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Organochlorines in Black-Crowned Night Heron (Nycticorax nycticorax) Eggs
Reflect Persistent Contamination in Northeastern US Estuaries
A. C. Matz, K. C. Parsons
Manomet Center for Conservation Sciences, P.O. Box 1770, Manomet, Massachusetts 02345, USA
Received: 21 November 2002 /Accepted: 5 June 2003
Abstract. Colonially nesting aquatic birds can indicate site-
specific contamination because they are high-level predators
and dependent upon local resources during the breeding sea-
son. We compared persistent organochlorine concentrations in
black-crowned night heron (Nycticorax nycticorax) eggs col-
lected in 1992–93 among areas of known contamination (New
York Harbor, Boston Harbor, Cape Cod, and Delaware Bay)
and a reference site (Nantucket Island) in the northeastern
United States (7–16 eggs/site). Total PCBs, p,p⬘-DDE, oxy-
chlordane, heptachlor epoxide, and trans-nonachlor were de-
tected in most eggs and were significantly higher in New York
Harbor compared to all other sites (ANOVA on factor scores
from the first principal component, which accounted for 75%
of data variance, p⬍0.0001). New York also had the highest
contamination index (the number of Superfund sites within 20
km of the colony) among the sites. Nantucket, the reference
site, had consistently low contamination in eggs, and the lowest
contamination index. We conclude that black-crowned night
heron eggs are useful indicators of site-specific persistent or-
ganochlorine contamination, as indexed by the number of
nearby Superfund sites.
If females are nonmigratory or arrive well in advance of laying,
eggs of colonially nesting birds are excellent indicators of
ecosystem contamination because these birds are often at a
high trophic level, dependent upon foraging areas near their
colony during the breeding season, and philopatric (Custer et
al. 1991; Kushlan 1993). Contaminant exposure in colonially
nesting wading birds (Ciconiiformes) have been associated
with spatial differences in agricultural chemical use (Parsons et
al. 2000), heavy metals (Fitzner et al. 1995), and dioxins and
furans associated with paper mills (Elliott et al. 1989; Henshel
et al. 1995). Specifically, black-crowned night herons (BCNH)
(Nycticorax nycticorax) have been used to indicate localized
persistent organochlorine (OC) contamination at sites through-
out North America (Ohlendorf 1981; Henny et al. 1984; Henny
and Blus 1986; Hoffman et al. 1986; Rattner et al. 1993, 1994;
Blus et al. 1997). They are primarily piscivorous (Davis 1993),
their foraging range is generally less than 25 km from the
colony (Hoefler 1979), and they arrive at breeding sites in the
northeastern United States approximately one month before
laying (Burger 1978).
We measured persistent OC contaminants in BCNH eggs
collected from colonies in four northeastern US estuaries (Bos-
ton Harbor, Cape Cod, New York Harbor, and Delaware Bay),
and from Nantucket Island, a nonestuarine offshore island, in
1992–93. Our objective was to determine if differences in
contaminant concentrations among the sites in BCNH eggs
were reflected in a site environmental quality index, the num-
ber of Comprehensive Environmental Response, Compensa-
tion, and Liabilities Act National Priorities List (Superfund)
sites within a 20-km radius of the colony.
Materials and Methods
Study Areas
We collected BCNH eggs in 1992–93 under appropriate state and
federal permits from colonies in New York Harbor and Cape Cod, and
in 1993 from Boston Harbor, Delaware Bay, and Nantucket. The New
York Harbor colonies were on non-barrier dredge spoil islands located
between Staten Island, New York and New Jersey in the Arthur Kill
(Prall’s Island, 40°36⬘N 74°12⬘W, and Isle of Meadows, 40°34⬘N
74°12⬘W), and managed by the City of New York. The Cape Cod
colony was on a barrier island (Sampson’s Island, 41°37⬘N 70°25⬘W)
managed as a wildlife refuge by the town of Barnstable, Massachu-
setts, off the south shore of Cape Cod. The surrounding area was
largely residential, except for cranberry farms and the Massachusetts
Military Reservation, a source of volatile organic compounds, PCBs,
and pesticides (www.epa.gov/superfund), approximately 10 km to the
northwest. The Boston Harbor colony was on one of approximately 30
drumlin islands in Boston Harbor (Middle Brewster Island, 42°20⬘N
70°53⬘W), managed by the National Park Service. The Delaware Bay
colony was on Pea Patch Island (39°35⬘N, 75°34⬘W) located in upper
Delaware Bay, and owned and managed by the State of Delaware.
Surrounding land uses included industry, agriculture, and residential
development. The reference colony was on a barrier beach peninsula
(Coatue, 41°17⬘N 70°06⬘W) on the north shore of Nantucket Island,
Correspondence to: A. C. Matz at present address; U.S. Fish and
Wildlife Service, 101-12th Ave., Box 19, Room 110, Fairbanks, AK
99701, USA; email: angela_matz@fws.gov
Arch. Environ. Contam. Toxicol. 46, 270 –274 (2004)
DOI: 10.1007/s00244-003-2265-9
ARCHIVES OF
Environmental
Contamination
and
Toxicology
© 2004 Springer-Verlag New York Inc.
MA, managed by the Nantucket Conservation Foundation. Forty per-
cent of the land area of Nantucket was open space; the remainder was
residential and agricultural.
Sample Collection
One egg per nest was collected during incubation from 7–16 nests
randomly distributed throughout each colony. Egg contents were re-
moved using chemically clean instruments, placed in chemically clean
jars, stored frozen, then shipped frozen via overnight mail to the
analytical laboratory. We rinsed eggshells with water, air-dried them
for at least four weeks, then averaged 3–5 (⫾0.005 mm) thickness
measurements taken over intact membranes at the equator with a
modified Starrett micrometer (L.S. Starrett Co., Athol, MA).
Analytical Chemistry
Egg contents were analyzed for 20 OC pesticides and metabolites and
total polychlorinated biphenyls (PCBs) as the sum of Aroclors (1242,
1248, 1254, and 1260), at Mississippi State Chemical Laboratory,
Mississippi State, MI, using established methods (Environmental Pro-
tection Agency 1980). Briefly, samples were mixed with anhydrous
sodium sulfate, soxhlet-extracted with hexane, dried, dissolved in
petroleum ether and extracted with acetonitrile saturated with petro-
leum ether. Residues partitioned into petroleum ether were transferred
to a Florisil glass column, then eluted with 6% diethyl ether/94%
petroleum ether (Fraction I, plus three additional fractions), followed
by 200 mL 15% diethyl ether/85% petroleum ether (Fraction II). Both
fractions were concentrated and Fraction I transferred to a silicic acid
column to separate PCBs, the residues were quantified by packed or
megabore column electron capture gas chromatography. Detection
limits were 0.01 g/g wet weight (ww) for pesticides and 0.05 g/g
ww for PCBs. No analytes were detected in procedural blanks. Spike
recoveries were within 70 –120%, except PCB 1260 in 1993 (57%) and
HCB (63% and 65% in 1992 and 1993, respectively). Relative percent
differences between duplicates were ⬍12%.
Data Analysis
Contaminants that were detected in ⬎90% of samples at all sites were
analyzed using multivariate analyses (Sparks et al. 1999) to control the
increased Type I error rate inherent in multiple univariate tests, and to
discern patterns or relationships not evident from univariate testing
(yet allow for examination of individual variables and post-hoc test-
ing). Analyte concentrations were corrected for moisture loss that
occurs during incubation (Stickel et al. 1973), the few non-detections
were substituted with a random number between zero and the detection
limit, and data were log-transformed to reduce heteroscedasticity and
achieve normality. Residues were not lipid-adjusted, as none were
significantly correlated with egg lipid content (Hebert and Keenleyside
1995). Data were then reduced to the principal components (PCs) that
accounted for ⱖ75% of the variance within the data. We used Analysis
of Variance (ANOVA) with PC factor scores as the dependent vari-
ables to test for differences among sites (Jackson 1991), with Bonfer-
roni-adjusted post-hoc testing. Eggshell thickness was also tested for
differences among sites (ANOVA), and for significant correlation with
p,p⬘-DDE (-4,4⬘-dichlorodiphenyl dichloroethene) concentrations
(Pearson’s r). Unless otherwise stated, ␣⫽0.05. Data were analyzed
with SYSTAT 7.0 and 8.0 (SPSS, Inc., Chicago, IL), and SAS 8.0
(SAS Institute, Inc., Cary, NC).
Contamination Index
There are many environmental quality indices for coastal and estuarine
sites, including monitoring programs such as the National Oceanic and
Atmospheric Administration’s (NOAA) Mussel Watch, sediment sam-
pling by state agencies, and the United States Environmental Protec-
tion Agency’s (USEPA) integrative Index of Watershed Indicators.
However, none were performed identically near all of the sampled
BCNH colonies. We therefore used the number of Superfund sites
within a 20-km radius of the colony, obtained from USEPA’s Super-
fund website (www.epa.gov/superfund). Sites included those with
PCBs or OC pesticides as primary contaminants of concern, and
landfills, which often have PCB or OC contamination. We graphically
compared this index to differences in BCNH egg contamination
among sites.
Results
We collected 7 BCNH eggs from Boston Harbor, 7 from
Delaware Bay, 16 from Cape Cod, 11 from New York Harbor,
and 8 from Nantucket. Only oxychlordane, heptachlor epoxide,
trans-nonachlor, p,p⬘-DDE, and total PCBs (sum of Aroclors
1242, 1248, 1254, and 1260) were detected in ⬎90% of sam-
ples at all sites. These contaminants were significantly different
among sites (ANOVA with factor scores from the first PC,
accounting for 75% of total variance and with factor loadings
ⱖ0.85, p⬍0.0001), with greater contaminant concentrations
at New York compared to all other sites (Table 1). The number
of Superfund sites with PCBs or OCs as primary contaminants
of concern also reflected PCB, DDE (Figure 1a), oxychlordane,
heptachlor epoxide, and trans-nonachlor contamination among
the sites, although inclusion of landfills increased Delaware
Bay’s index relative to the other sites (Figure 1b). Other
contaminants, which were not consistently detected (i.e., in
⬍90% of samples at one or more sites), were summarized
according to percent detections; some were found only in eggs
from New York Harbor or Cape Cod (Table 2).
Eggshell thickness was not different among estuaries (p⫽
0.350), and was negatively correlated with p,p⬘-DDE concen-
trations (Pearson r⫽⫺0.466, n⫽48, p⫽0.001) (New York
n⫽10 for this analysis only). Mean eggshell thickness at all
colonies (0.263 ⫾0.024 mm) was 4.4% thinner than the
pre-1947 norm (0.275 ⫾0.002 mm, n⫽142 eggs from
western US; Henny et al. 1984).
Discussion
Organochlorine contaminants detected in BCNH eggs reflected
the environmental quality index (the number of nearby Super-
fund sites). In spite of the relatively small sample sizes, New
York Harbor, which had the highest number of PCB/pesticide
and landfill Superfund sites near the colony, consistently had
the highest concentrations of persistent OC contaminants, and
some contaminants detected in New York Harbor eggs were
detected nowhere else. In contrast, the offshore site on Nan-
tucket, with no nearby Superfund sites, consistently had the
lowest contaminant concentrations. Trends from highest to
lowest contamination (Figure 1) initially appear to reflect in-
creasing urbanization and associated industries, with two ex-
OCs in Black-Crowned Night Heron Eggs 271
ceptions. The Cape Cod colony was in a non-urban watershed,
but was close to Otis Air National Guard/Camp Edwards (the
Massachusetts Military Reservation), a heavily contaminated
Superfund site (www.epa.gov/superfund/sites/npl/ma.htm#Otis
Air National Guard (USAF)). Delaware Bay had a large num-
ber of surrounding landfills, which have a variety of contami-
nants of concern. Exposure to other contaminants have been
documented at Pea Patch Island (Parsons et al. 2000; Rattner et
al. 2000).
Black-crowned night-heron populations have declined in
Table 1. Wet weight concentrations
a
of persistent organochlorine contaminants in black-crowned night heron eggs collected from five north-
eastern US sites,
b
1992–93
Contaminant
Nantucket
A
(n⫽8)
Delaware Bay
A
(n⫽7)
Boston Harbor
A
(n⫽7)
Cape Cod
A
(n⫽16)
New York
Harbor
B
(n⫽11)
oxychlordane 0.01 (ND–0.09) 0.02 (ND–0.03) 0.02 (0.01–0.04) 0.03 (ND–0.37) 0.06 (ND–0.23)
heptachlor epoxide 0.01 (ND–0.04) 0.01 (ND–0.02) 0.01 (ND–0.03) 0.01 (ND–0.15) 0.03 (ND–0.11)
trans-nonachlor 0.02 (ND–0.09) 0.03 (0.02–0.05) 0.05 (0.03–0.11) 0.05 (ND–0.54) 0.06 (ND–0.41)
total PCBs 1.47 (0.71–3.26) 3.03 (0.93–6.46) 3.83 (2.02–13.21) 5.35 (1.88–40.73) 6.98 (0.19–33.91)
p,p⬘-DDE 0.61 (0.17–9.45) 1.00 (0.68–1.55) 0.54 (0.35–1.36) 1.24 (0.19–12.72) 2.07 (0.07–
a
Given are geometric mean (and range), g/g, where ND is not detected at nominal detection limits of 0.01 g/g for pesticides and 0.05 g/g
for PCBs. Data were adjusted for moisture changes associated with development.
b
Unlike superscripts indicate significant differences among colonies (ANOVA on factor scores from the principal component that accounted for
75% of data variance, p⬍0.0001).
Fig. 1. (a) Geometric mean concentrations of total PCBs and p,p⬘-DDE (g/g wet weight) in black-crowned night-heron eggs from five sites in
the northeastern US, 1992–93. (b) The number of Comprehensive Environmental Response, Compensation, and Liabilities Act National Priorities
List (Superfund) sites within 20 km of the nesting colonies where the eggs were collected. Superfund sites included those with PCBs or pesticides
listed as primary contaminant of concern and landfills, which often have PCB or organochlorine pesticide contamination
272 A. C. Matz and K. C. Parsons
North America (Davis 1993), due in part to OC contaminants.
In this study, 8% of eggs had p,p⬘-DDE ⬎8 ppm (one each at
Cape Cod and Nantucket, and two at New York Harbor), which
Henny et al. (1984) associated with lower productivity in
western U.S. colonies. In spite of a significant relationship
between p,p⬘-DDE concentrations and eggshell thickness, how-
ever, p,p⬘-DDE residues in this study were far below the ⬎50
ppm associated with 20% decrease in eggshell thickness by
Henny et al. (1984). Total PCB concentrations (Table 1) from
the more contaminated sites approached concentrations found
in a contaminated site in Green Bay, WI (geometric mean of
9.32 g/g ww), where there were linear relationships between
total PCBs (as well as toxic equivalents and PCB congeners)
and hepatic cytochrome P450-associated monooxygenase ac-
tivities and P450 proteins (Rattner et al. 1994). Similar con-
centrations were correlated with decreased body weight at
hatching in pipping BCNH embryos from colonies in San
Francisco Bay (averages of 1.54 and 3.43 g/g ww) (Hoffman
et al. 1986).
More recent measurements of persistent contaminants in
BCNH embryos indicate decreasing concentrations through
time, however (Blus et al. 1997; Rattner et al. 2000). Ad-
ditionally, differential productivity at the study sites (except
Nantucket) was attributed to predation, starvation, and other
contaminants in addition to persistent OCs (Parsons et al.
2001), and Blus et al. (1997) concluded that establishment
of predators near BCNH colonies lead to decreased produc-
tivity.
Even with concentrations below effect levels, high trophic
status and colony philopatry ensure the utility of BCNH and
other wading birds as indicators of estuarine quality, which
includes environmental contaminants. Specifically, we found
that BCNH eggs reflected persistent organochlorine contami-
nation, as indexed by the number of nearby Superfund sites, in
northeastern US estuarine and coastal sites.
Acknowledgments. Funding and logistical assistance were pro-
vided by the US Fish and Wildlife Service New England Field
Office, Delaware Department of Natural Resources and Environ-
mental Control, New York City Audubon Society, New York City
Department of Parks, Nantucket Conservation Foundation, Geral-
dine R. Dodge Foundation, Massachusetts Audubon Society, Bos-
ton Harbor Islands State Park, Island Foundation, and Manomet
members. We also thank Drew Major and Ken Carr of the US Fish
and Wildlife Service, and Manomet Program Manager Amanda
McColpin for project assistance, and two anonymous reviewers.
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Table 2. Percent of black-crowned night heron eggs collected from
five northeastern US sites, 1992–93, in which organochlorine con-
taminants were detected
a
Contaminant
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(n⫽8)
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Bay
(n⫽7)
Boston
Harbor
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Cod
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b
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␥-chlordane
c
,
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d
,
toxaphene 0.0 0.0 0.0 0.0 0.0
HCB
e
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␥-HCH 0.0 0.0 0.0 0.0 27.3
-HCH 0.0 0.0 0.0 43.8 54.5
o,p⬘-DDE 0.0 0.0 0.0 25.0 9.1
␣-chlordane 12.5 14.3 100.0 6.3 0.0
o,p⬘-DDD
f
0.0 0.0 0.0 18.8 72.7
endrin
g
12.5 0.0 0.0 6.3 9.1
dieldrin
h
12.5 71.4 100.0 93.8 54.5
cis-nonachlor 75.0 100.0 100.0 62.5 36.4
p,p⬘-DDD 50.0 100.0 100.0 93.8 100.0
p,p⬘-DDT 37.5 28.6 71.4 37.5 72.7
mirex
i
0.0 28.6 42.9 25.0 63.6
a
Nominal detection limits were 0.01 g/g wet weight.
b
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c
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indene.
d
dichlorodiphenyl-1,1,1-trichloroethane.
e
dichlorodiphenyl-dichloro-ethane.
f
hexachlorobenzene.
g
3,4,5,6,9,9,-hexachloro-1a,2,2a,3,6,6a,7,7a-octahydro-2,7:3,6-
dimethanonaphth[2,3-b]oxirene.
h
1,2,3,4,10,10-hexachloro-6,7-epoxy-1,4,4a,5,6,7,8a-octahydro-endo,
exo-1,4:5,8-dimethanonaphthalene.
i
1,1a,2,2,3,3a,4,5,5,5a,5b,6-dodecachloro-octahydro-1,3,4-metheno-
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274 A. C. Matz and K. C. Parsons
