Metals in Albatross Feathers from Midway Atoll: Influence of Species, Age, and Nest Location

Environmental Research Section A 82, 207}221 (2000) doi:10.1006/enrs.1999.4015, available online at http://www.idealibrary.com on

Metals in Albatross Feathers from Midway Atoll: Influence of Species, Age, and Nest Location Joanna Burger*,-,1 and Michael Gochfeld-,? *Division of Life Sciences, Graduate Program in Ecology and Evolution, Rutgers University, Piscataway, New Jersey 08854-8082; -Environmental and Occupational Health Sciences Institute, Piscataway, New Jersey 08854; and ?Environmental and Community Medicine, UMDNJ-Robert Wood Johnson Medical School, Piscataway, New Jersey 08854 Received November 11, 1998

We also collected down and feathers from Laysan albatross chicks whose nests were close to buildings, including buildings with Baking lead paint and those that had been lead-abated. Lead levels in the down and feathers of chicks close to nonabated buildings were 10 times higher than for chicks from other locations. Conversely, levels of cadmium and tin were lower near the buildings. Near lead-abated buildings, lead levels decreased as a function of distance, indicating residual contamination on the soil. Our results indicate that black-footed albatross adults and chicks generally have higher levels of heavy metals in their feathers than Laysans. Chicks of both species have higher levels in their down than in their contour feathers, indicating potentially higher exposure during the early chick phase.

Female birds sequester some heavy metals in their eggs, which are then transferred to the developing embryo. Semiprecocial birds such as albatrosses are fully covered with down at hatching, but are dependent on their parents for food for many weeks. At hatching, levels of metals in the chick’s down represent exposure from the female via egg, while levels in fully formed feathers at Bedgling, several months later, represent mainly exposure from food provided by their parents. In this paper we examine the concentrations of ‘‘metals’’ (heavy metals, mercury, lead, cadmium, chromium, manganese, tin; and metalloids, arsenic and selenium), in the down and contour (body) feathers of half-grown young albatrosses, and contour feathers of one of their parents. We collected feathers from Laysan Diomedea immutabilis and black-footed Diomedea nigripes albatrosses from Midway Atoll in the central PaciAc Ocean. We test the null hypotheses that there is no difference in metal levels as a function of species, age, feather type, and location on the island. Using linear regression we found signiAcant models accounting for the variation in the concentrations of mercury, lead, cadmium, selenium, chromium, and manganese (but not arsenic or tin) as a function of feather type (all metals), collection location (all metals but lead), species (selenium only), and interactions between these factors. Most metals (except mercury, arsenic, and tin) were signiAcantly higher in down than in the contour feathers of either chicks or adults. Comparing the two species, black-footed albatross chicks had higher levels of most elements (except arsenic) in their feathers and/or down. Black-footed adults had signiAcantly higher levels of mercury and selenium.

( 2000 Academic Press

Key Words: Diomedea immutabilis; Diomedea nigripes; albatrosses; age differences; cadmium; chromium; lead; manganese; mercury; selenium; bioindicator.

INTRODUCTION

Contaminants can bioaccumulate over time to reach sublethal, or even lethal, levels in organisms unless they are excreted or detoxi7ed. This problem is particularly severe for heavy metals in long-lived organisms that are at the top of their food chains (van Straalen and Ernst, 1991; Burger et al., 1992; Sundlof et al., 1994). Some seabirds accumulate contaminants such as mercury, cadmium, and selenium, achieving tissue concentrations shown in laboratory or 7eld studies to cause adverse effects (organ toxicity, reproductive or neurobehavioral impairment) (Eisler, 1987; Ohlendorf et al., 1989; Nisbet, 1993; Burger, 1993). Although rarely are there clear cases of neurodevelopmental and lethal effects

1To whom correspondence should be addressed at Division of Life Sciences, Rutgers University, Nelson Hall, 604 Allison Road, Piscataway, NJ 08854-8082. Fax: (732) 445-5870. E-mail: [email protected]. 207

0013-9351/00 $35.00 Copyright ( 2000 by Academic Press All rights of reproduction in any form reserved.

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of metals on wild bird populations, such a case was reported for albatrosses on Midway Atoll by Sileo and Fefer (1983) who found that some Laysan albatross Diomedea immutabilis chicks on Midway Atoll suffered lead poisoning from eating paint chips that were 8aking off buildings. They observed chicks eating paint chips, and paint chips were found in the stomachs of these chicks. Sileo and Fefer (1987) reported that ingestion of weathered paint chips with up to 144,000 ppm lead was the cause of the lead poisoning. The lead-poisoned chicks exhibited symptoms of drooping wings and nerve degeneration, and lead poisoning was one of the causes of mortality (Sileo and Fefer, 1983; Work and Smith, 1996). However, other heavy metals were not examined in these albatrosses, nor have the albatrosses been examined for age-related differences, nor for exposure differences that can be detected in the down and fully formed feathers of the young. Pollutant data for oceanic birds are generally lacking (Walker, 1990), and this study partially addresses this lack. Jones et at. (1996) examined persistent chlorinated hydrocarbons in albatrosses from Midway. They found that levels of polychlorinated biphenyls ranged from 177 ng/g wet weight in eggs to 2750 ng/g wet weight in adult fat. Total TCDD toxic equivalents (TEQs) ranged from 17.2 to 297 pg/g wet weight, and these concentrations were near or above the levels known to cause adverse effects in other 7sh-eating birds (Jones et al., 1996). Recently, Auman et al. (in press) reported that levels of total PCBs and organochlorine insecticides were higher in the plasma of chicks and adults, and in the eggs, of black-footed albatrosses compared to Laysan albatrosses. Given that potential adverse effects in the albatrosses in Midway could be caused by high levels of lead or chlorinated hydrocarbons, it seemed prudent to examine the levels of other toxic metals. In this paper we examine the levels of heavy metals and the metalloids, arsenic and selenium (hereinafter referred to as metals), in the feathers of blackfooted (Diomedea nigripes) and Laysan albatrosses and their chicks nesting on Sand Island of Midway Atoll. We collected feather samples in May 1997, when the half-grown chicks were partially molting into their juvenile plumage. This allowed us to collect both mature down and contour feathers from the same chicks, giving an indication of heavy metal exposure from the egg (down) and from food provided by their parents (down, feathers). Laysan albatrosses nest throughout Sand Island, close to and far from buildings, allowing us to compare metal

levels in birds nesting close to buildings as well as in more remote locations. Black-footed albatrosses nest only in the more remote parts of the island, away from the buildings. We also collected feathers from some chicks in nests near buildings, both those that had been lead-abated and those that still had 8aking lead paint. Some of the latter chicks showed signs of lead poisoning (drooping wings, after Sileo and Fefer, 1983) and had lead paint chips in their stomachs. We test the null hypotheses that there are no differences in metal levels as a function of (1) species, (2) age or feather type, or (3) location. The chicks of both species of albatrosses are sedentary, remaining on or near their nest for many months. The adults regurgitate primarily squid (Ommastrephidae) and 8ying 7sh eggs (Exocoetidae) to the chicks approximately once a day (Harrison et al., 1983). This regurgitation involves a mutual display lasting several minutes prior to feeding, allowing us to identify the parents of particular chicks, and to both capture and collect feathers at the same time. MATERIALS AND METHODS

Under appropriate federal and wildlife refuge permits we collected feathers from albatrosses on Midway Atoll in the central Paci7c. Midway Atoll (28315@N, 177320@W) is 1850 km northwest of Honolulu. It was developed as a communication station in the early 20th century, and was a major United States Navy base during and after the Second World War when it experienced heavy bombardment as well as numerous aircraft, aerial cables, and the introduction of rats, which resulted in the decline of many species of seabirds (Fisher, 1966; Whittow, 1993a,b). Until recently, Midway Island has been off limits except to the military, and access to many parts of the island was restricted even to military personnel. In July of 1997, Midway Island was taken over by the U.S. Fish & Wildlife Service, which in conjunction with Oceanic Society Expeditions will partially manage the islands for ecotourism. Midway Atoll is now a National Wildlife Refuge, and refuge personnel can control access to different parts of the island. There are still hundreds of buildings, many roads, and paved runways and taxiways on the island. Some of the buildings are in disrepair, and others were renovated and have undergone lead abatement. Midway Atoll comprises three islands, only Sand Island of which is occupied by humans. The atoll’s fringing reef is nearly circular and is 10.5 km in

METALS IN ALBATROSS FEATHERS

diameter. Sand Island (453 ha) is heavily vegetated with exotic plants (Casuarina spp., Verbesina encelioides, Bidens alba, and Pluchea spp.), as well as native species (Naupaka, Scaevola taccada, and Beach Heliotrope, Tournefortia sp.). Over a million seabirds of 15 species nest on Midway Islands, and the Laysan (400,000 pairs) and black-footed (7000) albatrosses are the most abundant species (Whittow, 1993b; U.S. Fish & Wildlife Service, 1996). The Laysan colony is the largest in the world (Sileo and Fefer, 1987), and they nest throughout Sand Island in nearly all habitats except on solid concrete. Albatross chicks are semiprecocial; they are fully covered with down at hatching and can thermoregulate (Gill, 1990), but they remain at their nest site and depend entirely on their parents for food for over 5 months (Rice and Kenyon, 1962). The adults return to the nest with their crops full of semidigested food, mainly squid and the eggs of 8ying 7sh. There is an elaborate behavioral interaction lasting several minutes, which precedes the feeding. Since chicks handled after a feeding often regurgitate, we identi7ed subjects as soon as we observed a prefeeding interaction and captured the adult before the feeding occurred. Using this method it was possible to pull feathers without having the chick regurgitate any food. Adult birds were captured by hand or by net, and young were captured by hand just before they were fed. We chose chicks that had both down feathers and fully formed breast feathers. Following release the parent usually walked a few meters away or circled brie8y, while we handled the chick. Feeding then occurred within 5}10 min of our release of the chick. We collected down and contour feather samples by plucking two large pinches of about 20 feathers from the sides of the breast. One of our variables was ‘‘location’’ on the island. We sampled Laysan albatrosses from three locations: near the end of the runway (‘‘remote’’), near buildings which had undergone lead-paint removal (‘‘abated’’), and near buildings that had not undergone lead-paint removal (‘‘nonabated’’; chicks only). The latter group was small, making it dif7cult to collect feathers from their parents. Further, these chicks all exhibited signs of lead poisoning (drooped wings, Sileo and Fefer, 1983). Feather samples were collected from black-footed albatross only from the end of the runway (remote) because they do not normally nest close to the buildings. Feathers were placed in envelopes for later analysis in the Elemental Analysis Laboratory of the Environmental and Occupational Health Sciences Institute (EOHSI). We analyzed lead, cadmium, selenium, chromium, manganese, arsenic, tin, and

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mercury. Lead was analyzed because of the previously reported lead poisoning of chicks whose nests were near buildings (Sileo and Fefer, 1983). Mercury and cadmium were analyzed because they often concentrate in the marine prey consumed by albatrosses and are of general concern because of bioaccumulation up the food chain (Eisler, 1987). We examined selenium because it is known to ameliorate the toxic effects of mercury and can itself be quite toxic to birds (Eisler, 1985; Ohlendorf et al., 1989). Manganese was examined because it is being considered as an additive to gasoline to replace lead (Cooper, 1984), and it is prudent to obtain baseline levels before such a global change occurs. We study tin because of the widespread use of highly toxic organic tin compounds in antifouling paints, which are still used by the military. Arsenic was examined because this highly toxic element is often found to bioacummulate in marine food chains. We analyzed chromium because it has neurotoxic effects in birds, yet little is known about chromium in marine environments (Burger and Gochfeld, 1995a). Further, this is the suite of elements we have been analyzing for a variety of marine birds worldwide, largely because of their known presence in marine systems and their adverse biological effects (Fowler, 1990), and only expense precluded the analysis of other elements. At EOHSI feathers and down were washed vigorously in deionized water alternated with acetone to remove loosely adherent external contamination (Applequist et al., 1984; Walsh, 1990; Burger, 1993). After washing, feathers were air dried overnight. The sample was weighed to 0.1 mg. Feathers were then digested in 70% analytic-grade nitric acid in a microwave vessel for 10 min under 130 psi (9.16 kg/cm2), and samples were subsequently diluted in deionized water. Mercury was analyzed by cold vapor technique, and all other metals were analyzed by Perkin-Elmer 5100 graphite furnace atomic absorption, with Zeeman correction. All concentrations in feathers are expressed in parts per billion (ng/g on dry weights). Instrument detection limits were 0.02 ppb for cadmium, 0.08 ppb for chromium, 0.15 ppb for lead, 0.09 ppb for manganese, 0.2 ppb for mercury, and 0.7 ppb for selenium, but matrix detection limits were about an order of magnitude higher. All specimens were run in batches that included a standard calibration curve and spiked specimens. The accepted recoveries ranged from 87 to 105% and no batches with recoveries outside these limits were encountered in this study. The coef7cient of variation (CV) on replicate samples ranged from 3 to 6%.

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Further quality control included periodic blind analysis of an aliquot from a large sample of known concentration and blind runs of duplicate samples during the analysis for each metal. Metal concentrations often approximate a lognormal distribution. Both arithmetic and geometric means are given to facilitate comparisons with other studies in the literature. Data were analyzed by multiple regression on log-transformed values to determine the factors that entered the models (PROC GLM in SAS), followed by nonparametric KruskalWallis one-way analyses of variance to compare concentrations between species and between age classes (PROC NPAR1WAY with Wilcoxon option, SAS, 1985). We constructed two types of models for the metals we examined: (1) those that included feather samples from both species, except for the Laysan chicks near buildings with lead paint; and (2) those that contained all the Laysan samples. Feather type refers to down, chick contour, or adult contour, feathers. We accept P(0.05 as signi7cant, but in some places also provide values for signi7cance between 0.10 and 0.05 because it provides the reader with more information about factors that might have been signi7cant with higher sample sizes. RESULTS

The metal levels in down and feathers of Midway albatrosses are given in Table 1. Black-footeds were studied only on the air7eld. The Laysan data exclude abnormal chicks near buildings (see below). We analyzed data with multiple linear regression for both species together (Table 2) and then for Laysan Albatrosses alone (Tables 3 and 4). Species Differences We compared the levels in each feather type by species (Table 1). There were signi7cant differences as a function of feather type for most metals in both species. Tin and arsenic did not differ, and cadmium differed only for Laysan (down vs chick contour; Table 1). Mercury levels in feathers of adults were signi7cantly higher than for chicks, and levels in black-footed albatrosses were signi7cantly higher than for Laysans for all plumages. For both species, lead and manganese levels were signi7cantly and cadmium somewhat higher in the down of chicks compared to the feathers of either chicks or adults. The pattern for selenium differed between the species (Table 1). In Laysans, the levels in the feathers of chicks were lower than either their down or the feathers of their parents, while in black-

footeds the levels of selenium in adult feathers were signi7cantly lower than those of their chick’s down. The pattern for chromium differed the most between the two species (Table 1). In black-footed albatrosses, the levels of chromium were signi7cantly higher in the plumage of chicks (both down and feathers) compared to adults, while in Laysans, the levels of chromium were signi7cantly lower in the plumage of chicks. Species differences were not apparent for lead, arsenic, or tin. The best regression models accounting for variations in metal levels are presented in Table 2 for Laysan and black-footed albatrosses (excluding the Laysans nesting close to buildings with lead paint). For mercury, the best model explained 81% (r2"0.81) of the variation in terms of species and feather type. For lead, the best model explained only 16% of the variation, and feather type was the only signi7cant factor accounting for the variation. For cadmium, 50% of the variation was explained by feather type, location, and an interaction between species and feather type. For selenium and chromium, 28 and 29% of the variation was explained by feather type, location, and interactions of these factors; for manganese, only feather type and location were signi7cant in explaining 27% of the variation (Table 2). Overall, feather type, followed by nesting location seemed to explain much of the variation in metal levels. Locational Differences in Laysan Albatross The models presented above (Table 2) excluded the lead-exposed, abnormal chicks nesting near the buildings where lead paint had not been removed. When all the Laysans (including these chicks) are examined together, signi7cantly more of the variation in metal concentrations is explained by the models (Table 3). There were signi7cant models for all metals except arsenic, which approached signi7cance. For most metals between 21 and 63% of the variation (based on r-squared values) was explained by location and feather type (and interactions of the two, Table 3). For tin, however, only location contributed signi7cantly to explaining variation (Table 3). For mercury, feather type accounted for most of the variation in levels (Table 3). However, for all other metals, the most signi7cant contributor was location (Table 3), thus we examined the concentrations by location (Table 4). The most striking differences as a function of location occurred for lead (Table 4). Mean lead levels were 10 times higher in both the down and the feathers of chicks collected

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TABLE 1 Concentrations of Metals in Feathers and Down of Black-Footed and Laysan Albatrosses on Midway Atoll Chick Down

Feathers

Black-footed albatross;on air7eld (N"17) Lead 1,750$195 1,110$229 (1,580) (757) Cadmium 2,470$456 1,580$333 (1,880) (513) Selenium 3,260$164 2,330$122 (3,190) (2,280) Chromium 11,900$3,290 11,600$4,830 (6,540) (4,210) Manganese 3,230$450 2,030$293 (2,890) (1,800) Arsenic 87.0$29.7 101$39.7 (6.13) (2.30) Tin 5,250$1,080 4,700$892 (2,040) (2,250) Mercury 6,700$562 5,570$361 (6,370) (5,380) Laysan Albatross;normal (N"35) Lead 2,410$370 (1,530) Cadmium 773$218 (393) Selenium 2,570$222 (2,330) Chromium 2,890$366 (2,290) Manganese 3,270$393 (2,750) Arsenic 155$39.8 (4.87) Tin 3,680$708 (1,040) Mercury 2,100$74.3 (2,050)

734$99.5 (424) 496$196 (116) 1,700$187 (1,370) 1,940$275 (1,400) 1,630$215 (1,130) 182$41.4 (9.89) 3,420$642 (1,290) 2,150$119 (2,050)

Down vs feather Kruskal-Wallis s2 (P)

6.00 (0.01) 2.08 (NS) 12.46 (0.0004) 1.02 (NS) 8.94 (0.003) 0.11 (NS) 0.02 (NS) 1.87 (NS)

Adult Feathers

973$125 (808) 152$25.8 (133) 3,260$320 (2,960) 1,420$160 (1,300) 1,780$195 (1,570) 208$48.5 (25.0) 3,640$886 (509) 19,600$1,750 (17,700)

18.46 (0.0001) 12.58 (0.0004) 12.54 (0.0004) 5.66 (0.02) 17.34 (0.0001) 0.46 (NS) 0.00 (NS) 0.16 (NS)

799$5.8 (707) 364$103 (157) 2,290$294 (1,930) 6,570$2,280 (1,930) 1,720$255 (1,080) 110$25.0 (10.4) 5,400$933 (2,380) 3,460$388 (3,060)

Adult vs young Kruskal-Wallis s2 (P)

0.15 (NS) 2.14 (NS) 4.49 (0.034) 3.15 (0.08) 0.00 (NS) 3.71 (0.054) 1.54 (NS) 17.52 (0.0001)

1.01 (NS) 0.37 (NS) 4.01 (0.045) 0.13 (NS) 0.00 (NS) 0.24 (NS) 1.49 (NS) 12.92 (0.0003)

Comparison between species (s2, P)

Lead Cadmium Selenium Chromium Manganese Arsenic Tin Mercury

Chick down

Chick feathers

0.45 (NS) 18.2 (0.0001) 10.4 (0.001) 9.93 (0.002) 0.06 (NS) 0.06 (NS) 2.11 (NS) 696 (0.0001)

1.73 (NS) 5.08 (0.02) 8.85 (0.003) 5.99 (0.01) 4.08 (0.04) 1.54 (NS) 4.24 (0.04) 31.9 (0.0001)

Adult feathers

0.60 0.42 7.63 0.13 0.54 2.30 1.00 2.73

(NS) (NS) (0.006) (NS) (NS) (NS) (NS) (0.0001)

Note. Given are means$SE (geometric means are given below in parentheses).Comparisons are made with Kruskal-Wallis one-way ANOVA, yielding a s2 statistic. All values are in ng/g (ppb dry weight.); NS, not signi7cant.

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TABLE 2 Multiple Linear Regression Explaining Variation in Metal Levels in Two Species of Albatrosses from PROC GLM Analysis (Droop-Winged Birds Not Included)

Model F df r2 P Variable entering (F, P) Species Feather type Species * Feather type

Lead

Cadmium

Selenium

Chromium

Manganese

Arsenic

Tin

Mercury

3.46 8151 0.16 0.001

18.27 8152 0.50 0.0001

7.12 8152 0.28 0.0001

7.20 8152 0.29 0.0001

6.73 8152 0.27 0.0001

1.74 8152 0.09 0.09

0.74 8151 0.04 NS

72.86 8148 0.81 0.0001

NSa

NS

NS

NS

NS

NS

9.52 (0.0001) NS

26.60 (0.0001) 4.89 (0.009) 44.01 (0.0001) 4.99 (0.008)

8.98 (0.003) 11.22 (0.0001) NS

9.83 (0.0001) 8.87 (0.0002) 15.87 (0.0001) NS

14.07 (0.0001) NS

NS

NS

NS

11.22 (0.001) NS

4.32 (0.04) 2.50 (0.09)

2.81 (0.06) NS

312.43 (0.0001) 63.73 (0.0001) 17.35 (0.0001) NS

NS

NS

Location

NS

Feather type * Location

NS

4.08 (0.045) 2.51 (0.08)

a NS, not signi7cant.

near buildings where lead paint had not been removed than those in all other chicks. Cadmium levels, however, were higher in the down and feathers of chicks from the remote location compared to levels in chicks collected near buildings. Tin levels were lower in the down and feathers of chicks from near non-lead-abated buildings compared to all other chicks. The pattern for selenium was less clear (Table 4). Most of the differences in feather type occurred in the birds collected near buildings (both with and without lead abatement). For all metals where there were signi7cant plumage differences, levels were

signi7cantly higher in the down of chicks compared to the feathers of chicks or adults (Table 4). One notable exception is lead; there was no signi7cant difference between the lead levels in the down and feathers of chicks collected near buildings with no lead abatement. For lead, where the locational differences in levels were most dramatic, there was no overlap in lead levels of birds from the non-lead-abatement area with those from the other two sites. The levels of lead in the down of chicks collected near lead-abated buildings, however, were also higher than those collected from the remote site at the end of the air7eld

TABLE 3 Multiple Linear Regression Explaining Variation of Metal Levels in All Laysan Albatrosses from PROC GLM Analysis (Droop-Winged Birds Included)

Model F df r2 P Variables entering (F, P) Feather type Location Feather type * Location aNS, not signi7cant.

Lead

Cadmium

Selenium

Chromium

Manganese

Arsenic

Tin

Mercury

29.41 7130 0.63 0.0001

17.22 7131 0.49 0.0001

5.23 7131 0.23 0.0001

4.82 7131 0.21 0.0001

11.93 7131 0.40 0.0001

1.65 7131 0.09 0.09

3.43 7131 0.16 0.002

7.88 7128 0.31 0.0001

5.59 (0.005) 81.93 (0.0001) 2.26 (0.09)

20.96 (0.0001) 29.86 (0.0001) 4.56 (0.005)

8.20 (0.0005) 5.53 (0.005) NS

4.81 (0.01) 10.69 (0.0001) NS

18.08 (0.0001) 15.51 (0.0001) NS

NS

NS

2.42 (0.09) 2.19 (0.09)

8.17 (0.0005) NS

13.0 (0.0001) 2.64 (0.08) 2.93 (0.04)

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TABLE 4 Concentrations of Metals in Laysan Albatrosses on Midway Atoll (All Values in ng/g [ppb Dry Weight]) Chick Feathers

Adult feathers

Wilcoxon s2 (P)

1170$549 (601) A 1020$395 (455) A 2040$255 (1810) A 2630$459 (2060) B 1910$240 (1700) B 71.8$40.9 (1.41) A 2640$530 (1140) B 2150$138 (2090) A

813$130 (693) A 672$211 (281) A 2120$206 (1970) A 13100$4740 (3830) A 1810$208 (1660) B 59.3$19.2 (4.92) A 6240$1450 (3920) A 2710$315 (2530) A

4.27 (NS)

Laysan albatross;near buildings with lead abatement (N"19) Lead 3090$585.7 817$158 (2100) A (373) B Cadmium 455$185 52.7$10.0 (252) A (36.8) B Selenium 2620$389 1410$258 (2270) A (1080) B Chromium 2160$302 1350$272 (1860) A (1010) A Manganese 3330$646 1390$337 (2630) A (798) B Arsenic 158$49.8 276$61.1 (4.16) A (51.0) A Tin 4330$1200 4070$1090 (1530) A (1430) A Mercury 1980$99.4 2150$190 (1941) B (2019) B

788$91.5 (718) B 124$22.4 (99.6) B 2420$503 (1900) A,B 1530$279 (1130) A 1640$430 (772) B 150$40.0 (18.5) A 4750$1230 (1620) A 3990$600 (3490) A

Down Laysan albatross;on ‘‘remote’’ air7eld (N"16) Lead 1590$331 (1050) A Cadmium 1150$412 (667) A Selenium 2510$168 (2400) A Chromium 3770$663 (2930) B Manganese 3200$414 (2900) A Arsenic 152$65.8 (5.88) A Tin 2900$584 (661) B Mercury 2240$105 (2200) A

Laysan albatross;near buildings without lead abatement (droop-winged N"15);chicks only Lead 40200$6070 31900$6630 ; (32600) A (21300) A Cadmium 740$230 189$51.5 ; (520.6) A (135) B Selenium 1630$176 1100$145 ; (1490) A (1000) B Chromium 2750$425 1600$383 ; (2350) A (1340) A Manganese 9720$2110 2210$349 ; (7530) A (1950) B Arsenic 270$107 183$49.2 ; (24.5) A (18.4) A Tin 1270$412 1230$663 ; (55.3) A (40.9) A Mercury 2010$171.0 1810$132 ; (1900) A (1750) A

3.55 (NS) 4.92 (0.09) 1.24 (NS) 10.0 (0.007) 1.37 (NS) 4.42 (NS) 2.37 (NS)

20.3 (0.0001) 28.9 (0.0001) 15.0 (0.0006) 5.73 (0.06) 11.9 (0.003) 3.47 (NS) 0.14 (NS) 16.83 (0.0002)

61 (NS) 12.3 (0.0004) 4.30 (0.04) 6.19 (0.01) 16.8 (0.0001) 0.02 (NS) 0.20 (NS) 0.77 (NS)

Note. Given are means$SE (geometric means are given below in parentheses.) Letters are based on Duncan Multiple Range test using multiple regression on log-transformed values; different letters indicate signi7cant differences; NS, not signi7cant.

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TABLE 5 Concentrations of Metals in Feathers and Down of Laysan Albatross Chicks on Midway Atoll

Down Lead Cadmium Selenium Chromium Manganese FIG. 1. Lead levels as a function of distance from buildings where lead paint had been abated. There were very few chicks close to buildings. Most of the Laysan chicks were sampled near the end of the runway more than 1000 m from the buildings and are not included in the 7gure. Each group of three symbols represents one chick (down and contour) and its parent.

Arsenic Tin Mercury Feathers Lead

(refer to Table 4). Therefore we examined lead levels in this middle group as a function of the distance their nest was from any building (presumably one source of lead). Lead levels generally decreased with distance of the nesting territory from a building (Fig. 1). The relationship is clearest for down, both within the lead abatement sites (using a one-tailed test, s2"3.42, P(0.05), and when the three major study sties are compared. Lead levels in the remote area were lowest (geometric mean of 1050 ppb), they were intermediate in the lead-abatement sites (geometric mean of 2100 ppb), and they were highest near buildings with no lead abatement (geometric mean of 32,600 ppb). We did not expect a relationship for adults because they do not eat objects near their nests, as do young. Another method of examining the data is to compare the levels of heavy metals in normal birds with those showing signs of lead poisoning (drooped wings, Table 5). The patterns for feathers and down are similar. Laysan albatross chicks with drooped wings had signi7cantly higher levels of lead and manganese in their down and feathers, and signi7cantly lower levels of selenium and tin, than normal-appearing chicks (Table 5). There were no signi7cant differences in mercury, cadmium, chromium, and arsenic. Relationships among Feather Types One objective of this study was to examine the relationship between the levels of metals in parents

Cadmium Selenium Chromium Manganese Arsenic Tin Mercury

Droop-winged

Normal

15 40,200$6,070 (32,600) 740$230 (521) 1,630$176 (1,490) 2,750$425 (2,350) 9,720$2,110 (7,530) 270$107 (24.5) 1,270$412 (55.3) 2,010$171 (1,900) 12 31,900$6,630 (21,300) 189$51.5 (135) 1,100$145 (1,000) 1,600$383 (1,340) 2,210$349 (1,950) 183$49.2 (18.4) 1,230$663 (40.9) 1,810$132 (1,750)

35 2,410$370 (1,530) 773$218 (393) 2,570$222 (2,330) 2,890$366 (2,290) 3,270$393 (2,750) 155$39.8 (4.87) 3,680$708 (1,040) 2,100$74.4 (2,050) 35 978$262 (464) 496$196 (116) 1,700$187 (1,370) 1,940$275 (1,400) 1,630$215 (1,130) 182$41.4 (9.89) 3,420$642 (1,290) 2,150$119 (2,050)

Kruskal-Wallis s2 (P)

30.41(0.0001) 1.59(NS) 7.99(0.005) 0.09(NS) 18.74(0.0001) 1.36(NS) 7.26(0.007) 0.20(NS)

24.53(0.0001) 0.26(NS) 3.72(0.054) 0.15(NS) 3.30(0.07) 0.27(NS) 8.03(0.005) 2.18(NS)

Note. Given are means$SE; geometric means are given below in parentheses. All values are in ng/g (ppb dry weight); NS, not signi7cant.

and their chicks (Table 6). For Black-footed albatross the only signi7cant correlations (P(0.10) were for arsenic, and these were not what we had predicted (positive between adult vs chick down and negative for adult vs chick contour feathers. Arsenic was not correlated between adult and chicks of Laysan albatross. For Laysans, there were consistently and highly signi7cant correlations for selenium, chromium, and tin in adults and their chicks. In addition, cadmium and manganese were correlated between adult and chick contour feathers but not down. There were no consistent relationships between the levels of lead or mercury in any of these comparisons. There are several reasons for the low correlations. We did not know the gender of the

METALS IN ALBATROSS FEATHERS

TABLE 6 Correlations of Metal Levels Between Parents and Their Chicks (Adult Feathers vs Chick Down and Adult Feathers vs Chick Feathers)

Black-footed albatross Lead Cadmium Selenium Chromium Manganese Arsenic Tin Mercury Laysan albatross Lead Cadmium Selenium Chromium Manganese Arsenic Tin Mercury

Adult vs chick down

Adult vs chick contour

NS NS NS NS NS 0.42 (0.02) NS NS

NS NS NS NS NS !0.35 (0.07) NS NS

NS NS 0.49 (0.0001) 0.35 (0.005) NS NS 0.23 (0.07) NS

NS (0.0002) (0.0001) (0.0009) (0.0001) NS 0.39 (0.002) NS

0.46 0.64 0.41 0.64

Note. Given are Kendall q coef7cients and P values (NS, not signi7cant, and signi7es P'0.10).

parent doing the feeding (both parents feed chicks), but male and female albatrosses are known to make trips of different durations (Weimerskirch et al., 1997), and hence may have different exposure themselves. DISCUSSION

Species Differences As early as the late 1960s black-footed albatross on Midway showed higher levels of contaminants (DDT, PCB, mercury) than Laysan albatross (Fisher, 1973). In the mid-1980s, morbidity due to lead paint chips was reported in Laysans from Midway (Sileo and Fefer, 1983). Black-footed albatrosses were not examined, mainly because they do not nest near buildings on Midway. Work and Smith (1996) also demonstrated that albatross chicks nesting near buildings on Midway, and to a lesser extent on Kauai Island (Hawaii), had elevated lead levels and had lead paint chips in their proventriculus. They found that 62% of chicks next to buildings had elevated blood lead levels, ranging up to 26 lg/ml (Work and Smith, 1996), an extremely high level. Recently, Auman et al. (in press) reported that levels of total PCBs and organochlorine insecticides were higher in the plasma of chicks and adults, and

215

in the eggs, of black-footed albatrosses compared to Laysan albatrosses. Further, concentrations of PCBs in black-footed albatrosses were near those which could have subtle population level effects, and dioxin equivalents were near the concentrations that caused embryo lethality and deformities in 7sh-eating colonial waterbirds in the North American Great Lakes (Auman et al., in press). These factors were partly responsible for our study of heavy metals, since the additive effect of heavy metal burdens could place black-footed albatrosses further at risk. Considering eight metals and three feather types for birds nesting in the remote location (end of airstrip), we found that black-footed had higher levels than Laysans in 21 comparisons, 12 of which were signi7cant (P(0.05) and 5 highly signi7cant (P(0.001). Laysans had signi7cantly higher levels of selenium in adult feathers than black-footed albatrosses. Both species are relatively small albatrosses, distinguished by their Northern Hemisphere distribution and subtropical breeding range (Whittow, 1993a,b). On arrival at the breeding colonies on Midway, male Laysans average 3310 g (Fisher, 1967), while black-footeds average 3400 g (Frings and Frings, 1961). Both species delay breeding until they are 8}9 years old, and live 30}40 years. Thus adults may be expected to bioaccumulate heavy metals because they are long-lived. Although albatrosses may travel up to 2000 km from the nest to feed, they usually stay within a day’s travel (500 km) when feeding young (Fisher and Fisher, 1969). Outside the breeding season Laysan’s range mainly to the west and black-footeds mainly to the east of Midway (Harrison, 1990). Differences in metal levels may re8ect such differences in prey from different regions, but data on prey from different regions of the northern Paci7c are not available. The primary food of black-footed albatross is the eggs of 8ying 7sh, followed by squid and crustacea (Harrison et al., 1983), while the main food of Laysans is squid, followed by 8ying-7sh eggs, crustaceans, and 7sh (Whittow, 1993a). Thus they feed on the same foods, although the relative proportions differ, and their temporal patterns of foraging differ. Laysans feed largely at night, when deep-water squid come to the surface, while black-footeds feed mainly in daytime on clumps of 8ying-7sh eggs (Harrison, 1990) as well as by scavenging offal discarded by ships (Whittow, 1993b). By volume, quantitative analysis indicates that Laysans take 65% squid, while black-footeds take 50% 8ying-7sh eggs and

216

BURGER AND GOCHFELD

only 32% squid (Harrison et al., 1983). These differences in foods taken and in method and location of foraging may account for the species differences in dietary exposure to metals. Adult size and chick growth rates may contribute to the variation as well. The 8edging period (hatch to 8edge) is about 165 days for Laysan vs 140 for black-footed (Harrison, 1990). Parental Exposure Albatross adults are exposed to heavy metals and selenium through their food and water. Once ingested, contaminants can be excreted directly or absorbed; subsequently they can be delivered to target organs or sequestered in feathers (Braune, 1987, Lewis and Furness, 1991) or other tissues; females may also excrete metals in eggs and eggshells (Fimreite et al., 1982, Burger and Gochfeld, 1991, 1993, 1995b, 1998; Burger 1994). Kim et al. (1996) recently suggested that some pelagic seabirds (albatrosses and petrels) are capable of demethylating methylmercury in the liver and storing it as an immobilizable inorganic form. Heavy metals in the feathers represent circulating concentrations in the blood during the few weeks of feather formation, which in turn represents both local exposure and mobilization from internal tissues (Tejning, 1967; Braune and Gaskin, 1987; Lewis and Furness, 1991; Monteiro, 1996). Once the feather matures, the vascular connection atrophies, leaving the feather as a record of blood levels at the time of its formation, and the concentration of metals in the feathers remains nearly constant (Braune and Gaskin, 1987). It is thus important to understand both the timing and pattern of molt and where birds were at the time of the molt. For most birds, feathers and eggs can serve as an indicator of internal contamination (Goede and deBruin, 1984, 1986; Furness et al., 1986; Burger, 1993). These levels can then be used to assess whether there are potential reproductive de7cits in populations (Burger, 1994). Honda et al. (1990) suggested that metal levels in tissues of seabirds from the northern Paci7c Ocean come from natural processes and not from anthropogenic sources. Species that feed on squid and 7sh have high mercury levels, while those that feed only on squid often have high cadmium levels (Honda et al., 1990). There were no differences in cadmium in the feathers of adults, perhaps re8ecting a similar diet of squid (Harrison et al., 1983; Whittow, 1993a). However, black-footed albatross chicks had higher levels of cadmium in both down and feathers than Laysans, which might re8ect a higher diet of squid.

We did note that black-footed adults more often regurgitated whole or parts of squid to their young than Laysans (unpublished data). Cadmium levels in seabird feathers are usually less than 200 ppb (Burger, 1993), while those in the feathers of both Midway albatross species were higher. The geometric mean level of cadmium in the down of black-footed albatrosses on Midway was 1880 ppb, well above levels reported for other species. Most studies of metal contamination in seabirds have examined only mercury (Burger, 1993), making it dif7cult to compare other metals in species with similar food habits and lifestyle. The United Nations Group of Experts on Scienti7c Aspects of Marine Pollution noted that mercury, lead, and cadmium are the most critical metal pollutants in marine waters (Fowler, 1990), but few data are available for lead and cadmium. In a recent review, Furness and Camphuysen (1997) noted that pelagic seabirds show greater increases in mercury concentrations in feathers over the last 150 years than coastal ones, and these increases have been greatest for seabirds feeding on mesopelagic (nonsurface) prey. They attribute this difference to the methylation of mercury in low-oxygen, deeper waters by bacteria (Monteiro, 1996), and the higher concentrations of mercury in mesopelagic compared to epipelagic (surface) 7sh (Monteiro et al., 1996). In this study, we found that mercury levels were signi7cantly higher in adults than young, with levels in adult black-footed albatrosses 7ve times higher than those in adult Laysan albatrosses. This difference is particularly interesting because the albatrosses feed on the same foods, although the timing of foraging differs (Whittow, 1993a,b). Further, the levels of mercury in the feathers of adult blackfooted albatrosses (geometric mean of 17,700 ppb) are similar to the median for 7ve studies of mercury levels in albatrosses (20,000 ppb, Burger and Gochfeld, 1999). Levels in albatrosses, however, are the highest reported for any species. The relatively high levels of mercury in feathers of albatrosses may be due to bioaccumulation since albatrosses have a lifespan of about 50 years, which is greater than that of smaller seabirds. Presumably the albatrosses accumulate heavy metal burdens in their internal tissues, and these metals are available for mobilization and sequestration in feathers during feather formation (Tejning, 1967; Braune and Gaskin, 1987; Lewis and Furness, 1991; Montiero, 1996). Sublethal behavioral effects of lead and mercury in birds are associated with feather levels of 4000 to 5000 ppb (Eisler 1987, 1988; Burger and Gochfeld,

METALS IN ALBATROSS FEATHERS

1997a,b), with cadmium being more toxic at lower levels (Eisler, 1987). Thus, the levels of lead and cadmium in the feathers of adult albatrosses on Midway appear to be below the levels known to be associated with sublethal effects. However, the mercury levels in feathers of adult black-footed albatrosses are much higher than those that are associated with sublethal effects in laboratory studies (Eisler, 1988; Burger and Gochfeld, 1997b). It is possible, however, as Furness et al. (1986) suggest, that since some marine birds can demethylate mercury, these high levels are less toxic, but this requires further testing. The levels of selenium that are associated with adverse reproductive effects in bird eggs are far higher than those we observed in this study (Ohlendorf et al., 1986). Little is known of the levels that cause adverse effects in birds for the other elements, but the levels are below those found in other birds where there were no ill effects reported (Burger, 1993). Exposure of the Young Contaminant burdens in young birds can come from pollutants sequestered in the eggs (see above) or from exposure during development, which in seabirds is normally a function of the food parents provide to them. Albatross chicks weigh over 2000 g when they leave Midway compared to about 190 g at hatching (Whittow, 1993a), hence the transovarian maternal contribution to the 8edgling’s metal burden is relatively small (Thompson et al., 1991; Monteiro et al., 1994). Thus concentrations of metals in 8edgling feathers derive mainly from dietary intake of the chicks (shown in the laboratory with mercury, Lewis and Furness, 1991, 1993). In semiprecocial species, the metal concentrations in down at hatching come entirely from the egg since down was formed prior to hatching and the metals are sequestered in the down during embryonic development (Becker et al., 1993). Further, it is assumed that metal concentrations in eggs (and thus down) re8ect local exposure through the ingestion of contaminants just prior to egg laying (Furness, 1993; Lewis et al., 1993; Monteiro and Furness, 1995). Thus by comparing metal concentrations in hatchling down and fully formed feathers from the same chicks it is possible to examine the sources of exposure. The relationship of metal concentration in the down and 8edgling feathers of the same chick is complex, depending on whether the down is sampled at hatching (when it re8ects egg levels) or later in development when it may re8ect chick food exposure

217

as well. First, the levels of some metals correlate with those in eggs (for mercury, Becker et al., 1993; Stewart et al., 1997). However, Stewart et al. (1997) found no relationship between the concentrations of mercury in down and 8edgling feathers in Shetland Island seabirds. They attributed their 7nding to the fact that mercury in eggs represents accumulation over a longer period of time than exposure just prior to egg laying (when the adults were feeding around the colony), and 8edgling feather levels represent food parents collected from the vicinity of the breeding colony. Metal levels averaged higher in down than in contour feathers which may re8ect their different structural characteristics (Lucas and Stettenheim, 1972), or the time course of exposure (heavier earlier when down was forming). Several previous studies have found higher concentrations of mercury in down than in 8edgling feathers of (1) black-legged kittiwakes (Rissa tridactyla), Arctic tern (Sterna paradisaea), Arctic skua (Stercorarius parasiticus), and great skua (Catharacta skua) from the Shetlands (Stewart et al., 1997), (2) common terns (Sterna hirundo) from the Azores (Monteiro et al., 1994), and (3) herring gull (Larus argentatus) and common tern (but not black-headed gull, Larus ridibundus) from the German North Sea (Becker et al., 1994). Burger (1995) found lower concentrations of mercury, but higher concentrations of chromium and manganese and no difference for lead and cadmium in the down versus 8edgling feathers of herring gulls from Long Island (New York, U.S.A.; Burger, 1995). In this study, concentrations of most metals were higher in down than in the feathers of chicks. This may be due to the time course of development for these chicks. We sampled chicks weighing between 1000 and 1300 g (compared with (200 g at hatching) and about 2000 g at 8edging. The major growth spurt for albatross chicks occurs when they still have down, and while the individual down feathers are similarly elongating and have an active blood supply. In the present study, however, we collected down at the same time we collected fully formed feathers from the same chicks. Thus the down was not hatchling down, as is usually collected, but was down from nearly full-grown chicks. Since the down continues to grow as the chicks grow, and has an intact blood supply, metal accumulation in the down represents metals not only from the female but also from foods gathered by both parents. Further, the chicks have had several months to sequester heavy metals in their down feathers, but only a few weeks when their feathers were growing. The down feathers are pushed out by the developing feathers, and in some

218

BURGER AND GOCHFELD

cases the down is still attached to the end of fully formed breast feathers. The presence of signi7cantly higher levels of mostmetals in down compared to either their own feathers or those of their parents suggests that they are continually exposed to heavy metals acquired from their foods. Although food is entirely provided by their parents, albatross chicks spend several months on their territory, and during this time they ingest food and other objects they 7nd lying near their nests. While in the remote locations of Sand Island the only objects chicks 7nd are food items left by parents, near the shore and near buildings the chicks pick up dirt, paint chips, and other things (Sileo and Fefer, 1983). The Laysan feathers (and down) collected from chicks whose nests were near buildings without lead abatement had lead levels that were 10 times higher than those in chicks nesting elsewhere on the island, indicating clear exposure differences. Work and Smith (1996) likewise found much higher lead exposure for chicks \17 m from buildings. We expected that adults would have higher concentrations of metals in their feathers than young because they have had several years to bioaccumulate metals in their internal tissues, and these can be mobilized into the blood and deposited in feathers during formation (see above). Burger (1993) summarized studies of metals in birds and reported that adults had signi7cantly higher concentrations than young for mercury (20 of 21 studies), lead (4 of 7), cadmium (3 of 5), manganese (5 of 5), and selenium (3 of 3), with chromium showing less of a difference (only 1 of 4 studies). Since then, the same result has been shown for other species, mainly gulls and terns (Thompson et al., 1993; Gochfeld et al., 1996; Burger, 1996; Stewart et al., 1997; Burger and Gochfeld, 1997c). In the present study, however, where there were differences, levels were the highest in down compared to feathers of their own or their parents (except for mercury). For both albatrosses, there were generally no differences between the levels in the feathers of adults and their young (except for chromium). For chromium, black-footed albatross adults had lower levels than their young, and the reverse was true for Laysans. For black-footed albatrosses, the differences in chromium levels were great; levels in down and feathers of chicks were nearly 10 times higher than those in adults. We cannot account for this difference at this time, but it bears further examination. There were two exceptions to the generalization that levels were higher in down compared to chick or

adult feathers: mercury and lead. Lead was a dramatic exception to the general lack of differences between metal concentrations in contour feathers of adults and their chicks since young Laysan albatrosses obtained high concentrations from ingestion of lead paint (Sileo and Fefer, 1983). Lead concentrations, however, should be higher only in Laysan albatross young from nests near buildings where lead paint 8akes off. In this study, we found this to be the case. There were no species differences in lead levels in the feathers of chicks and their parents from nests in the same location on Sand Island (refer to Table 2). However, when Laysans are examined separately, lead levels were lowest in chick feathers from the airstrip (the most remote location, where black-footeds also nested), slightly higher in chicks whose nests where near buildings where lead paint had been removed, and were 10 times higher in the feathers of chicks near buildings with 8aking lead paint. Mercury Mercury is the one metal that nearly always shows bioaccumulation with age (Burger, 1993; Furness, 1997). The large differences in mercury levels in feathers of adult and young are no doubt due to the large age differences while young were less than 6 months old, adults could be between 10 and 50 years old, giving them many more years to accumulate metals, perhaps not even reaching a steady state. Comparisons of Adults and Their Young Correlational analyses for pollutants are often unsatisfying, since many factors may weaken the correlations. The only signi7cant correlations for black-footed albatross was for arsenic, and we found the con8icting relationship (signi7cantly positive for chick down and negative for chick contour feathers) puzzling. There were more positive relationships for Laysans. We would expect to have signi7cantly positive correlations between adult female feathers and the down of newly hatched chicks. Correlations between adult males and their chicks would be much weaker or nonexistent. As chicks grow, the correlations should weaken. The metal levels in adult feathers were deposited during the molt cycle prior to commencing breeding (molt and breeding are offset to conserve energy), while the metal levels in chicks are deposited from food brought by the parents. Thus the differences between species may re8ect the fact that black-footeds change their feeding area,

219

METALS IN ALBATROSS FEATHERS

while Laysan’s feed in the same area or on the same food during their molt and while feeding young. An avenue for future study is whether correlations will be stronger for essential elements (selenium, chromium, manganese) than for nonessential ones (lead, mercury, cadmium). The data in the present study are partially consistent with this view for Laysans but not for black-footed. Health Implications for Midway Our results clearly indicate that chicks living near buildings that did not have lead paint removed had lead levels in their feathers that were 10 times higher than chicks from elsewhere on Sand Island, and we found clinically apparent lead poisoning. Further, lead levels in feathers of chicks decreased as a function of distance from lead-abated buildings. The source of the lead is presumably from lead paint 8akes (Sileo and Fefer, 1983), and we found lead paint 8akes in the stomachs of some dead chicks that had drooping wings when they were still alive (unpublished data). Our data thus suggest that buildings where lead paint has not been removed still pose a problem for young albatrosses, and that there is still some risk even near buildings where lead paint has been removed. Although one must be careful in extrapolating from albatrosses to people, it is worth noting that the human population is changing on Midway Island. Since World War II the military has occupied Midway, with attendant restrictions on families and strict restrictions on movement on the island. However, in 1997 the U.S. Fish and Wildlife Service assumed complete control of Midway as a National Wildlife Refuge. The Service is encouraging the development of ecotourism (for seabirds) and 7shing on the island. There is also military tourism: men who served there during and after the War are returning with their families to visit the island. Thus, there will be increased human use of the island, including by small children who might ingest dirt. While the problem may be less severe for transient tourists, it may prove problematic for the families living on the island who manage the refuge and service the tourist industry. ACKNOWLEDGMENTS We thank P. Pyle, R. Shallenberger, and N. Seto for their logistical help and insights into albatrosses while we were on Midway. P. Stettenheim provided valuable information on the growth of down feathers. We thank the Midway Atoll National Wildlife Refuge for permits to work on Midway (78642), the U.S.

Fish and Wildlife Service for collecting permits, and the Consortium for Risk Evaluation with Stakeholder Participation (CRESP) through the Department of Energy (AI DE-FC01-95EW55084) for partial funds to attend the Cooper meeting in Hawaii, and the Occupational and Environmental Health Sciences Institute and NIEHS (ESO 5022) for partial funds for heavy metal analysis.

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