (54.5 and 62.8 mg kg ~, D D E and PCBs, respectively; Faber & Hickey, 1973). Concentrations of DDE reported in the literature are considered to be relatively reliable, regardless of advances in analytical methodology, but PCBs reported prior to 1974 are probably underestimated because of changes in methods of PCB quantitation based on Aroclor mixtures (Turle et al., 1988). Thus, any declines in PCB levels apparent by comparing our data with those from the earlier analyses are probably also underestimates. Concentrations of D D E in horned grebe eggs in our study (1.11 mg k g ' ) were substantially lower than the 5.13 mg k g ' found in samples collected from Saskatchewan during the late 1960s (Vermeer & Reynolds, 1970). D D E levels were also considerably lower than those in samples collected from Alberta in
1971 (2.56 mg kg i; Riske, 1976), although PCB levels were similar (3.14 versus 4.24 mg kg 1; Riske, 1976). A comparison of mean D D E residues in western grebe samples taken in 1986 (1.65 mg kg 1) to those taken from Alberta in 1969 and 1971 (7.76 and 4.88 mg kg 1 respectively) and Saskatchewan in 1969 (3.70 mg kg 1) reveals a similar decline (Vermeer & Reynolds, 1970; Riske, 1976). Reductions in D D E residues probably reflect the cessation of the usage of D D T in agricultural areas along the west coast wintering grounds of western grebes and probably of Alberta-nesting horned grebes. However, DDE levels in eared grebe eggs collected in Manitoba and Saskatchewan from 1982 to 1986 were similar to those in eggs analyzed in Saskatchewan in 1969 (0.55 mg kg ~) and in Alberta in 1976 (1.06 mg kg ') (Vermeer & Reynolds, 1970; Riske, 1976). No early data are available for contaminant levels in the eggs of pied-billed grebes nesting on the Canadian prairies: levels of DDE and PCBs in a Wisconsin-nesting population in 1970 were 10-fold greater than those of our samples (6.61 and 6.21 mg kg ~, respectively; Faber & Hickey, 1973), indicating either large population differences or a decline in contaminant levels over time. Analysis of historical red-necked grebe eggshell thickness data indicated that eastern populations (Manitoba-nesting; see Table 4) underwent reductions in shell thickness during the D D T era from which they had not yet completely recovered by 1983, whereas western populations (Alberta-nesting) maintained shell thickness throughout that time. Lack of information about the migratory routes and wintering grounds of Saskatchewan-nesting birds makes interpretation of shell thinning trends in that province difficult. The correlation between DDE and Ratcliffe index observed in rednecked grebe eggs has been demonstrated in many other species of inland aquatic birds (Fox et al., 1980; Lindvall & Low, 1980; Haseltine et al., 1981; McEwen et al., 1984). The existence of this relationship, in combination with the increase in shell thickness apparent since 1972 in eastern prairie populations of red-necked grebes, suggests that D D E levels were higher in these populations prior to the banning of DDT. Residue data for Manitoba-nesting red-necked grebes during the D D T era are not available, however, for comparison to our values and those of De Smet (1987). De Smet (1987) found high variability in shell thickness indices, and although the mean degree of shell thinning relative to pre-DDT shells was only 4.6% (compared to our Ratcliffe index value of 1.8 for prairie-nesting populations), shells of individual eggs were as much as 39% thinner. He found a high incidence of cracked eggs, and attributed the high rate of single egg disappearance between nest checks (8.3%) to cracking of thin-shelled eggs that were subsequently ejected from the nest by parents (De Smet, 1987). Shell thickness need not be significantly decreased for an overall loss in shell strength to occur. Both D D E and PCBs are known to cause a reduction in density of shell pores and mammillae resulting in decreased shell quality, although the relation-
Organochlorine contaminants and eggshell thinning in grebes
ship with PCBs is less well documented (reviewed in Risebrough, 1986). An Alberta colony of common terns (Sterna hirundo) with a mean egg D D E content of 3.98 mg kg ~ and almost undetectable PCB levels exhibited a strong positive correlation between shell pore and mammillae densities and egg success, whereas shell thickness was unrelated and not significantly lower than p r e - D D T thickness (Fox, 1976). Eggs of Manitoba red-necked grebes had similar D D E levels in 1986; thus, the egg-cracking observed by De Smet (1987) in 1981 may have been the result of decreased shell strength not apparent from the measurements used to derive the Ratcliffe index. Consistently low contaminant levels (from the early 1970s till 1983) and the unchanged shell thickness of Alberta-nesting red-necked grebes during the D D T era, suggest that the decline in reproductive success noted by Riske (1976) in that population was unlikely to have been caused by organochlorines and eggshell thinning. The effects of human recreational activities were most likely the major cause of the decline, as evidenced by the 3-fold greater hatching success experienced by pairs breeding on small, non-recreational ponds. Similar effects of human disturbance on the nesting success of c o m m o n loons were observed on northern lakes in Saskatchewan and Ontario (Rummel & Goetzinger, 1975; Fox et al., 1980). Nevertheless, Riske (1976) reported that three red-necked grebe eggs collected from one lake had D D E and PCB levels as high as 17.8 and 39.4 mg kg t respectively, with corresponding mean shell thickness reductions of 11.8°/o, perhaps indicating a local source of contamination. Concentrations of total mercury in red-necked grebes were similar across all three provinces, suggesting that wintering areas either do not provide the source of this element, or that the degree of contamination is similar along the Atlantic and Pacific coasts. Concentrations were slightly less than those measured in the eggs of c o m m o n loons in northern Saskatchewan during the mid-1970s (mean of 0.35 mg kg ~ wet weight: Fox et al., 1980) or those of red-breasted mergansers (Mergus serrator) in Lake Michigan (mean of 0.49 nag kg ~ wet weight; Heinz et al., 1983). Reproductive success was normal in both populations. Reproductive impairment in c o m m o n loons in northwestern Ontario was associated with egg mercury concentrations >1 mg kg ~ (Barr, 1986).
ACKNOWLEDGEMENTS The authors thank L. Cocks for collecting eggs in Alberta, and H. DeVogel, R. Friesen and L. Sperling for assisting with egg collections in Saskatchewan. J. Dyck and K. Roney allowed us access to the historical egg collections at the Ontario Museum and the Saskatchewan Museum of Natural History, respectively. G. Erickson of the Provincial Museum of Alberta kindly measured eggs for Ratcliffe indices. World Wildlife Fund C a n a d a (Wildlife Toxicology Fund) supported the project in 1986 and 1987.
57
REFERENCES Anderson, D.W. & Hickey, J.J. (1972). Eggshell changes in certain North American birds. In Proceedings of the 15th International Ornithological Congress, pp. 51440. Barr, J.F. (1986). Population dynamics of the Common loon (Gavia immer) associated with mercury-contaminated waters in northwestern Ontario. Canadian Wildlife Service, Occasional Paper No. 56, 23 pp. Bishop, C.A., Weseloh, D.V., Burgess, N.M., Struger, J., Norstrom, R.J., Turle, R. & Logan, K.A. (1992). An atlas of contaminants in eggs of fish-eating colonial birds of the Great Lakes (197(~1988), Volume II: Accounts by chemical. Canadian Wildlife Service, Tech. Rep. Series No. 153, 315 pp. Boellstorff, D.E., Ohlendorf, H.M., Anderson, D.W., O'Neill, E.J., Keith, J.O. & Prouty, R.M. (1985). Organochlorine chemical residues in white pelicans and western grebes from the Klamath Basin, California. Arch. Environ. Contain. Toxieol., 14, 485-93. De Smet, K.D. (1987). Organochlorines, predators and reproductive success of the red-necked grebe in southern Manitoba. Condor, 89, 460-7. Elliott, J.E., Norstrom, R.J. & Keith, J.A. (1988). Organochlorines and eggshell thinning in northern gannets (Sula bassanus) from eastern Canada, 1968-1984. Environ. Pollut., 52, 81-102. Elliott, J.E., Noble, D.G., Norstrom, R.J., & Whitehead, P.E. (1989). Organochlorine contaminants in seabird eggs from the Pacific coast of Canada, 1971 1986. Environ. Monitor. Assess., 12, 67-82. Faber, R.A. & Hickey, J.J. (1973). Eggshell thinning, chlorinated hydrocarbons, and mercury in inland aquatic bird eggs, 1969 and 1970. Pestic. Monit. J., 7, 27 36. Fleming, W.J., Clark, D.R., Jr. & Henny, C.J. (1983). Organochlorine pesticides and PCBs: a continuing problem for the 1980s. Trans. N. Amer. Wildl. Nat. Resour. Conf, 48, 18699. Fox, G.A. (19761. Eggshell quality: its ecological and physiological significance in a DDE-contaminated common tern population. Wilson Bull., 88, 459 77. Fox, G.A., Yonge, K.S. & Sealy, S.G. (1980). Breeding performance, pollutant burden and eggshell thinning in common loons Gavia immer nesting on a boreal forest lake. Ornis. Scand., 11,243 8. Fox, G.A. & Weseloh, D.V. (1987). Colonial waterbirds as bio-indicators of environmental contamination in the Great Lakes. In The Value of Birds, ed. A.W. Diamond & F.L. Filion. ICBP Technical Publication No. 6, pp. 209-16. Haseltine, S.D., Heinz, G.H., Reichel, W.L. & Moore, J.F. (1981). Organochlorine and metal residues in eggs of waterfowl nesting on islands in Lake Michigan off Door County, Wisconsin, 1977-78. Pestic. Monit. J., 15, 90~7. Heinz, G.H., Haseltine, S.D., Reichel, W.L. & Hensler, G.L. (1983). Relationships of environmental contaminants to reproductive success in red-breasted mergansers Mergus serrator from Lake Michigan. Environ. Pollut., 32, 211-32. Henny, C.J., Blus, L.J., Krynitsky, A.J. & Bunck, C,M. (1984). Current impact of DDE on black-crowned nightherons in the intermountain west. J. Wildl. Manage., 48, 1-13. Henny, C.J., Blus, L.J. & Hulse, C.S. (1985). Trends and effects of organochlorine residues on Oregon and Nevada wading birds, 1979-83. Colonial Waterbirds, 8, 117-28. Keith, J.A. & Gruchy, I.M. (1972). Residue levels of chemical pollutants in North American birdlife. In Proceedings of the 15th International Ornithological Congress, pp. 437-54. King, K.A., Blankinship, D.R., Payne, E., Krynitsky, A.J. & Hensler, G.L. (1985). Brown pelican populations and pollutants in Texas 1975-1981. Wilson Bull., 97, 201-14. Koonz, W.H. & Rakowski, P.W. (1985). Status of colonial waterbirds nesting in southern Manitoba. Can. Field-Nat., 99, 19-29.
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D . J . Forsyth, P. A. Martin, K. D. De Smet, M. E. Riske
Lindvall, M.L. & Low, J.B. (1980). Effects of DDE, TDE, and PCBs on shell thickness of western grebe eggs, Bear River Migratory Bird Refuge, Utah--1973-74. Pestic. Monit. J., 14, 108-11. McEwen, L.C., Stafford, C.J. & Hensler, G.L. (1984). Organochlorine residues in eggs of black-crowned nightherons from Colorado and Wyoming. Environ. Toxieol. Chem., 3, 367-76. Munro, J.A. (1941). The grebes: studies of waterfowl in British Columbia. British Columbia Prov. Mus. Occasional Paper No. 3. Palmer, R.S. (1962). Handbook of North American birds, Vol. 1, New Haven, Yale Univ. Press, New Haven, CT. Pearce, P.A., Elliott, J.E., Peakall, D.B., & Norstrom, R.J. (1989). Organochlorine contaminants in eggs of seabirds in the Northwest Atlantic, 1968 1984. Environ. Pollut., 56, 217-35. Ratcliffe, D.A. (1967). Decrease in eggshell weight in certain birds of prey. Nature, 215, 208 10. Reynolds, L.M. & Cooper, T. (1975). Analysis of organochlorine residues in fish. In Water Quality Parameters, ASTM STP 573, American Society for Testing and Materials, Philadelphia, pp. 196~205. Risebrough, R.W. (1986). Pesticides and bird populations. Current Ornithol., 3, 397427. Riske, M.E. (1976). Environmental and human impacts upon grebes breeding in central Alberta. PhD thesis, University of Calgary, Calgary, Alberta, 482 pp. Rudd, R.L. & Herman, S.G. (1972). Ecosystematic transferral of pesticide residues in an aquatic environment. In Environmental Toxicology of Pesticides, ed. F. Matsumura. G.
Boush & T. Misato. Academic Press, New York, pp. 471 85. Rummel, L. & Goetzinger, C. (1975). The communication of intraspecific aggression in the common loon. Auk, 92, 333-46. SAS Institute, Inc. (1985). SAS User's Guide: Statistics, Version 5 edition. Cary, N.C. Stickel, L.F., Wiemeyer, S.N. & Blus, L.J. (1973). Pesticide residues in eggs of wild birds: adjustment for loss of moisture and lipid. Bull. Environ. Contain. Toxicol., 9, 193 6. Tate, J., Jr. (1981). The blue list for 1981: the first decade. Amer. Birds, 35, 3-10. Tate, J., Jr. (1986). The blue list for 1986. Amer. Birds, 40, 227 36. Turle, R., Norstrom, R.J. & Won, H.T. (1988). Quality assurance as applied to long-term monitoring of chemical residues and specimen banking. In Progress in Environmental Spechnen Banking, ed. S.A. Wise, R. Zeisler & G.M. Goldstein. National Bureau of Standards (USA), Special Pub. 740, pp. 171 83. Turle, R., Norstrom, R.J. & Collins, B. (1991). Comparison of PCB quantitation methods: re-analysis of archived specimens of herring gull eggs from the Great Lakes. Chemosphere, 22, 201 13. Vermeer, K. & Reynolds, L.M. (1970). Organochlorine residues in aquatic birds in the Canadian prairie provinces. Can. Field-Nat., 84, 117-30. Walker, C.H. (1983) Pesticides and bird~mechanisms of selective toxicity. Agric. Ecosystems Environ., 9, 211 26. Wetmore, A. (1924). Food and economic relations of North American grebes. U.S. Dept. Agric., Bull. No. 1196.