Metal levels in feathers of 12 species of seabirds from Midway Atoll in the northern Pacific Ocean

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Abstract

Seabirds are excellent subjects for examination of heavy metals because they are long-lived, feed at different distances from land, and exhibit different trophic levels. In this paper we compare the levels of lead, cadmium, mercury arsenic, chromium, manganese, selenium, and tin in the feathers of birds nesting on Midway Atoll in the northern Pacific Ocean. We test the null hypothesis that there are no interspecific differences in the levels of metals in the feathers of the adult black-footed albatross (Diomedea nigripes), Laysan albatross (Diomedea immutabilis), red-footed booby (Sula sula), great frigatebird (Fregata minor), Bonin petrel (Pterodroma hypoleuca), Christmas shearwater (Puffinus nativitatis), red-tailed tropicbird (Phaethon rubricauda), wedge-tailed shearwater (Puffinus pacificus), brown noddy (Anous stolidus), sooty tern (Sterna fuscata), grey-backed tern (Sterna lunata), and white tern (Gygis alba), and young of some of these species. There were interspecific differences in the levels of all metals for adults. Christmas shearwater had the highest levels of lead, cadmium, selenium and manganese, but the second lowest levels of mercury. In general, metal levels were the lowest in the smallest species (white tern), but were not the highest in the largest species (black-footed albatross), except for manganese, arsenic and mercury. There was a high variance in metal levels among adults for some species, but not for others. White tern adults were variable for lead, while Christmas shearwaters were variable for lead and cadmium. Compared to the means for metals in other birds generally (after Burger, 1993), Christmas shearwaters had higher levels of lead, white terns, brown noddy, Christmas shearwater, frigatebirds and Laysan albatrosses had higher levels of cadmium, and bonin petrel, wedge-tailed shearwater, tropicbirds, frigatebirds, red-footed boobies, and both albatrosses had higher levels of mercury. Whereas the means for lead and cadmium were below the known effects levels, some individuals had levels high enough to cause adverse effects in the birds. The mean values for mercury in Bonin petrel, red-tailed tropicbird, and black-footed albatross were higher than the levels known to cause adverse reproductive and behavioral effects.

Introduction

There is considerable concern about the levels of heavy metals in organisms and their ecosystems, particularly species at higher trophic levels subject to bioaccumulation. While anthropogenic contaminants from urban, industrial and agricultural runoff are a major issue, levels are augmented by natural geological processes (Mailman, 1980). Global transport and deposition is an important source of mercury for many ecosystems, including the ocean (Fitzgerald, 1989).

Seabirds are particularly vulnerable to contaminants because they are long-lived and are often at the top of their food chains (Hunter and Johnson, 1982, van Straalen and Ernst, 1991, Burger et al., 1992, Burger et al., 1994). Because they are often top trophic level carnivores, seabirds have been used as bioindicators of environmental contaminants (Monteiro and Furness, 1995, Lewis and Furness, 1993).

There is a need for data on the same species in a wide range of geographical areas and for data comparing many different species representing different trophic levels from the same general area. Each approach provides useful information.

Feathers are useful indicators of heavy metal contamination because birds sequester heavy metals in their feathers, and the proportion of the body burden that is in feathers is relatively constant for any metal (Burger, 1993). For some bird species a relatively high proportion of the body burden of certain metals is in the feathers (Burger, 1993). Monteiro et al. (1998) showed that there is a high correlation between the levels of mercury in the diet of seabirds, and the levels in feathers, thus seabirds can be used as indicators of food chain effects.

In this paper we compare the levels of metals in the feathers of twelve seabird species nesting on Midway Island in the northern Pacific Ocean. For all species we present levels for feathers of adults. Young birds were available for only six species. We test the null hypothesis that there were no differences in metal levels in feathers as a function of age, size, and trophic level position. We predicted that: (1) larger birds would have higher levels of metals, consistent with their generally longer life; and (2) birds at higher trophic levels would have higher levels than those that are lower, because of bioamphlification. We were particularly interested in whether the levels of metals in feathers from the birds at Midway were similar to those known to be associated with behavioral deficits or lowered reproductive success in laboratory studies.

Although the means and standard errors for the metals, except tin, have been presented elsewhere for some species (Burger and Gochfeld, 2000a, Gochfeld et al., 1999), the following information is presented for the first time: (1) levels of tin for 12 seabird species; (2) ranges for all metals in all species; and (3) metal concentrations for red-footed booby (Sula sula) and great frigatebird (Fregata minor). Furthermore, by presenting the metals for all species in one place it is possible to examine the trophic level relationships.

Section snippets

Materials and methods

Midway Atoll (28°15′ N, 177°20′ W) is 1850 km north-west of Honolulu and is comprised of three islands, of which only Sand Island is occupied by humans. 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.).

In the early 20th century, Midway was developed as a communication station, and because of its strategic position, was a

Results

The metal levels in the feathers of adult red-footed booby and great frigatebird are shown in Table 1. There were significant species differences for all metals except chromium and arsenic. Frigatebirds had significantly higher levels of lead, cadmium, and selenium, while boobies had higher levels of manganese and mercury.

The means and standard errors are in Table 2 for adults of all 12 species and in Table 3 for the young of six species. For all metals there was a significant interspecific

Red-footed booby and great frigatebird

The other species examined in this paper are treated in more detail elsewhere. However, metal data for the red-footed booby and great frigatebirds are presented in this paper for the first time. Red-footed boobies usually feed in deep, warm waters, often far from land (Palmer, 1962). They eat mostly flying fish and squid, usually obtained by diving vertically into the water (Palmer, 1962, Schreiber et al., 1996). Fish often make up 65–99% of the diet, depending upon location, and the fish range

Conclusions

The results of this study indicate that although all 12 species nested on Midway Island, there were significant interspecific differences in the levels of all metals in the feathers of adults. Furthermore, there were significant interspecific differences in feather levels for young of the six species whose young were old enough to collect fully-formed feathers for all metals except lead. These differences reflect trophic level differences, based on dietary information, and do not reflect the

Acknowledgements

We thank P. Pyle, R. Shallenberger, and N. Seto for their logistical help and insights into albatrosses while we were on Midway, P. and B. Murray for advice and companionship on Midway, T. Shukla for chemical analysis, R. Ramos for computer graphics, and C. Dixon, M. McMahon and S. Shukla for statistical assistance. We thank the Midway Atoll National Wildlife Refuge for permits to work on Midway (No. 78642), the US Fish and Wildlife Service for collecting permits, and the Consortium for Risk

References (65)

  • G.R. Phillips et al.

    Relation between trophic position and mercury accumulation among fishes from the Tongue River reservoir

    Environ Res

    (1980)
  • H. Applequist et al.

    Mercury stability in bird feathers

    Mar Pollut Bull

    (1984)
  • N.P. Ashmole et al.

    Comparative feeding ecology of sea birds of a tropical oceanic island

    Bull Peabody Mus Nat Hist

    (1967)
  • K.R. Bull et al.

    High levels of cadmium in Atlantic seabirds and sea-skaters

    Nature

    (1977)
  • J. Burger

    Metals in avian feathers: bioindicators of environmental pollution

    Rev Environ Toxicol

    (1993)
  • J. Burger

    A risk assessment for lead in birds

    J Toxicol Environ Health

    (1995)
  • J. Burger

    Heavy metal and selenium levels in feathers of herring gull (Larus argentatus): differences due to year, gender, age at Captree, Long Island

    Environ Monit Assess

    (1995)
  • J. Burger et al.

    Effects of lead on Larids: a review of laboratory and field studies

    J Toxicol Environ Health

    (2000)
  • J. Burger et al.

    Mercury bioaccumulation in organisms from three Puerto Rican estuaries

    Environ Monit Assess

    (1992)
  • J. Burger et al.

    Heavy metal concentrations in feathers of common Loons (Gavia immer) in the northeastern United States and age differences in mercury levels

    Environ Monit Assess

    (1994)
  • Burger J, Shukla T, Dixon C et al. Metals in feathers of sooty tern, white tern, grey-backed tern and brown noddy from...
  • Carboneras C. Procellariidae: Petrels and Shearwaters. In: del Hoyo, Elliott JA, Sargatal J, editors. Handbook of the...
  • W.C. Cooper

    The health implications of increased manganese in the environment resulting from the combustion of fuel additives: a review of the literature

    J Toxicol Environ Health

    (1984)
  • Eisler R. Selenium hazards to fish, wildlife, and invertebrates: a synoptic review. US Fish and Wildlife Service....
  • Eisler R. Cadmium hazards to fish, wildlife, and invertebrates: a synoptic review. US Fish and Wildlife Service....
  • Eisler R. Chromium hazards to fish, wildlife, and invertebrates: a synoptic review. US Fish and Wildlife Service....
  • Eisler R. Mercury hazards to fish, wildlife, and invertebrates: a synoptic review. US Fish and Wildlife Service....
  • Eisler R. Lead hazards to fish, wildlife, and invertebrates: a synoptic review. US Fish and Wildlife Service....
  • Fisher HI. Midway’s deadly antennas. July–August, 1–3. Audubon,...
  • H.I. Fisher et al.

    The visits of Laysan albatrosses to the breeding colony

    Micronesica

    (1969)
  • W.F. Fitzgerald

    Atmospheric and oceanic cycling of mercury

  • J.W. Franson

    Interpretation of tissue lead residues in birds other than waterfowl

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