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Perc removal


PCBs, DDE, DDT, and TCDD-EQ in 
Two Species of Albatross on 
Sand Island, Midway Atoll, North Pacific Ocean 

Environmental Toxicology and Chemistry, v.16, n.3, Mar97

HEIDI J. AUMAN,† JAMES P. LUDWIG,‡ CHERYL L. SUMMER,‡ DAVID A. VERBRUGGE,† KENNETH L. FROESE, † THEO COLBORN§ and JOHN P. GIESY*†

† Department of Fisheries and Wildlife, Pesticide Research Center and Institute of Environmental Toxicology, Natural Resources, Michigan
State University, East Lansing, Michigan 48824-1222, USA
‡ The SERE Group, Ltd., 1380 Road 2W, Kingville, Ontario N9Y 2Z6, Canada
§World Wildlife Fund, 1250 24th Street NW, Washington, DC 20037, USA
* To whom correspondence may be addressed.

(Received 26 February 1996; Accepted 24 June 1996)

Abstract-Concentrations of total polychlorinated biphenyls (PCBs) and organochlorine insecticides, including the 1, 1, 1 -trichloro-2, 2'-bis-p-chlorophenyl-ethane (DDT) complex, were measured in the plasma of chicks and adults and in eggs of Laysan albatrosses (Diomedea immutabilis) and black-footed albatrosses (Diomedea nigripes) in a remote area of the central North Pacific Ocean. Significant differences in total concentrations of PCBs, DDT, and 1, 1-dichloro-2,2'-bis-p-chlorophenyl-ethylene (DDE) in the plasma were detected between species and among sampling periods. Current concentrations of DDE in eggs of Laysan albatrosses are well below the threshold for eggshell thinning, based on the sensitivities of other fish-eating birds, whereas concentrations of DDE in eggs of black-footed albatrosses were approximately one-half of the threshold concentrations necessary for eggshell thinning. The shells of Laysan and black-footed albatross eggs are not currently exhibiting significant thinning that is resulting in population-level effects. Current concentrations of PCBs are near those that could be having subtle population-level effects in the black-footed albatross, but not in the Laysan albatross. The hazard posed to the albatrosses by current concentrations of PCBs was assessed by calculating a hazard quotient (HQ), based on composite dose-response relationships for other species. Dioxin equivalents (TEq) based on mammalian toxic equivalency factors resulted in the greatest HQ, which was near the concentration when embryo lethality and deformities are observed in fish-eating colonial waterbirds of the North American Great Lakes. Current concentrations of both PCBs and the DDT complex were similar to those in some species of piscivorous birds of the North American Great Lakes region.

Keywords-Organochlorine insecticides Dioxin equivalents Black-footed albatross Laysan albatross

INTRODUCTION

As a result of human activities, the global environment has become contaminated with synthetic hydrocarbons in complex mixtures [ I], but the toxic effects resulting from exposure to these polyhalogenated aromatic hydrocarbons (PHAHs) on wildlife have been difficult to establish [2]. The accumulation of PHAHs by birds has been studied in a number of locations [3]. These studies have been primarily in areas such as the North American Great Lakes that are known to be contaminated to a degree significant enough to cause adverse effects [ 1,2]. Fewer studies have addressed the issue of global contamination, especially in remote locations that are not directly impacted by local sources of contamination. One such location is the central North Pacific Ocean.

Two widely distributed synthetic PHAHs that have caused adverse effects in wildlife are polychlorinated biphenyls (PCBs) and 1,1-dichloro-2,2'-bis-p-chlorophenyl-ethylene (DDE) [2,3]. Polychlorinated biphenyls form a major group of persistent, bioaccumulating, environmental contaminants that have been detected ubiquitously in the environment [3]. Polychlorinated biphenyls have been demonstrated to influence fecundity, embryology, metabolism, immunocompetence, neurological development, endocrine function, and cell growth [1]. Use of the chlorinated insecticide 1,1,1-trichloro-2,2'-bis-p-chjorophenyl-ethane (DDT), which is metabolized to the more persistent DDE, was restricted in the United States by the U.S. Environmental Protection Agency (U.S. EPA) in 1972. The insecticide DDT is still manufactured and used in some countries, and it is transported through the atmosphere into distant ecosystems. Eggshell thinning is the most significant bioaccumulative effect of DDE in avian predators [4]. Accumulation of halogenated hydrocarbons has not been studied extensively in albatrosses of the North Pacific Ocean. Here we report the concentrations of PCBs and selected chlorinated insecticides, including the DDT complex, in albatrosses of the central North Pacific Ocean.

MATERIALS AND METHODS

Samples of blood and eggs were collected from known-aged adults and chicks of both black-footed albatrosses (Diomedea nigripes) and Laysan albatrosses (Diomedea immutabilis) on Sand Island, Midway Atoll, in the central North Pacific Ocean (28°11 'N, 177°22'W) during three time periods over the nesting season. The two fall sampling periods, November through December, 1992 and 1993, occurred during courtship, nest building, and egg laying. In the winter sampling period, January through February 1993, the parent albatrosses were incubating eggs or attending newly hatched chicks. Blood was collected from both chicks and adults during the spring sampling period, April through May 1993, during the chick rearing phase. Blood was drawn from the brachial vein of each bird and placed into vacutainers containing 0.015 ml ethylenediaminetetraacetic acid (EDTA) anticoagulant and stored at -20°C until analyses could be performed. Eggs were removed from the nests and contents of either individual eggs or composites were placed into numbered, chemically cleaned jars. Adipose tissue was dissected from euthanatized adult albatrosses that had been captured alive after being injured in accidents involving vehicles or guy wires.

Table 1. Age, total concentrations (ng/ml) of PCBs, DDE, and DDT, and DDE/DDT ratios in the plasma of adult Laysan and black-footed albatrossesa

		       Laysan albatross            Black-footed albatross     .
Variable 	N 	Mean	SD 	Range 	N 	Mean 	SD 	Range
Age (years) 	40 	11.3 	12.4 	1-38 	8 	21.6 	5.7 	13-27
DDE 		40 	16.0 	11.3 	3-46 	36 	35.1 	26 	0-98
DDT 		40 	4.8 	2.7 	1-10.2 	30 	8.6 	5.5 	3.2-32
DDE/DDT ratio	40 	6.1 	6.4 	0.6-23 	30 	5.2 	5.1 	0.7-19.7
PCBs 		39 	34.8 	15.1 	12-76 	36 	110 	103.2 	10-448

a PCBs = polychlorinated biphenyls; 
  DDE = 1,1-dichloro-2,2'-bis-chlorophenyl-ethylene; 
  DDT = 1,1,1-trichloro-2,2'-bis-p-chlorophenyl-ethane.

The methods for extracting and analyzing PCBs and chlorinated insecticides in the plasma have been described previously [5]. One milliliter of albatross plasma was denatured with methanol, extracted with hexane-diethyl ether, and purified by Florisil® (Sigma Chemical, St. Louis, MO, USA) and silica gel chromatography. The resulting fractions were then analyzed by gas chromatography and electron capture detection (GCECD). Analyte identities were confirmed by high-resolution gas chromatography/low-resolution mass spectrometry (HRGC/LRMS) by use of a Hewlett-Packard 5970 mass selective detector (Hewlett Packard, San Fernando, CA, USA) operated in the selected ion monitoring mode (SIM). Total concentrations of PCBs were determined by summing concentrations of individual congeners [6].

Statistical methods were performed by SAS (analysis of variance [ANOVA] or NPAR1WAY, regression, general linear models procedure, SAS/STAT 6.03; SAS Institute, Carey, NC, USA). In the five albatrosses sampled twice in different sample periods, mean values of each pair of residue concentrations were used in ANOVA calculations.

RESULTS AND DISCUSSION

Of the compounds monitored in blood plasma, only PCBs, DDT, and DDE were found to occur at concentrations that were significantly greater than the method detection limits (MDLs; Appendix). Although reportable concentrations of some of the other organochlorine compounds were found in some individuals, most of the concentrations were small, and we have little confidence in reporting these values. In most cases less than 10% of the measurements for a particular compound were greater than the MDL. Polychlorinated biphenyls were detected in all but 1 of the 76 plasma samples, with a range of 0.1 to 0.448 µg PCB/ml. 1,1-Dichloro-2,2'-bis-pchlorophenyl-ethylene was detected in all plasma samples, and DDT was detected in all but six plasma samples, with a range of 0 to 98 ng/ml and 1 to 32 ng/ml, respectively (Table 1). Concentrations of total PCBs and DDE were more than twice as great in plasma of black-footed albatrosses than they were in plasma of Laysan albatrosses (Table 1). This difference between species could be in part due to differences in diet and feeding strategy differences between the two species, which occupy different ecological niches. The Laysan albatross diet consists primarily of ommastrephid squid (68% of the diet); the remainder of the diet consists of approximately 9% fish, 9% crustaceans, and 4% coelenterates [7]. Black-footed albatrosses eat mostly flying fish (family Exocoetidae) and flying fish eggs (50%), whereas squid make up approximately 32% of the diet [8]. Additionally, black-footed albatrosses commonly scavenge human garbage, a habit Laysan albatrosses rarely adopt.

Concentrations of PCBs in plasma of Laysan albatross chicks were significantly less (p < 0.0001) than those in blackfooted albatross adults (ANOVA; p < 0.0001). Significant differences (p < 0.001) in concentrations of total PCB, DDT, and DDE in plasma between black-footed and Laysan albatrosses were observed (Table 1). Total concentrations of PCBs and DDE did not vary significantly with age of adults.

Significant differences in concentrations of total PCB, DDT, and DDE were observed among sampling periods (ANOVA; p < 0.0001). The DDE/DDT ratio was also significantly different among sampling periods. For black-footed albatross adults, total PCBs were greatest in the winter, but remained somewhat similar throughout the entire nesting season. For Laysan albatross adults, total concentrations of PCBs and DDE were greatest in the spring of 1993, whereas the fall 1992 sample period had less total PCBs than the other periods (Table 2). This may be due to mobilization of fat reserves at an increased rate due to extended periods of egg incubation without feeding and foraging over great distances to obtain food for the chicks [9].

Total concentrations of PCBs and DDE were measured in plasma from one Laysan albatross and four black-footed albatross adults that were each sampled twice, during two different nesting periods. Concentrations of PCBs, DDE, DDT, and the DDE/DDT ratio were comparable among sampling periods within individual birds. The exceptions are black-footed albatrosses 2 and 3, which showed greater PCB concentrations 1 year after they were first sampled (Table 3).

Concentrations of PHAHs in the adipose tissue were compared to those in both species of albatrosses that had been accidentally killed in December 1969 [10], even though protocols used at that time were different than those used in our study. In 1969, concentrations of PCBs and DDE in visceral fat of Laysan albatrosses were 22.3 mg/kg and 13.7 mg/kg, respectively; whereas visceral fat of black-footed albatrosses contained a mean concentration of 15.3 (7.5-21.3) mg/kg and 15.3 (5.1-22.7) mg/kg of PCBs and DDE, respectively. Concentrations of total PCBs in adipose tissue of Laysan albatrosses in 1969 ranged from 4.1 to 9.2 with a mean of 6.7 mg/kg, whereas the concentration of DDE ranged from 1.8 to 4.8 mg/kg wet weight [10]. The concentrations of total PCBs in the adipose tissue of Laysan albatrosses in the study on which we report here ranged from 2.1 to 2.8 mg/kg wet weight (ppm). Thus, concentrations of PCBs have decreased by a factor of two over the past 25 years. [10,11]. The birds sampled in the current study were killed in the early part of the breeding cycle when fat reserves were greatest. Therefore, sampling later in the season could have shown greater PCB concentrations in the blood due to metabolized fat reserves.

Table 2. Total concentrations (ng/ml) of PCBs, DDE, and DDT, and DDE/DDT ratios in plasma of albatrossesa

			 Black-footed albatross        Laysan albatross   .
Period 	Variable 	N 	Mean 	Range 	    N 	  Mean	  Range
Fall 1992 
	Total PCBs 	8 	109.8 	77-129 	    10 	  39.2 	  27.0-76.0
	DDE 		8 	48.0 	34.3-68.0   10 	  10.8 	  7.1-22.0
	DDT 		7 	12.1 	3.2-32.0    10 	  6.8 	  3.8-9.6
	DDE/DDT 	7 	5.9 	2.1-19.7    10 	  1.7 	  1.0-3.1
Winter 1993	
	Total PCBs 	7 	176.9 	73.0-369.0  5 	  43.8 	  12.0-70.0
	DDE 		7 	44.7 	0-77.0 	    5     28.2    12.0-46.0
	DDT 		3 	10.7 	4.5-14.1    5 	  2.04 	  1.6-2.5
	DDE/DDT 	3 	6.3 	3.6-9.6     5 	  13.6 	  7.5-23.0
Spring 1993 	
	Total PCBs 	2 	169.5 	137.0-202.0 2 	  55.0 	  53.0-57.0
	DDE 		2 	16.5 	8.0-25.0    2 	  37.5 	  36.0-39.0
	DDT 		— 	— 	— 	    2 	  4.2 	  4.1-4.3
	DDE/DDT 	— 	— 	— 	    2 	  9.0 	  8.8-9.1
Fall 1993
	Total PCBs 	7 	168.9 	47.0-448.0  9 	  31.3 	  15.0-59.0
	DDE 		7 	53.1 	18.0-98.0   9 	  22.3 	  9.0-42.0
	DDT 		7 	6.5 	3.3-16.6    9 	  1.6 	  1.0-2.5
	DDE/DDT 	7 	10.4 	1.1-16.9    9 	  13.6 	  9.0-18.0

a  PCBs = polychlorinated biphenyls; 
   DDE = 1, 1 -dichloro-2,2'-bis-chlorophenyl-ethylene; 
   DDT = 1,1,1trichloro-2,2'-bis-p-chlorophenyl-ethane.

Comparisons to Great Lakes fish-eating birds

Concentrations of polychlorinated diaromatic hydrocarbons (PCDH) have been much studied in birds of the North American Great Lakes region. A great deal of information exists on both concentrations of residues and toxic effects that have been observed in a range of species. Many of these effects have been attributed to specific toxicants, such as PCBs and DDTs. For this reason, concentrations of total PCBs and p,p'-DDE in plasma and eggs of albatrosses (Tables 3 and 4) were compared to concentrations in plasma and eggs of Great Lakes fish-eating birds (Figs. 1 to 4). Mean concentrations of total PCB in the plasma of Great Lakes-influenced bald eagle (Haliaeetus leucocephalus) chicks, defined as living within 8 km of Great Lakes shorelines [12], were slightly greater than the mean total PCB concentrations in plasma of adult black-footed albatrosses, but considerably greater than those in adult Laysan albatrosses. Bald eagle chicks from interior regions in the Great Lakes basin had similar mean total concentrations of PCBs in plasma as both black-footed and Laysan albatross chicks (Fig. 1). Mean DDE concentrations in plasma of adult black-footed and Laysan albatrosses were less than those in Great Lakes-influenced but greater than in interior bald eagle chicks [12]. Adult Caspian terns (Sterna caspia) [5] had mean concentrations of DDE in the plasma that were greater than DDE concentrations in both adult black-footed and Laysan albatrosses (Fig. 2). Mean concentrations of both PCBs and DDE in eggs of both species of albatrosses were similar to or less than those in eggs of piscivorous birds of the North American Great Lakes region. Concentrations of DDE in Laysan albatross eggs were six times less than concentrations in bald eagle eggs from interior regions of Michigan and 33 times less than those in eggs of eagles living along the shores of the Great Lakes (Fig. 3). Concentrations of DDE in black-footed albatross eggs were the same as those in eggs of bald eagles living in the interior of Michigan [13] and about one-half the concentration observed in Caspian terns and double-crested cormorants (Phalacrocorax auritus) from the North American Great Lakes [14] (Fig. 3). Mean total PCB concentrations in both black-footed and Laysan albatross eggs were less than PCB concentrations in eggs from Great Lakes-influenced bald eagles and bald eagles from the interior of Michigan [13], Caspian terns, and double-crested cormorants [14] (Fig. 4). The fact that concentrations of PCBs and p,p'-DDE in adult albatrosses from a remote area were similar to those in several fish-eating birds of the North American Great Lakes region indicates that contamination with these chemicals is global in nature.

Hazard assessments

Assessment of the hazard presented by current concentrations of total PCBs and DDE in albatrosses is difficult because no controlled studies of the effects of these compounds have been conducted in these or even closely related species. Furthermore, little information is available on concentrations of these compounds that occurred in the past. Not even crude estimates of these effects can be made from regression analyses. Therefore, the best estimate of possible effects can be made by comparing current concentrations of contaminants in eggs of albatrosses (Table 5) to dose-response relationships for other species of birds.

A hazard quotient (HQ) was determined to be the quotient of the average current concentrations of PCB, DDE, or 2,3,7,8tetrachlorodibenzo-p-dioxin equivalents (TEq) divided by the no observable adverse effect concentration (NOAEC) (Table 6). We used the NOAEC values suggested by Giesy et al. [15]. An HQ of 1.0 would indicate that the NOAEC had been achieved. The ratio between the NOAEC and lowest observable adverse effect concentration (LOAEC) is dependent on the slope of the dose-response function, and is generally between 5 and 10 [1]. Based on field studies of the relationship between concentrations of PCBs and adverse effects, significant population-level effects would be expected to occur at concentrations about 20 times greater than the NOAEC [1]. Assuming that both albatross species have similar sensitivities to these PHAHs, and that their sensitivities are similar to other wild fish-eating birds, the ratios indicate that concentrations of both PCBs and DDE in Laysan albatross are at the lower end of the range of possible effects, with current concentrations of neither total PCBs nor DDE expected to cause population-level adverse effects. The hazard ratio for current concentrations of PCBs in black-footed albatross eggs is close to 10. This indicates that current concentrations of PCBs are at the threshold of where population-level adverse effects would be expected to occur. The hazard quotients for DDE concentrations in both Laysan and black-footed albatrosses are much less than the threshold for adverse population-level effects (Table 6).

Table 3. Concentrations (ng/ml) of total PCBs, DDE, and DDT, and DDE/DDT ratios in plasma of five adult Laysan (LAAL) or black-footed (BFAL) albatrosses sampled twicea

		    BFAL 1  	    BFAL 2   	   BFAL 3    	   BFAL 4    	    LAAL 1   .
		Sam- 	Sam- 	Sam- 	Sam- 	Sam- 	Sam- 	Sam- 	Sam- 	Sam- 	Sam
		ple 1 	pie 2 	pie 1 	pie 2 	pie 1 	pie 2 	pie 1 	pie 2 	pie 1 	pie 2
Total PCBs 	99 	79 	103 	448 	101 	350 	73 	54 	37 	38
DDE 		63 	98 	68 	74 6	7 	18 	43 	34 	23 	24
DDT 		3.2 	5.8 	32.0 	5.4 	—	16.6 	4.5 	3.3 	1.9 	1.6
DDE/DDT ratio 	19.7 	16.9 	2.1 	13.7 	—	1.1 	9.6 	10.3 	12.1 	15.0

a  PCBs = polychlorinated biphenyls; 
   DDE = 1,1-dichloro-2,2'-bis-chlorophenyl-ethylene; 
   DDT = 1,1,1trichloro-2,2'-bis-p-chlorophenyl-ethane.

TEq

Because the greatest toxicity of PCBs, polychlorinated dibenzodioxins (PCDDs), polychlorinated dibenzofurans (PCDFs), and structurally similar dioxin-like congeners that bind to the aryl hydrocarbon receptor (Ah-r) act through the same receptor-mediated mechanism [1,16], concentrations of individual congeners can be corrected for their relative potency by the use of toxic equivalency factors (TEF), based on several toxic effects, including lethality, deformities, or enzyme induction [1,2,17-22]. Alternatively, an in vitro bioassay can be used to calculate the total 2,3,7,8-TCDD-like activity [1]. When the bioassay is used all of the interactions among individual congeners are corrected for and the resulting dioxin equivalents are referred to as TCDD-EQ. The TCDD-EQ were measured in and TEq calculated for eggs of both species of albatrosses (Table 6).

Table 4. Concentrations of DDE, total PCBs, and TEq in pooled samples of Laysan or black-footed albatross eggsa

				Laysan 	   Black-footed
				albatross  albatross
PCDD/PCDF TEq (ng/kg ww)b,c	22 	   37
PCB-TEq (ng/kg ww)b 		30 	   87
Total TEq (ng/kg ww)b 		52 	   124
Total PCBs (mg/kg ww) 		1.0	   3.8
DDE (mg/kg ww) 			0.3 	   1.8

a  DDE = 1,1-dichloro-2,2'-bis-chlorophenyl-ethylene; 
   PCBs = polychlorinated biphenyls; 
   TEq = 2,3,7,8-tetrachlorodibenzo-p-dioxin equivalents; 
   PCDD = polychlorinated dibenzodioxins; 
   PCDF = polychlorinated dibenzofurans; ww = wet weight.
b  Toxic equivalency factor (TEF) values from Ahlborg and Hanberg [29]. 
c  ww = wet weight.

No studies of the effects of TEq have been conducted on closely related species of "tube noses" (family Diomedeidae), the group to which albatrosses belong. The most relevant toxicologic information related to albatrosses is probably for birds in the order Pelicaniformes, to which double-crested cormorants belong. A few studies have been conducted that have correlated the concentrations of TEq in the diet or eggs of wild birds with observed effects or determined the toxicity of 2,3,7,8-TCDD or other compounds acting through the same mechanism of action, but with different potencies, to surrogate bird species (Fig. 5). Thus, it was necessary to derive an NOAEC from the effects of TCDD on surrogate species. We chose a value of 7 ng TEq/kg wet weight in egg as the threshold concentration (NOAEC) on which to base our calculation of HQ in the hazard assessment [15]. Although on the conservative side, the value selected for the NOAEC is near the median for the NOAEC values calculated from the literature information on the toxicity of TCDD to avian species [23,24]. The NOAEC used in our HQ is similar but not identical to those suggested by other workers. Our value is approximately 16-fold less than that derived by the U.S. EPA in their guidance document for wildlife hazard assessments of the effects of 2,3,7,8-TCDD on wildlife, but in the range of values predicted from other species [24]. An HQ of 7.4 was calculated for the Laysan albatross and 17.7 for black-footed albatross (Table 6). If we assume that the LOAEC is approximately 10 X greater than the NOAEC we would not expect TEq to be causing any adverse effects on Laysan albatross, but subtle effects of TEq on productivity of black-footed albatross should be observed.

Fig. 1. Mean total concentrations of polychlorinated biphenyls in plasma of Laysan and black-footed albatross adults and chicks compared to bald eagle chicks from the interior and Great Lakes-influenced areas of the Great Lakes region. Data from Bowerman et al. [12].

Fig. 2. Mean concentrations of 1, 1 -dichloro-2,2'-bis-p-chlorophenylethylene in the plasma of Laysan and black-footed albatross adults compared to adult Caspian terns and bald eagle chicks in the interior and Great Lakes-influenced areas of the Great Lakes region. Data from Mora et al. [5] and Bowerman et al. [12].

Based on these hazard assessments, the black-footed albatross would be expected to be experiencing subtle population-level effects on productivity, whereas no such effects would be predicted in the Laysan albatross population. To determine the validity of the predictions based on HQ, we sought to compare the predicted effects to observed effects, both current and historical. Historical productivity data are scarce, but indicate that the egg crushing rates and hatching rates from 1962 to 1964 in black-footed albatrosses [25] are comparable to those in both Laysan albatross and black-footed albatross from 1993 and 1994 (Table 7). However, the recent rate of cracked eggs in black-footed albatrosses is greater than 5%, twice the rate of cracked eggs found recently in Laysan albatrosses (Table 7) [26]. Both the HQ and observations of egg quality and hatching rate indicate that DDE is unlikely to be the cause of eggshell cracking. In fact, no decreases in eggshell weight or increase in egg breakage were reported between 1910 and 1969 in either albatross species, when DDE concentrations were greater than those found currently [10]. The HQs calculated for PCBs in both the Laysan albatross and the black-footed albatross were greater than 1.0. The value for Laysan albatrosses was near enough to the NOAEC that little or no population-level adverse effects would be expected. The HQ for black-footed albatrosses was approximately 10, which, based on observations in populations of fish-eating birds of the North American Great Lakes, would be expected to be causing subtle population-level effects, such as embryo lethality [1,2] and deformities [14,27,28]. The rates of hatching were similar between black-footed albatrosses and Laysan albatrosses, but the (difference a lesser rate in black-footed albatrosses than in Laysan albatrosses) was statistically significant (Table 7). The differences in rates of deformities between the two species, although statistically significant, was more equivocal. The hazard assessment is necessarily crude, because there is no toxicologic information available from field or laboratory studies involving albatrosses. The uncertainties could be either positive or negative and it is impossible to know what the final result of such potentially offsetting uncertainties would be. However, if we assume that Laysan albatrosses and black-footed albatrosses have similar sensitivities to PCBs and TEq and that these species are represented by a median value measured for other species, either in laboratory studies or from ecoepidemiologic studies, we would conclude that current exposures to both PCBs and TEq would be near the threshold for population-level adverse effects. The TEq seem to be the more critical of the two toxicants because the HQ of TEq was greater than that of PCBs. Based on this crude initial analysis, we conclude that there is little or no assimilative capacity for additional TEq in the global environment. That is, if additional TEq were deposited into albatross eggs it would be expected to cause population-level adverse effects. A number of compounds are known to be able to act through the same Ah-mediated mechanism of action as 2,3,7,8-TCDD [1]. This being the case, it is suggested that more information be gathered on the global distribution of compounds that can contribute to TEq and on the relative sensitivities of animals that might be at risk. Finally, we believe that this research has demonstrated that populations of animals in relatively remote areas are contaminated to a sufficient degree to warrant consideration of global controls on the distribution of persistent, bioaccumulative toxic compounds.

Fig. 3. Mean total concentrations of polychlorinated biphenyls in the eggs of Laysan and black-footed albatrosses compared to bald eagle eggs from Great Lakes-influenced and interior areas of the Great Lakes region and to Caspian terns and double-crested cormorants of the Great Lakes. Data from Bowerman [13] and Yamashita et al. [14].

Fig. 4. Mean concentrations of l,1-dichloro-2,2'-bis-p-chlorophenylethyl. in the eggs of Laysan and black-footed albatrosses compared to bald eagle eggs from Great Lakes-influenced and interior areas and to Caspian terns and double-crested cormorants of the Great Lakes region. Data from Bowerman [12], Mora et al. [5], and Yamashita et al. [14].

Table 5. Concentrations (ng/g wet weight) of individual compounds in the DDT complex, measured on individual black-footed or Laysan albatross eggs (N = 20)

		Black-footed albatross Laysan albatross
Compounds 	Mean	SD	Mean	SD
p,p'-DDT 	35.5 	17.5 	11.5 	0.5
p,p'-DDE 	1,550 	250 	121 	69
o,p'-DDE 	0.5 	0.2 	0.5 	0.2
p,p'-DDD 	3.3 	0.5 	1.1 	0.3
o,p'-DDD 	1.7 	0.2 	1.1 	0.1
Lipid content 	10.61 	3.42 	21.6 	9.1

a DDT = 1,1,1,-tichloro-2,2'-bis-p-chlorophenyl-ethane; 
  DDE = 1,1dichloro-2,2'-bis-p-chlorophenyl-ethylene; 
  DDD = 1,1-di-(p-chlorophenyl)-2,2-dichloroethane.

Table 6. Hazard quotients (HQs)a for Laysan albatrosses (LAAL) and black-footed albatrosses (BFAL) based on concentrations in eggs collected in 1993 and composite NOAECsb

	PCBs 	DDE 	TEqc
LAAL 	2.6d 	0.09 	7.4
BFAL 	9.7d 	0.51 	17.7 

a  HQ = egg concentration of PCB/NOAEC or DDE/NOAEC.
b  NOAEC = no observable adverse effect concentration; 
   PCBs = polychlorinated biphenyls; 
   DDE = 1,1-dichloro-2,2'-bis-p-chlorophenyl-ethylene; 
   TEq = 2,3,7,8-tetrachlorodibenzo-p-dioxin equivalents.
c  From Jones et al. [22].
d  Based on proportions of Aroclors, not corrected for weathering.

Table 7. Mean egg crushing, egg cracking, and hatching rates for  Laysan albatrosses (LAAL) and black-footed albatrosses (BFAL) on Midway Atoll

		% Eggs 	% Eggs 	% Eggs
Species/period	crushed	cracked	hatched
BFAL/1993-1994 	2.62 	5.34 	71.53
LAAL/1993-1994 	2.21 	2.84 	74.45
LAAL/1962-1964a 1-3 	 ——	71-73

a  1962-1964 data from Fischer [9].

Fig. 5. Concentrations of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) or TCDD-equivalents (TEq) found to cause toxicologic effects in avian species. The solid lines labelled BFAL and LAAL give the concentrations of TEq measured in the eggs of black-footed and Laysan albatrosses, respectively. Sources of information are given in brackets.

a 1962-1964 data from Fisher [9].

Acknowledgement-This research was made possible by a grant from the U.S. Environmental Protection Agency through the World Wildlife Fund (CR 820227-01-0). Many thanks are given to C.P.O. Greg Diefenderfer for his extensive volunteer work on Midway, Jill DeDoes for performing extractions, and the U.S. Navy and U.S. Fish and Wildlife Service for allowing our research on Midway Atoll.

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APPENDIX

Organochlorine insecticides measured in the blood plasma of albatrosses, along with the method detection limits

		 Method detection
Compounda  	  limits (ng/ml)
Endosulfan I 		0.8
Dieldrin 		0.8
Endrin 			1.1
Endosulfan II 		1.2
Methoxychlor 		2.9
Hexachlorobenzene 	0.3
Heptachlor 		0.6
Aldrin 			0.5
p,p'-DDE 		0.6
Oxychlordane 		0.6
Gamma-chlordane 	0.7
o,p'-DDE 		1.1
Alpha-chlordane 	0.7
Trans-nonachlor 	0.7
o,p'-DDD 		1.7
p,p'-DDD 		1.5
p,p'-DDT 		1.1
Lindane 		0.6
Heptachlor epoxide	0.7

a DDE = 1, 1 -dichloro-2,2'-bis-chlorophenyl-ethylene; 
  DDD = 1,1di-(p-chlorophenyl)-2,2-dichloroethane; 
  DDT = 1,1,1-trichloro2,2'-bis-p-chlorophenyl-ethane.

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