Environmental Toxicology and Chemistry, Vol. 32, No. 3, pp. 490–492, 2013
# 2013 SETAC
Printed in the USA
DOI: 10.1002/etc.2109
ET&C Impact Papers
ECOTOXICOLOGY OF ORGANOCHLORINE CHEMICALS IN BIRDS OF THE GREAT LAKES
DONALD E. TILLITT *y and JOHN P. GIESYz
yU.S. Geological Survey, Columbia Environmental Research Center, Columbia, Missouri
zDepartment of Biomedical Veterinary Sciences and Toxicology Centre, University of Saskatchewan, Saskatoon, Saskatchewan, Canada
(Submitted 20 October 2012; Returned for Revision 28 October 2012; Accepted 9 November 2012)
The legacy of Rachel Carson and her now historic book
Silent Spring [1] was fulfilled in the United States with passage
of environmental legislation such as the Clean Water Act,
the Federal Insecticide, Fungicide, and Rodenticide Act,
and the Toxic Substance Control Act in the 1970s. Carson’s
writings, television interviews, and testimony before Congress
alerted a nation and the world to the unintended effects of
persistent, bioaccumulative chemicals on populations of fish,
wildlife, and possibly humans. Her writings in the popular press
brought attention to scientific findings that declines in populations of a variety of birds were directly linked to the widespread
use of dichlorodiphenyltrichloroethane (DDT) in agriculture,
public health, and horticulture. By the 1970s, DDT and other
persistent organic pollutants (POPs) were being banned or
phased out, and the intent of these regulatory acts became
apparent in a number of locations across the United States,
including the Great Lakes. Concentrations of DDT and its
major product of transformation, dichlorodiphenylchloroethane
(DDE), were decreasing in top predators, such as bald eagles
(Haliaeetus leucocephalus), osprey (Pandion haliaetus), colonial waterbirds, and other fish-eating wildlife [2]. Eggshell
thinning and the associated mortality of bird embryos caused
by DDE had decreased in the Great Lakes and elsewhere by the
early 1980s [3].
Nevertheless, populations of certain species of birds in the
Great Lakes were not recovering as quickly as expected.
Hatching rates increased in a number of bird species; yet,
fledging rates in certain populations remained low, and deformities of the bills, feet, head, and eyes were observed at elevated
rates compared with populations from areas not associated with
the Great Lakes or from more remote areas. Collectively, the
deformities observed in a variety of fish-eating species of birds
were described as Great Lakes embryo mortality and edema
disease syndrome (GLEMEDS) [4]. The Canadian Wildlife
Service initiated a herring gull (Larus argentatus) monitoring
program in 1973 [2], partially to monitor the status and trends of
concentrations or persistent residues in eggs but also to monitor
biological outcomes in the birds. Meanwhile, in the United
States, the U.S. Fish and Wildlife Service was also observing
deformities in colonial waterbirds in certain populations they
monitored, particularly in Green Bay (Lake Michigan) and
Saginaw Bay (Lake Huron) (e.g., Kubiak et al. [5]). Additionally, a family of avid birders routinely visited several islands to
observe and enumerate the breeding of colonial waterbirds [6].
In all cases, these monitoring efforts demonstrated that populations of most species of birds increased in the 1980s to the
1990s; but in certain locations, and particularly among colonial
waterbirds, GLEMEDS continued to be observed.
The causal agent(s) for the embryo deformities in select
populations of Great Lakes birds had not been confirmed, but
the toxicity of polychlorinated biphenyls (PCBs), chlorinated
dioxins, and chlorinated furans, collectively known as dioxinlike compounds (DLCs), had been hypothesized. Discovery of
the aryl hydrocarbon receptor (AhR) and then characterization
of responses of several classes of chemicals that activate the
AhR signal-transduction pathway in vertebrates revealed two
important facts about agonists of this receptor [7]. First, similar
signs of wasting syndrome (reduced weight gain), activation
of hepatic oxidative enzymes (e.g., cytochrome P4501A
[CYP1A]), immune suppression, and developmental anomalies
(cardiovascular defects, cranial and pericardial edema, hemorrhage) were consistently observed in mammals, birds, and fish
when exposed to DLCs [8]. Although sensitivity among species
varies, similar AhR-mediated effects were observed following
exposure to DLCs. Second, the potency of different AhR
agonists to induce signs of dioxin-like toxicity followed quantitative structure–activity relationships among the different
toxicological responses, leading to the development of relative
toxic potency factors for DLC congeners compared to the
standard, 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) [8].
The potency of individual dioxin-like congeners to induce
CYP1A activity through a ligand-activated pathway and transcriptional activation of the ‘‘AhR gene battery’’ was proportionally related to the potency of that same congener to cause
other pathological signs such as reduced weight gain or immune
suppression [9].
These findings led to better tools for evaluating both the
toxicity of DLCs and vertebrate exposure to DLCs. For example, the ability of DLCs to induce CYP1A activity in vitro could
be used to evaluate the sensitivity of a particular species or
to assess the toxic potency of a mixture of DLCs. Complex
mixtures of DLCs could be tested and evaluated for overall
toxic potency to elicit AhR-related effects using cell bioassays
and responses such as ethoxyresorufin O-deethylase induction
[10]. Advances in understanding the molecular signaling pathways of DLCs were critical events that allowed development of
exposure-assessment tools. The subsequent marriage of these
new technologies for exposure and toxicity assessment of DLCs
together with intensive on-site monitoring of waterbird colonies
All Supplemental Data may be found in the online version of this article.
See Table S1 for the number of citations and rank of all the ‘‘Top 100’’
papers, which in this essay are references [13,16].
* To whom correspondence may be addressed
(dtillitt@usgs.gov).
Published online in Wiley Online Library
(wileyonlinelibrary.com).
490
Environ. Toxicol. Chem. 32, 2013
in the Great Lakes proved to be critical in the determination of
causal linkages between GLEMEDS observed in populations of
Great Lakes fish-eating birds and DLCs.
Colonial waterbirds exhibited classic signs of DLC-related
toxicity—including teratogenicity, decreased fledging rates,
altered biochemical metabolism, and reproductive problems—
in populations nesting near industrial areas of the Great Lakes,
such as Saginaw Bay (Lake Huron), Green Bay (Lake Michigan), Maumee Bay (Lake Erie), and Hamilton Harbor (Lake
Ontario) [2,4,5]. Initial monitoring by the Canadian Wildlife
Service focused on the herring gull, with status and trends
evaluated through the measurement of contaminant concentrations in eggs collected annually from 13 designated colonies [2].
In an effort to properly interpret these measurements, develop
biomagnification factors, and better understand ecosystem
chemical dynamics, the Canadian Wildlife Service created a
toxicokinetic model for the intercompartmental movement of a
series of POPs in herring gulls [11,12]. This model turned out to
be important for the evaluation of colonial waterbirds in the
Great Lakes and ultimately other locations around the world
where fish-eating birds were contaminated with organochlorine
chemicals. Indeed, the publication by Braune and Norstrom [13]
was one of the most cited papers in Environmental Toxicology
and Chemistry [14] and has been used in numerous modeling
efforts to evaluate the exposure of birds to organochlorine
chemicals.
The identification of individual compounds and a more
complete understanding of their distribution in fish-eating birds
was a critical step in testing the hypothesis that DLCs were
causing the deformities, edema, wasting syndrome, and reproductive problems observed in certain breeding colonies of Great
Lakes waterbirds. However, a single compound or class of
compounds had not been identified and linked with these
emerging effects, collectively referred to as GLEMEDS [4].
In laboratory exposure, PCBs were known to cause GLEMEDS
in birds. At about the same time, polychlorinated dibenzo-pdioxins (PCDDs) and polychlorinated dibenzofurans (PCDFs)
had been identified as the agents responsible for chick edema
disease [15].
The hundreds of PCB, PCDD, and PCDF congeners, all
with different potencies, were found to have varying profiles
(i.e., relative proportions among congeners), based on different
sources and distribution patterns. Consequently, the toxicity of
these complex mixtures could not be rapidly assessed. Also,
there was only limited information on the actual environmental
concentrations of these DLCs in fish and wildlife due to the
challenges of analyzing very low concentrations (picograms to
nanograms per gram range). Chemical methods for DLCs were
experimental, available only in limited laboratories, and costly.
This led to the need for an analytical method to quantify low
concentrations of DLCs and evaluate the potency of those
mixtures in environmental samples, including fish and wildlife
[10].
The advances in knowledge regarding the mechanistic
aspects of the AhR, signal-transduction pathways, specific gene
responses, and quantitative structure–activity relationships
among end points provided the opportunity for the development
of bioassay approaches to measure DLCs. In particular, the
H4IIE rat hepatoma cell line was found to contain an intact AhR
pathway with inducible CYP1A activity, measured as ethoxyresorufin O-deethylase [10]. The H4IIE bioassay proved to be
a useful screening tool for integrating the cumulative potencies
of DLC mixtures in environmental samples, and it cost much
less than chemical analysis [16]. This bioassay represented a
491
means of rapid assessment that led to the ability to quantify
complex mixtures of DLCs, particularly in eggs of fish-eating
waterbirds. Dose–response relationships between bioassayderived potencies of DLCs in eggs of colonial waterbirds
and signs of GLEMEDS in distinct populations of Caspian
terns (Hydroprogne caspia), double-crested cormorants (Phalacrocorax auritus), Forster’s terns (Sterna forsteri), and herring gulls provided strong evidence that DLCs were causing
GLEMEDS in a variety of nesting bird populations in the lower
Great Lakes [16–20]. This piece of evidence proved to be
critical for the determination of causality [4]. Moreover, the
use of bioassay systems, like the H4IIE bioassay, for measurement of DLCs and their potencies in environmental samples
grew after this period and became an extremely useful approach
for environmental assessments [21]. The linkages of GLEMEDS in colonial waterbirds to DLCs also served as an
important conceptual model for assessment of these chemical
mixtures in other locations around the world.
Today, advances in molecular biology have allowed
sequencing of the AhR and discovery of the basis for sensitivity
differences toward DLCs in birds. It has been known for some
time that the sensitivity of birds to embryotoxic effects of AhR
agonists varies among species [8]. The most sensitive avian
species to DLC-related effects has consistently been the domestic
chicken (Gallus gallus domesticus), while other species have
sensitivities toward DLCs that are hundreds (Japanese quail,
Coturnix japonica) to thousands (double-crested cormorant or
herring gull) of times less than that observed in chickens. The
reason for the differential sensitivity among avian species was
unknown until recently, when it was discovered that amino acid
sequences in the ligand binding domain of AhR1 portend the
relative sensitivity of a species to DLC-induced embryotoxicity
[22]. Subsequent studies have reaffirmed the importance of two
amino acids in AhR1 and demonstrated that the prototypical
DLC, TCDD, is not always the most potent congener for
eliciting dioxin-related toxicity in birds [23]. Indeed, there
appear to be three distinct categories of avian sensitivity based
on the amino acid substitution patterns at these two residues
sites (residues 324 and 380) in the binding domain of AhR1
[24].
The ability to predict species’ relative sensitivities based on
the sequence of AhR1 is an important tool for evaluating risk
from these chemicals, particularly for threatened and endangered species of birds in which toxicological testing is largely
impractical. The new understanding of the relative potencies of
various DLCs compared to TCDD will also be important for
risk assessments and understanding the relative importance of
different classes of DLCs. As DLCs continue to elicit responses
in select avian populations of the Great Lakes, better toxicological evaluations of risk or recovery will allow better natural
resource management actions.
SUPPLEMENTAL DATA
Table S1 (49 KB PDF).
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G.T. Ankley and J.W. Gorsuch
Table 1. Ranking by citation frequency of the top 100 (102) papers published in Environmental Toxicology and Chemistry
Rank
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21 (A)
21 (B)
23
24
Publication
year
Volume
Jobling S, Sheahan D, Osborne JA,
Matthiessen P, Sumpter JP
1996
15
194–202
818
Routledge EJ, Sumpter JP
1996
15
241–248
752
Di Toro DM, Zarba CS, Hansen DJ, Berry
WJ, Swartz RC, Cowan CE, Pavlou SP,
Allen HE, Thomas NA, Paquin PR
Solomon KR, Baker DB, Richards RP, Dixon
DR, Klaine SJ, LaPoint TW, Kendall RJ,
Weisskopf CP, Giddings JM, Giesy JP,
Hall LW, Williams WM
Di Toro DM, Allen HE, Bergman HL, Meyer
JS, Paquin PR, Santore RC
Di Toro DM, Mahony JD, Hansen DJ, Scott
KJ, Hicks MB, Mayr SM, Redmond MS
Harries JE, Sheahan DA, Jobling S,
Matthiessen P, Neall M, Sumpter JP,
Taylor T, Zaman N
Matthiessen P, Gibbs PE
1991
10
1541–1583
727
1996
15
31–74
461
2001
20
2383–2396
423
1990
9
1487–1502
392
1997
16
534–542
390
1998
17
37–43
321
Gustafson DI
1989
8
339–357
304
Russom CL, Bradbury SP, Broderius SJ,
Hammermeister DE, Drummond RA
1997
16
948–967
290
Debruijn J, Busser F, Seinen W,
Hermens J
1989
8
499–512
282
Lange R, Hutchinson TH, Croudace CP,
Siegmund F, Schweinfurth H, Hampe P,
Panter GH, Sumpter JP
Harries JE, Sheahan DA, Jobling S,
Matthiessen P, Neall P, Routledge EJ,
Rycroft R, Sumpter JP, Tylor T
Chung KT, Stevens SE
2001
20
1216–1227
281
1996
15
1993–2002
264
1993
12
2121–2132
261
Metcalfe CD, Metcalfe TL, Kiparissis Y,
Koenig BG, Khan C, Hughes RJ,
Croley TR, March RE, Potter T
2001
20
297–308
259
Digiulio RT, Washburn PC, Wenning RJ,
Winston GW, Jewell CS
Karickhoff SW, Morris KR
1989
8
1103–1123
252
1985
4
469–479
251
Title
Inhibition of testicular growth in rainbow trout
(Oncorhynchus mykiss) exposed to estrogenic
alkylphenolic chemicals
Estrogenic activity of surfactants and some of
their degradation products assessed using a
recombinant yeast screen
Technical basis for establishing sediment quality
criteria for nonionic organic-chemicals using
equilibrium partitioning
Ecological risk assessment of atrazine in North
American surface waters
Biotic ligand model of the acute toxicity of
metals. 1. Technical basis
Toxicity of cadmium in sediments: The role of
acid volatile sulfide
Estrogenic activity in five United Kingdom
rivers detected by measurement of
vitellogenesis in caged male trout
Critical appraisal of the evidence for
tributyltin-mediated endocrine disruption
in mollusks
Groundwater ubiquity score: A simple method
for assessing pesticide leachability
Predicting modes of toxic action from chemical
structure: Acute toxicity in the fathead
minnow (Pimephales promelas)
Determination of octanol water partition-coefficients
for hydrophobic organic-chemicals with the
slow-stirring method
Effects of the synthetic estrogen 17
alpha-ethinylestradiol on the life-cycle of
the fathead minnow (Pimephales promelas)
A survey of estrogenic activity in
United Kingdom inland waters
Degradation of azo dyes by environmental
microorganisms and helminths
Estrogenic potency of chemicals detected in
sewage treatment plant effluents as determined
by in vivo assays with Japanese medaka
(Oryzias latipes)
Biochemical responses in aquatic animals:
A review of determinants of oxidative stress
Sorption dynamics of hydrophobic pollutants in
sediment suspensions
Nanomaterials in the environment: Behavior,
fate, bioavailability, and effects
Induction of testis-ova in Japanese medaka
(Oryzias latipes) exposed to p-nonylphenol
Analysis of acid-volatile sulfide (AVS) and
simultaneously extracted metals (SEM) for
the estimation of potential toxicity in aquatic
sediments
Predicting toxicity in marine sediments with
numerical sediment quality guidelines
Principal response curves: Analysis of
time-dependent multivariate responses of
biological community to stress
Overview of a workshop on screening methods
for detecting potential (anti-) estrogenic/
androgenic chemicals in wildlife
Environmental factors affecting the formation
of methylmercury in low pH lakes
Authors
Pages
Total
citations
Klaine SJ, Alvarez PJJ, Batley GE, Fernandes
TF, Handy RD, Lyon DY, Mahendra S,
McLaughlin MJ, Lead JR
Gray MA, Metcalfe CD
2008
27
1825–1851
249
1997
16
1082–1086
248
Allen HE, Fu GM, Deng BL
1993
12
1441–1453
246
Long ER, Field LJ, MacDonald DD
1998
17
714–727
236
Van den Brink PJ, Ter Braak CJF
1999
18
138–148
236
Ankley G, Mihaich E, Stahl R, Tillitt D,
Colborn T, McMaster S, Miller R, Bantle J,
Campbell P, Denslow N, Dickerson R,
Folmar L, Fry M, Giesy J, Gray LE,
Guiney P, Hutchinson T, Kennedy S,
Kramer V, LeBlanc G, Mayes M, Nimrod
A, Patino R, Peterson R, Purdy R, Ringer
R, Thomas P, Touart L, Van der Kraak G,
Zacharewski T
Winfrey MR, Rudd JWM
1998
17
68–87
225
1990
9
853–869
221
Analyzing the Impact of Papers Published in . . .
Environ. Toxicol. Chem. 32, 2013
3
Table 1. (Continued )
Rank
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42 (A)
42 (B)
44
45
46
47
48
49
Publication
year
Volume
Pages
Total
citations
Santore RC, Di Toro DM, Paquin PR,
Allen HE, Meyer JS
2001
20
2397–2402
218
Sellstrom U, Kierkegaard A, de Wit C,
Jansson B
1998
17
1065–1072
215
Martin JW, Mabury SA, Solomon KR,
Muir DCG
2003
22
196–204
212
Wang WX, Fisher NS
1999
18
2034–2045
208
Wolfe MF, Schwarzbach S, Sulaiman RA
1998
17
146–160
207
Grieb TM, Driscoll CT, Gloss SP,
Schofield CL, Bowie GL, Porcella DB
Fulton MH, Key PB
1990
9
919–930
203
2001
20
37–45
198
Ankley GT, DiToro DM, Hansen DJ,
Berry WJ
Erickson RJ, Benoit DA, Mattson VR,
Nelson HP, Leonard EN
Metcalfe CD, Miao XS, Koenig BG,
Struger J
1996
15
2056–2066
197
1996
15
181–193
193
2003
22
2881–2889
192
Fisk AT, Norstrom RJ, Cymbalisty CD,
Muir DCG
1998
17
951–961
191
Allen Y, Scott AP, Matthiessen P,
Haworth S, Thain JE, Feist S
1999
18
1791–1800
189
Thomann RV, Connolly JP, Parkerton TF
1992
11
615–629
188
Baumard P, Budzinski H, Garrigues P
1998
17
765–776
186
Burton GA
Ankley GT, Jensen KM, Kahl MD,
Korte JJ, Makynen EA
1991
2001
10
20
1585–1627
1276–1290
185
184
Lovern SB, Klaper R
2006
25
1132–1137
183
Landrum PF, Lee H, Lydy MJ
1992
11
1709–1725
181
Huang CH, Sedlak DL
2001
20
133–139
181
Munkittrick KR, Vanderkraak GJ,
McMaster ME, Portt CB,
Vandenheuvel MR, Servos MR
1994
13
1089–1101
180
Cornelissen G, vanNoort PCM,
Govers HAJ
1997
16
1351–1357
179
Forbes VE, Calow P
1999
18
1544–1556
178
Ratte HT
1999
18
89–108
176
Williams PL, Dusenbery DB
1990
9
1285–1290
173
Braune BM, Norstrom RJ
1989
8
957–968
167
Title
Biotic ligand model of the acute toxicity of
metals. 2. Application to acute copper
toxicity in freshwater fish and Daphnia
Polybrominated diphenyl ethers and
hexabromocyclododecane in sediment
and fish from a Swedish river
Bioconcentration and tissue distribution of
perfluorinated acids in rainbow trout
(Oncorhynchus mykiss)
Assimilation efficiencies of chemical contaminants
in aquatic invertebrates: A synthesis
Effects of mercury on wildlife: A comprehensive
review
Factors affecting mercury accumulation in fish
in the upper Michigan peninsula
Acetylcholinesterase inhibition in estuarine
fish and invertebrates as an indicator of
organophosphorus insecticide exposure
and effects
Technical basis and proposal for deriving sediment
quality criteria for metals
The effects of water chemistry on the toxicity of
copper to fathead minnows
Distribution of acidic and neutral drugs in surface
waters near sewage treatment plants in the lower
Great Lakes, Canada
Dietary accumulation and depuration of
hydrophobic organochlorines: Bioaccumulation
parameters and their relationship with the
octanol/water partition coefficient
Survey of estrogenic activity in United Kingdom
estuarine and coastal waters and its effects on
gonadal development of the flounder Platichthys
flesus
An equilibrium model of organic-chemical
accumulation in aquatic food webs with
sediment interaction
Polycyclic aromatic hydrocarbons in sediments
and mussels of the western Mediterranean sea
Assessing the toxicity of freshwater sediments
Description and evaluation of a short-term
reproduction test with the fathead minnow
(Pimephales promelas)
Daphnia magna mortality when exposed to
titanium dioxide and fullerene (C-60)
nanoparticles
Toxicokinetics in aquatic systems: Model
comparisons and use in hazard assessment
Analysis of estrogenic hormones in municipal
wastewater effluent and surface water using
enzyme-linked immunosorbent assay and gas
chromatography/tandem mass spectrometry
Survey of receiving-water environmental impacts
associated with discharges from pulp-mills: 2.
Gonad size, liver size, hepatic erod activity and
plasma sex steroid levels in white sucker
Desorption kinetics of chlorobenzenes, polycyclic
aromatic hydrocarbons, and polychlorinated
biphenyls: Sediment extraction with Tenax1
and effects of contact time and solute
hydrophobicity
Is the per capita rate of increase a good measure
of population-level effects in ecotoxicology?
Bioaccumulation and toxicity of silver
compounds: A review
Aquatic toxicity testing using the nematode,
Caenorhabditis elegans
Dynamics of organochlorine compounds in
herring gulls: 3. Tissue distribution and
bioaccumulation in Lake Ontario gulls
Authors
(Continued)
4
Environ. Toxicol. Chem. 32, 2013
G.T. Ankley and J.W. Gorsuch
Table 1. (Continued )
Rank
50
Polychlorinated biphenyl residues and egg
mortality in double-crested cormorants
from the Great Lakes
51 (A)
Slowly reversible sorption of aliphatic halocarbons
in soils. 1. Formation of residual fractions
The potential for estradiol and ethinylestradiol
degradation in English rivers
Predictive models for photoinduced acute toxicity
of polycyclic aromatic-hydrocarbons to
Daphnia magna, Strauss (cladocera, crustacea)
Predicting the bioavailability of organic
xenobiotics to Pontoporeia hoyi in the
presence of humic and fulvic materials and
natural dissolved organic matter
An in vivo testing system for endocrine disruptors
in fish early life stages using induction of
vitellogenin
Chlorinated and brominated persistent organic
compounds in biological samples from the
environment
51 (B)
53
54 (A)
54 (B)
56 (A)
56 (B)
58
59
60
61 (A)
61 (B)
63
64
65
66 (A)
66 (B)
66 (C)
66 (D)
70
71 (A)
71 (B)
71 (C)
74
75
76
Publication
year
Volume
Pages
Total
citations
1992
11
1281–1288
160
1990
9
1107–1115
158
2002
21
480–488
158
1987
6
445–461
156
Landrum PF, Reinhold MD, Nihart SR,
Eadie BJ
1985
4
459–467
155
Tyler CR, van Aerle R, Hutchinson TH,
Maddix S, Trip H
1999
18
337–347
155
Jansson B, Andersson R, Asplund L, Litzen
K, Nylund K, Sellstrom U, Uvemo UB,
Wahlberg C, Wideqvist U, Odsjo T,
Olsson M
Altenburger R, Backhaus T, Boedeker W,
Faust M, Scholze M, Grimme LH
1993
12
1163–1174
153
2000
19
2341–2347
153
Brown JF, Wagner RE, Feng H, Bedard DL,
Brennan MJ, Carnahan JC, May RJ
Stein JE, Collier TK, Reichert WL, Casillas
E, Hom T, Varanasi U
1987
6
579–593
152
1992
11
701–714
151
Arcand-Hoy LD, Benson WH
1998
17
49–57
149
Mount DI, Norberg TJ
Hahn ME, Woodward BL, Stegeman JJ,
Kennedy SW
1984
1996
3
15
425–434
582–591
147
147
Swackhamer DL, Skoglund RS
1993
12
831–838
146
Sparling DW, Fellers GM, McConnell LL
2001
20
1591–1595
144
Suter GW
1993
12
1533–1539
143
Munkittrick KR, Vanderkraak GJ,
McMaster ME, Portt CB
1992
11
1427–1439
142
Meylan WM, Howard PH, Boethling RS,
Aronson D, Printup H, Gouchie S
1999
18
664–672
142
Chapman PM, Wang FY
Metcalfe CD, Koenig BG, Bennie DT,
Servos M, Ternes TA, Hirsch R
Squillace PJ, Pankow JF, Korte NE,
Zogorski JS
Booij K, Sleiderink HM, Smedes F
2001
2003
20
22
3–22
2872–2880
142
142
1997
16
1836–1844
141
1998
17
1236–1245
140
Orvos DR, Versteeg DJ, Inauen J,
Capdevielle M, Rothenstein A,
Cunningham V
Martin JW, Mabury SA, Solomon KR,
Muir DCG
McCarthy JF, Jimenez BD
2002
21
1338–1349
140
2003
22
189–195
140
1985
4
511–521
138
2002
21
1323–1329
137
1987
6
11–20
135
Title
Predictability of the toxicity of multiple chemical
mixtures to Vibrio fischeri: Mixtures composed
of similarly acting chemicals
Environmental dechlorination of PCBs
Bioindicators of contaminant exposure and
sublethal effects: Studies with benthic fish
in Puget Sounds, Washington
Fish reproduction: An ecologically relevant
indicator of endocrine disruption
A seven-day life-cycle cladoceran toxicity test
Rapid assessment of induced cytochrome P4501A
protein and catalytic activity in fish hepatoma
cells grown in multiwell plates: Response to
TCDD, TCDF, and two planar PCBS
Bioaccumulation of PCBs by algae: Kinetics
versus equilibrium
Pesticides and amphibian population declines in
California, USA
A critique of ecosystem health concepts and
indexes
Response of hepatic MFO activity and plasma
sex steroids to secondary treatment of bleached
kraft pulp mill effluent and mill shutdown
Improved method for estimating bioconcentration/
bioaccumulation factor from octanol/water
partition coefficient
Assessing sediment contamination in estuaries
Occurrence of neutral and acidic drugs in the
effluents of Canadian sewage treatment plants
Review of the environmental behavior and fate of
methyl tert-butyl ether
Calibrating the uptake kinetics of semipermeable
membrane devices using exposure standards
Aquatic toxicity of triclosan
Dietary accumulation of perfluorinated acids in
juvenile rainbow trout (Oncorhynchus mykiss)
Reduction in bioavailability to bluegills of
polycyclic aromatic-hydrocarbons bound to
dissolved humic material
Measurement of triclosan in wastewater treatment
systems
Reduction in bioavailability of organic
contaminants to the amphipod Pontoporeia
hoyi by dissolved organic matter of
sediment interstitial waters
Authors
Tillitt DE, Ankley GT, Giesy JP, Ludwig JP,
Kuritamatsuba H, Weseloh DV, Ross PS,
Bishop CA, Sileo L, Stromborg KL,
Larson J, Kubiak TJ
Pignatello JJ
Jurgens MD, Holthaus KIE, Johnson AC,
Smith JJL, Hetheridge M, Williams RJ
Newsted JL, Giesy JP
McAvoy DC, Schatowitz B, Jacob M,
Hauk A, Eckhoff WS
Landrum PF, Nihart SR, Eadie BJ,
Herche LR
Analyzing the Impact of Papers Published in . . .
Environ. Toxicol. Chem. 32, 2013
5
Table 1. (Continued )
Rank
77
78 (A)
78 (B)
78 (C)
81
82
83 (A)
83 (B)
85 (A)
85 (B)
87 (A)
87 (B)
87 (C)
90 (A)
90 (B)
90 (C)
93
94 (A)
94 (B)
94 (C)
94 (D)
98 (A)
98 (B)
100 (A)
100 (B)
100 (C)
Publication
year
Volume
Pages
Total
citations
Alvarez DA, Petty JD, Huckins JN,
Jones-Lepp TL, Getting DT, Goddard JP,
Manahan SE
Backhaus T, Altenburger R, Boedeker W,
Faust M, Scholze M, Grimme LH
2004
23
1640–1648
133
2000
19
2348–2356
131
Ankley GT, Jensen KM, Makynen EA,
Kahl MD, Korte JJ, Hornung MW,
Henry TR, Denny JS, Leino RL, Wilson
VS, Cardon MC, Hartig PC, Gray LE
Wania F, Dugani CB
2003
22
1350–1360
131
2003
22
1252–1261
131
Petrovic M, Sole M, de Alda MJL,
Barcelo D
2002
21
2146–2156
130
Spengler P, Korner W, Metzger JW
2001
20
2133–2141
129
Swartz RC, Schults DW, Ozretich RJ,
Lamberson JO, Cole FA, Dewitt TH,
Redmond MS, Ferraro SP
White JC, Kelsey JW, Hatzinger PB,
Alexander M
Meylan WM, Howard PH
1995
14
1977–1987
128
1997
16
2040–2045
128
1991
10
1283–1293
127
Kelsey JW, Alexander M
1997
16
582–585
127
Heinz GH, Hoffman DJ, Krynitsky AJ,
Weller DMG
Neff JM
1987
6
423–433
124
1997
16
917–927
124
Title
Authors
Development of a passive, in situ, integrative
sampler for hydrophilic organic contaminants
in aquatic environments
Predictability of the toxicity of a multiple mixture
of dissimilarly acting chemicals to Vibrio
fischeri
Effects of the androgenic growth promoter
17-b-trenbolone on fecundity and reproductive
endocrinology of the fathead minnow
Assessing the long-range transport potential of
polybrominated diphenyl ethers: A comparison
of four multimedia models
Endocrine disruptors in sewage treatment plants,
receiving river waters, and sediments:
Integration of chemical analysis and
biological effects on feral carp
Substances with estrogenic activity in effluents
of sewage treatment plants in southwestern
Germany. 1. Chemical analysis
Sigma-PAH: A model to predict the toxicity of
polynuclear aromatic hydrocarbon mixtures
in field-collected sediments
Factors affecting sequestration and bioavailability
of phenanthrene in soils
Bond contribution method for estimating Henry’s
law constants
Declining bioavailability and inappropriate
estimation of risk of persistent compounds
Reproduction in mallards fed selenium
Ecotoxicology of arsenic in the marine
environment
Acute and chronic toxicity of imidazolium-based
ionic liquids on Daphnia magna
Bioaccumulation and biotransformation of
polychlorinated dibenzo-p-dioxins and
dibenzofurans in fish
Mercury cycling and effects in freshwater
wetland ecosystems
Time-dependent isotherm shape of organic
compounds in soil organic matter:
Implications for sorption mechanism
Pesticide concentration patterns in agricultural
drainage networks in the Lake Erie basin
Swimming behavior as the indicator of
sublethal toxicity in fish
Occurrence and fate of tributyltin compounds
and triphenyltin compounds in western
Mediterranean coastal enclosures
Sensitivity of fish embryos to weathered crude oil:
Part I. Low-level exposure during incubation
causes malformations, genetic damage,
and mortality in larval Pacific herring
(Clupea pallasi)
Effect of kinetics of complexation by humic acid
on toxicity of copper to Ceriodaphnia dubia
Effects of bleached kraft mill effluent on fish in
the St. Maurice River, Quebec
Predicting the toxicity of metal-spiked laboratory
sediments using acid-volatile sulfide and
interstitial water normalizations
Biological methods for determining toxicity
of contaminated freshwater sediments to
invertebrates
Improved method for estimating water solubility
from octanol water partition coefficient
Xenobiotic and steroid biotransformation enzymes
in Atlantic salmon (Salmo salar) liver treated
with an estrogenic compound, 4-nonylphenol
Bernot RJ, Brueseke MA, Evans-White MA,
Lamberti GA
Opperhuizen A, Sijm DTHM
2005
24
87–92
124
1990
9
175–186
123
Zillioux EJ, Porcella DB, Benoit JM
1993
12
2245–2264
123
Xing BS, Pignatello JJ
1996
15
1282–1288
123
Richards RP, Baker DB
1993
12
13–26
121
Little EE, Finger SE
1990
9
13–19
119
Tolosa I, Merlini L, Debertrand N, Bayona
JM, Albaiges J
1992
11
145–155
119
Carls MG, Rice SD, Hose JE
1999
18
481–493
119
Ma HZ, Kim SD, Cha DK, Allen HE
1999
18
828–837
119
Hodson PV, McWhirter M, Ralph K, Gray B,
Thivierge D, Carey JH, Vanderkraak G,
Whittle DM, Levesque MC
Berry WJ, Hansen DJ, Mahony JD, Robson
DL, DiToro DM, Shipley BP, Rogers B,
Corbin JM, Boothman WS
Nebeker AV, Cairns MA, Gakstatter JH,
Malueg KW, Schuytema GS,
Krawczyk DF
Meylan WM, Howard PH, Boethling RS
1992
11
1635–1651
118
1996
15
2067–2079
118
1984
3
617–630
117
1996
15
100–106
117
Arukwe A, Forlin L, Goksoyr A
1997
16
2576–2583
117