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          Arch. Environ. Contam. Toxicol. 32, 217 (1997)
          � Springer-Verlag New York, Inc. 1997 


Heavy Metal and Selenium Concentrations in
Feathers of Egrets from Bali and Sulawesi, Indonesia 

J. Burger, M. Gochfeld 


Abstract 


Herons and egrets are ideal organisms to use as indicators of heavy
metal exposure in an ecosystem because different species feed at
different levels of the food chain and live in both coastal and inland
habitats. This paper reports on the concentration of heavy metals and
selenium in the feathers of cattle egrets Bubulcus ibis that were
examined from nesting and roosting sites in Bali and Sulawesi,
Indonesia, and in feathers of little egrets Egretta garzetta and
intermediate egrets E. intermedia from the same colony in Bali.
Mercury and manganese concentrations were significantly higher in
cattle egrets from Bali compared to Sulawesi, but otherwise there
were no significant differences. There were significant differences in
lead, cadmium and mercury among the three egret species nesting on
Bali: 1) the cadmium and mercury concentrations related to size and
trophic level (insectivorous cattle egrets had the lowest concentrations,
fish-eating intermediate egrets had the highest concentrations), and 2)
cattle egrets had significantly lower concentrations of lead than the
other two species. For cattle egrets, secondary flight feathers had
significantly higher levels of cadmium and mercury, and lower levels of
manganese, than mixed breast and tertiary feathers, reflecting temporal
differences in exposure. 

Introduction 


Increasingly, governmental and private agencies, and the general
public, are interested in assessing the health and well-being of our
global environments. With the realization of the magnitude of global
transport of many pollutants (Porcella 1994), there is renewed interest
in evaluating levels of toxics in ecosystems. Yet, it is not possible to
examine pollution levels in all organisms, in all ecosystems, world wide.
Thus it is necessary to select indicators of environmental degradation
that can be used to assess ecological health. 

Birds are useful models for the examination of pollutant levels over
wide geographical areas because they often are high on the food chain
and live for many years, allowing for bioaccumulation and detection of
detrimental levels (Walsh 1990; Burger 1994). Many species, or
closely related species, breed over large areas, in a variety of habitats,
in both coastal and inland habitats. 

Birds are visible and conspicuous, and their population levels,
pathologies and reproductive success can be measured and monitored
(Batty 1989). Moreover, the general public is interested in the
well-being of birds, and there is alarm when sick, injured or dying birds
are evident. Birds have some disadvantages: 1) they are mobile,
making it difficult to determine where they acquired the toxics, 2) some
species feed over a wide geographical area, and 3) endangered or
threatened species cannot easily be collected. These disadvantages
can be mitigated by examining levels in non-migratory species or in
young birds that have acquired all of their food locally. Levels of some
pollutants, such as heavy metals, can be determined from feathers, a
noninvasive technique that does not disrupt the bird, allowing for
sampling of endangered species (Goede and deBruin 1984, 1986;
Burger and Gochfeld 1991; Burger 1994). 

In this paper the concentrations of lead, mercury, cadmium, selenium,
chromium and manganese are examined in the feathers of cattle egrets
Bubulcus ibis from nesting and roosting sites in Bali and Sulawesi,
Indonesia, and in feathers of little egrets Egretta garzetta and
intermediate egrets E. intermedia from the same colony in Bali.
Indonesia is mostly agrarian, and is not highly industrialized, suggesting
that concentrations of metals might be relatively low. However, the
land is primarily volcanic, which might contribute to metal burdens in
superficial layers of soil. 

As a group, herons and egrets are especially useful bioindicators
because of their range in diet, range in habitats, and longevity.
Moreover, some species occur over most temperate and tropical
regions of the world, nesting in inland and coastal regions, along rivers,
and near other large bodies of water. Cattle egrets have become
nearly cosmopolitan in their nesting range (Hancock and Kushlan
1984), and they often nest near human habitations. Cattle egrets are
relatively low on the food chain because they eat primarily insects,
while the fish-eating little and intermediate egrets are at a higher
trophic level. Moreover, these egrets are non-migratory in Indonesia,
and thus reflect local exposure to contaminants. Indonesia has a
tropical climate, and the rice fields where cattle egrets forage are
present all year. 


Study Areas 


Indonesia, with its associated water, is one of the largest countries in
the world. Located on the equator, it has a nearly uniform climate
throughout the world, allowing for birds to be non-migratory. Feathers
were collected at roosting-colony sites on two islands, Bali and
Sulawesi. The area surrounding both study sites was primarily rice
paddies, with vegetable crops and cattle grazing in the higher regions.
At both sites the roosting-colony sites were at higher elevations, but
birds moved among the rice paddies and other agricultural areas. 

Feathers were collected under permits issued through Indonesian
Consulate in New York City, and stored in metal-free envelopes for
later analysis. 


Preparation and Residue Analysis 


Metal concentrations for feathers were analyzed in the Elemental
Analysis Laboratory at the Environmental and Occupational Health
Sciences Institute in Piscataway, New Jersey. Feathers were washed
vigorously in deionized water alternated with acetone to remove loosely
adherent external contamination (Applequist et al. 1984; Burger 1994),
and air dried overnight. Feathers were digested in 70% nitric acid in a
microwave vessel for ten min under 440 kilos per square cm pressure,
and samples were subsequently diluted in deionized water. Mercury
was analyzed by cold vapor technique, and all other metals were
analyzed by graphite furnace atomic absorption (Burger and Gochfeld
1991). All concentrations in feathers are expressed in parts per billion
(ppb) on dry weights obtained from the air dried specimens. Detection
limits were 2 ppb for mercury, 0.7 ppb for selenium, 0.15 ppb for lead,
and below 0.09 for the other metals. All specimens were run in
batches that included a standard calibration curve and spiked
specimens. The accepted recoveries ranged from 87 to 105%, and
batches with recoveries less than 85% were rerun. The Coefficient of
Variation on replicate, spiked samples ranged from 3 to 6%. Further
quality control included periodic blind analysis of an aliquot from a
large
sample of known concentrations, and blind runs of duplicate samples. 

Results 


Heavy metal and selenium concentrations varied as a function of
location, species, and feather type (Tables 1, 2). Cattle egrets from
Bali had significantly higher concentrations of mercury and manganese
in their feathers than those from Sulawesi; there were no other
significant differences. 

There were no significant differences in concentrations of selenium,
chromium, and manganese among the three species of egrets nesting
at the colony on Bali. However, lead concentrations were significantly
lower in cattle egrets compared to the other species (Table 1).
Cadmium and mercury concentrations were lowest in cattle egrets, and
highest in intermediate egret. 

For cattle egret, secondary feathers had significantly higher
concentrations of cadmium and mercury, and significantly lower levels
of manganese, than breast and tertiary feathers (Table 2). 

Except for cadmium and mercury (r = 0.27, P < 0.05), there were no
significant correlations among metal levels for feathers of cattle egret
(Table 3). There were a number of significant correlations among
metal levels for little egret, but only two for intermediate egret (Table
3). 

Discussion 


Methodological Considerations 

Ideally, without time, money, or logistical constraints, feathers should
be collected from the same place on each bird, and analyzed by
individual. This allows for examination of individual variation. However,
in this study feathers were pooled from 2-3 birds. This has the
advantage of increasing the number of birds examined, reducing the
risk of sampling bias, but does not allow for examining individual
variation. 

Metal concentrations in feathers reflect metal levels at the time of
feather formation, when the blood supply is intact (Goede and deBruin
1984, 1986). Circulating levels can come from current exposure
(through food or water) or from mobilization of metals stored in other
tissues (Braune and Gaskin 1987; Lewis and Furness 1991; Walsh
1990). If exposure is similar throughout the year, then an equilibrium
should be reached between circulating levels in the blood and in the
other body compartments. However, during molt metals can be
mobilized from tissues. Thus, it is possible that older birds might have
more metal available for mobilization and sequestration in feathers than
young birds. 

Another methodological problem with interpreting metal concentrations
in feathers involves knowing where the bird was when the feather was
forming. Since the egrets in Indonesia are non-migratory, the exact
timing of feather formation is less critical. Indonesia has stable
temperatures because it is located on the equator, and thus pastures,
flooded rice fields and fish farms are available all year. The nesting
colonies are used throughout the year as roosting sites. Nonetheless, if
exposure varied dramatically during the year, as might occur if farmers
used different amounts of chemicals at different times, then levels in
feathers might not reflect variations in pollutant levels during the year.
Differential chemical application seems unlikely in Bali and Sulawesi
since at any given point in time adjacent rice fields are in different
stages of development, and a small geographical area has rice fields in
all stages of development. Further, feathers from young birds are
usually the best bioindicators of exposure because they were grown
from foods derived entirely within the region of the nesting colony
(Burger 1994). However, in this case, the adults are nonmigratory,
eliminating this problem. 

The final methodological problem relates to which feathers are
analyzed. In general, breast feathers are a better indicator of metal
levels (Walsh 1990; Lewis and Furness 1991). In this paper we used a
combination of breast and tertiary feathers for the three species
examined in Bali. The data from cattle egrets indicated that mercury
and cadmium levels were higher in secondary feathers compared to
the others. Thus, these data do indicate that it is important to use the
same feathers when comparing across species and across locations. 

Species Differences in Metal Levels 

Species that are higher on the food chain should have higher
concentrations of heavy metals and selenium because they have longer
to bioaccumulate them. Cattle egrets are relatively low on the food
chain as they primarily eat insects, while the other two species eat fish,
other vertebrates (such as frogs) and invertebrates. In this study,
where there were significant differences in concentrations, cattle egret
had the lowest levels, as predicted by food chain relationships. Little
and intermediate egrets had similar levels of lead, but intermediate
egrets (the larger of the two), had higher levels of cadmium and
mercury. Thus, cadmium and mercury reflect both body size and food
chain differences. 

These species differences in lead, mercury, and cadmium levels are
nonetheless interesting because all three species feed in the same rice
fields. Cattle egrets, however, also feed along the roads on insects,
which may account for their lower concentrations of some metals. 

Locational Differences in Metal Levels for Cattle Egrets 

The cattle egrets nesting on Bali had significantly higher levels of
mercury and manganese than those from Sulawesi. This may reflect
the significantly higher human population levels in Bali. The colony in
Bali was located in the middle of a town that was surrounded by rice
fields and heavy agriculture, while the birds from Sulawesi lived on
grazing land. In both cases the birds are non-migratory, remaining
within the same island from year to year. 

Metal Levels in Egrets in Indonesia Compared to Elsewhere 

There are several advantages of examining metal levels in egrets: 1)
egrets frequently nest in colonies near areas of human activity, 2) they
represent different levels on the food chain since cattle egrets eat
insects, and the other species feed on fish of different sizes, 3) they
nest throughout much of the world, and 4) metal concentrations have
already been reported in a number of species worldwide. Moreover,
the egrets nesting in Indonesia are particularly useful because they are
nonmigratory, and reflect local exposure throughout the year. Thus,
they can be useful bioindicators of contamination. 

Cattle egrets now nest on most continents, and data are available on
heavy metal contamination. The concentrations of heavy metals and
selenium from this study in Indonesia are within the range reported for
cattle egrets nesting in New York, Delaware, Puerto Rico, and Egypt
for lead, mercury, cadmium, and selenium, but chromium
concentrations are lower and manganese concentrations are higher
than those reported elsewhere (Burger et al. 1992). Among all five
sites, the cattle egrets from Indonesia had the second highest
concentrations for lead and cadmium (Burger et al. 1992). Relatively
high concentrations of lead in cattle egret feathers may be partially
accounted for by the continued use of leaded gasoline in Indonesia;
cattle egrets feed on insects along the road where lead deposition is
likely to be high. Cattle egrets nesting in Hong Kong, where leaded
gasoline was used until 1991, had similarly high concentrations of lead
in their feathers (Burger and Gochfeld 1993). Mercury, selenium and
chromium were all much higher in the cattle egrets from Hong Kong
compared to Indonesia. 

For the fish-eating little egrets: 1) lead and manganese concentrations
were similar in Hong Kong and Indonesia; 2) mercury, selenium, and
chromium concentrations were lower in Indonesia; and 3) cadmium
concentrations were many times higher in Indonesia than Hong Kong
(Burger and Gochfeld 1993). Honda et al. (1986) also reported metal
concentrations for egrets from Korea; the egrets from Indonesia had
lower levels of mercury, but higher levels of lead, cadmium, and
manganese. These two comparisons suggest that cadmium was much
higher in Indonesia compared to either Korea or Hong Kong, and lead
and manganese were higher in Indonesia and Hong Kong than Korea. 

Cadmium enters the environment naturally from erosion in rocks and
volcanic activity, and from anthropogenic sources. Anthropogenic
sources include the purification of ores (smelters, mines), and from
commercial products such as batteries, paints and plastic stabilizers
(Parmeggiani 1983). Along with lead and mercury, global pollution is
likely to arise because of atmospheric transport (Furness et al. 1990).
Cadmium can be a neurotoxin and can interfere with calcium uptake
(Chang and Fu (1990). It also causes kidney toxicity in vertebrates, is a
carcinogen, and in birds, causes decreased testis weight and
spermatogenesis failure (Richardson et al. 1974; White et al. 1978). 

European soils usually have cadmium concentrations of 0.07 to 1.1
ppm (Kabata-Pendias and Pendias 1984). Cadmium accumulates in
insects, and is then transferred to fish (Dallinger et al. 1987;
Hatakeyama and Yasuno 1987), which could account for this high
levels in the egrets in this study. Further, since Indonesia is highly
volcanic, it is possible that the high levels of cadmium in the feathers
of
egrets reflect this source. Although cadmium levels in feathers of
many bird species are generally low (Burger 1994), the relatively high
levels of cadmium in feathers of Hawaiian seabirds (Cheng et al.
1984) may corroborate this, since these areas are also volcanic. 

Another consideration with cadmium levels in feathers is the
controversy surrounding whether feathers accumulate it; some authors
have found high levels (Mayack et al. 1981) while others have not
(Osborne et al. 1979). If cadmium is present, however, it is likely due
to sequestration from the blood since Goede and deBruin (1984) found
no increase in cadmium over time within the same feather, and no
external contamination attributable to immersion in tidal water or mud. 

eferences   [Links are to the NCBI PubMed database of biomedical
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Title: Archives of Environmental Contamination and Toxicology 32, 217 (1997)

Arch. Environ. Contam. Toxicol. 32, 217 (1997) © Springer-Verlag New York, Inc. 1997 Heavy Metal and Selenium Concentrations in Feathers of Egrets from Bali and Sulawesi, Indonesia J. Burger, M. Gochfeld

Table 3. Correlation coefficients (Kendall tau) for metal concentrations within feathers for Little egrets (N = 23, above diagonal) and Intermediate egret (below diagonal)

	Lead	Cadmium	Mercury	Selenium	Chromium	Manganese
Lead	-	NS	-0.37 (0.01)	NS	0.32 (0.03)	0.31 (0.03)
Cadmium	NS	-	NS	NS	-0.30 (0.05)	-0.37 (0.02)
Mercury	NS	NS	-	NS	-0.40 (0.009)	-0.36 (0.02)
Selenium	-0.35a (0.05)	NS	NS	-	NS	-0.37 (0.01)
Chromium	NS	0.35a (0.06)	NS	NS	-	0.49 (0.001)
Manganese	NS	NS	NS	NS	NS	-

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^aCattle egret had the same correlation for lead and selenium and for chromium and cadmium.

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© Springer-Verlag New York, Inc. 1997

Title: Archives of Environmental Contamination and Toxicology 32, 217 (1997)

Arch. Environ. Contam. Toxicol. 32, 217 (1997) © Springer-Verlag New York, Inc. 1997 Heavy Metal and Selenium Concentrations in Feathers of Egrets from Bali and Sulawesi, Indonesia J. Burger, M. Gochfeld

Table 2. Comparison of the mean (± standard error) concentration of metals (ppb, dry weight) in secondary flight feathers and breast/tertiary feathers of Cattle Egrets in Bali. Geometric mean in parenthesis. NS = not significant

	Breast and Tertiary	Secondary Flight	Wilcoxon X2 P
Number of samples	12	12
Lead	2,720 ± 704 (2,287)	2,698 ± 364 (2,069)	NS
Cadmium	235 ± 81 (145)	978 ± 294 (675)	6.8 (0.009)
Mercury	383 ± 48 (327)	808 ± 62 (783)	15.9 (0.001)
Chromium	603 ± 80 (570)	732 ± 140 (603)	NS
Manganese	19,290 ± 3,395 (17,343)	7,898 ± 1,457 (6,654)	9.2 (0.002)

Next table: Table 3

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© Springer-Verlag New York, Inc. 1997

Title: Archives of Environmental Contamination and Toxicology 32, 217 (1997)

Arch. Environ. Contam. Toxicol. 32, 217 (1997) © Springer-Verlag New York, Inc. 1997 Heavy Metal and Selenium Concentrations in Feathers of Egrets from Bali and Sulawesi, Indonesia J. Burger, M. Gochfeld

Table 1. Mean heavy metal and selenium concentrations (ppb, dry weight) in mixed breast and tertary feathers of egrets in Indonesia. NS = not significant. Given are means ± standard errors

	Cattle Egret		Wilcoxon Company within Cattle Egret	Bali		Wilcoxon Comparing all Three Egrets
	Sulawesi	Bali		Little Egret	Intermediate Egret
Number	12	12		23	17
Lead	3,578 ± 201 (1,708)	2,720 ± 704 (2,287)	NS	3,527 ± 486 (2,810)	3,671 ± 440 (3,249)	4.7 (0.09)
Cadmium	357 ± 204 (148)	235 ± 81 (145)	NS	746 ± 257 (329)	1,939 ± 360 (1,410)	18.3 (0.001)
Mercury	60 ± 32 (17)	383 ± 48 (327)	9.6 (0.002)	563 ± 62 (480)	1,127 ± 285 (744)	8.5 (0.01)
Selenium	887 ± 167 (796)	624 ± 85 (568)	NS	748 ± 75 (690)	814 ± 133 (684)	NS
Chromium	701 ± 68 (683)	603 ± 80 (570)	NS	575 ± 85 (434)	643 ± 146 (451)	NS
Manganese	5,942 ± 943 (5,182)	19,290 ± 3,395 (17,340)	11.0 (0.0009)	13,078 ± 2,573 (8,777)	16,670 ± 2,707 (13,863)	NS

Next table: Table 2

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© Springer-Verlag New York, Inc. 1997

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