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ORGANIC CHEMICAL
TOXICOLOGY OF FISHES
This is Volume 33 in the
FISH PHYSIOLOGY series
Edited by Anthony P. Farrell and Colin J. Brauner
Honorary Editors: William S. Hoar and David J. Randall
A complete list of books in this series appears at the end of the volume
ORGANIC CHEMICAL
TOXICOLOGY OF FISHES
Edited by
KEITH B. TIERNEY
Department of Biological Sciences
University of Alberta
Edmonton, Alberta
Canada
ANTHONY P. FARRELL
Department of Zoology, and
Faculty of Land and Food Systems
The University of British Columbia
Vancouver, British Columbia
Canada
COLIN J. BRAUNER
Department of Zoology
The University of British Columbia
Vancouver, British Columbia
Canada
AMSTERDAM BOSTON HEIDELBERG LONDON
NEW YORK OXFORD PARIS SAN DIEGO
SAN FRANCISCO SINGAPORE SYDNEY TOKYO
Academic Press is an imprint of Elsevier
Academic Press is an imprint of Elsevier
32 Jamestown Road, London NW1 7BY, UK
225 Wyman Street, Waltham, MA 02451, USA
525 B Street, Suite 1800, San Diego, CA 92101-4495, USA
Copyright r 2014 Elsevier Inc. All rights reserved
The cover illustrates the diversity of effects an example synthetic organic water pollutant can
have on fish. The chemical shown is 2,4-D, an herbicide that can be found in streams near
urbanization and agriculture. The fish shown is one that can live in such streams: rainbow trout
(Oncorhynchus mykiss). The effect shown on the left is the ability of 2,4-D (yellow line) to
stimulate olfactory sensory neurons vs. control (black line) (measured as an electro-
olfactogram; EOG). The effect shown on the right is the ability of 2,4-D to induce the
expression of an egg yolk precursor protein (vitellogenin) in male fish. Image credits: chemical,
Wikipedia; fish, Matthew Gilbert; EOG, Brian Blunt; well plate, Daniel Schlenk.
No part of this publication may be reproduced, stored in a retrieval system or transmitted in any
form or by any means electronic, mechanical, photocopying, recording or otherwise without the
prior written permission of the publisher
Permissions may be sought directly from Elsevier’s Science & Technology Rights
Department in Oxford, UK: phone (þ44) (0) 1865 843830; fax (þ44) (0) 1865 853333; email:
[email protected]. Alternatively, visit the Science and Technology Books website at
www.elsevierdirect.com/rights for further information
Notices
No responsibility is assumed by the publisher for any injury and/or damage to persons or
property as a matter of products liability, negligence or otherwise, or from any use or operation
of any methods, products, instructions or ideas contained in the material herein
Because of rapid advances in the medical sciences, in particular, independent verification of
diagnoses and drug dosages should be made
British Library Cataloguing-in-Publication Data
A catalogue record for this book is available from the British Library
Library of Congress Cataloging-in-Publication Data
A catalog record for this book is available from the Library of Congress
ISBN: 978-0-12-398254-4
ISSN: 1546-5098
For information on all Academic Press publications
visit our website at store.elsevier.com
Typeset by MPS Limited, Chennai, India
www.adi-mps.com
Printed and bound in United States of America
14 15 16 17 10 9 8 7 6 5 4 3 2 1
For Jeannie
CONTENTS
CONTRIBUTORS xi
ABBREVIATIONS AND ACRONYMS xv
PREFACE xxiii
1. Organic Contaminants and Fish
Keith B. Tierney, Christopher J. Kennedy, Frank Gobas,
Melissa Gledhill and Mark Sekela
1. Contaminants: A Short Historical Preamble 1
2. Contaminant Toxicokinetics in Fishes 14
3. Predicting Contaminant Movement in the Environment and Fish 34
4. Quantifying Contaminants and Exposures 40
5. Conclusion 41
2. Effects of Legacy Persistent Organic Pollutants (POPs) in
Fish—Current and Future Challenges
Lyndal L. Johnson, Bernadita F. Anulacion, Mary R. Arkoosh,
Douglas G. Burrows, Denis A. M. da Silva, Joseph P. Dietrich,
Mark S. Myers, Julann Spromberg and Gina M. Ylitalo
1. Introduction 54
2. Transformations of POPs in the Aquatic Environment 56
3. Endocrine Disruption 58
4. Effects on Early Development 77
5. Transgenerational Effects 84
6. Effects on Growth, Condition, and Energy Reserves 87
7. Effects on Reproduction 90
8. Immunotoxicity 97
9. Neoplasia and Related Pathological Conditions 102
10. Effects on Behavior, Including Foraging, Aggression, and
Predator Avoidance 105
11. Risk Assessment Challenges 108
vii
viii CONTENTS
3. Organometal(loid)s
Niladri Basu and David M. Janz
1. Introduction 142
2. Organic Mercury 144
3. Organoselenium 157
4. Organoarsenicals 170
5. Organotin Compounds 176
6. Other Organometal(loid)s 179
7. Conclusions 181
4. Effects on Fish of Polycyclic Aromatic Hydrocarbon (PAH)
and Naphthenic Acid Exposures
Tracy K. Collier, Bernadita F. Anulacion, Mary R. Arkoosh,
Joseph P. Dietrich, John P. Incardona, Lyndal L. Johnson,
Gina M. Ylitalo and Mark S. Myers
1 Introduction 196
2 Transformations of PAHs in the Aquatic Environment 198
3 Hepatic Neoplasia and Related Lesions in Wild Fish 200
4 Effects on Reproduction 211
5 Effects on Embryonic and Larval Development 215
6 Transgenerational Effects 222
7 Other Effects with Consequences for Survival of Postlarval Stages 224
8 Naphthenic Acids as a New Concern 230
9 Future Directions 234
5. Estrogenic Endocrine Disrupting Chemicals in Fish
Christopher J. Kennedy, Heather L. Osachoff and
Lesley K. Shelley
1. Introduction 257
2. EDC 260
3. Toxicokinetics 266
4. Mechanisms of Toxicity 273
5. Xenoestrogen Effects 285
6. Interactions with Other Toxic Agents 290
7. Knowledge Gaps and Future Directions 291
6. Insecticide Toxicity in Fish
M.H. Fulton, P.B. Key and M.E. DeLorenzo
1. Abstract/Introduction 310
2. Background 311
3. Insecticide Classes 312
4. Organophosphates 323
5. Carbamates 331
6. Pyrethroids 337
7. Neonicotinoids 345
CONTENTS ix
8. Phenylpyrazoles 347
9. Microbial-Based Insecticides 349
10. Insect Growth Regulators 351
11. Mixtures 353
12. Data Gaps 353
13. Summary 354
7. Effects of Herbicides on Fish
Keith R. Solomon, Kristoffer Dalhoff, David Volz and
Glen Van Der Kraak
1. Introduction 370
2. Classification of Herbicides 374
3. Acute Lethality of Herbicides to Fish 374
4. Sublethal Effects of Herbicides in Fish 387
5. Indirect Effects of Herbicides on Fish 402
6. Conclusions 403
8. Personal Care Products in the Aquatic Environment: A Case
Study on the Effects of Triclosan in Fish
Alice Hontela and Hamid R. Habibi
1. Introduction 412
2. Physical and Chemical Properties of Triclosan, and Its Use as a
Personal Care Product 413
3. Exposure in the Aquatic Environment 415
4. Kinetics and Metabolism of Triclosan 417
5. Toxicity of Triclosan 418
6. Reproductive and Developmental Effects 423
7. Effects of Triclosan on the Thyroid Axis 425
8. Interactions of Triclosan with Aryl Hydrocarbon and Ryanodine Receptors 426
9. Future Use of Triclosan and Related Environmental Issues 428
10. Conclusions and Knowledge Gaps 429
11. General Lessons Learned from the Case Study of Triclosan 431
9. Emerging Threats to Fishes: Engineered Organic Nanomaterials
Tyson J. MacCormack, Greg G. Goss and Richard D. Handy
1. Introduction 439
2. The Environmental Chemistry of Engineered Nanomaterials and
Bioavailability to Fishes 443
3. Acute Toxicity of Organic ENMs 445
4. Uptake Routes and Target Organs for Organic ENMs 445
5. Effects of Organic ENMs on the Physiological Systems of Fishes 451
6. Studies on Organic ENMs and Capping Agents 458
7. Nanocrystalline and Nanofibrillar Cellulosic Materials 463
8. Polymer-coated ENMs in the Agricultural Sector 465
9. Key Needs in Environmental Risk Assessment of Organic ENMs 466
10. Conclusions and Perspectives 469
x CONTENTS
10. Handling Fish Mixture Exposures in Risk Assessment
Dick de Zwart and Leo Posthuma
1 Introduction 482
2 Fish and Mixtures 485
3 Principles of Risk and Impact Assessment of Chemicals and Mixtures 488
4 Cumulative Risk Assessment for Mixtures of Toxicants 500
5 Evidence for Mixture Impacts in the Field 512
6 Conclusions, Overview, and Summary 519
INDEX 525
OTHER VOLUMES IN THE FISH PHYSIOLOGY SERIES 543
COLOR PLATE SECTION
CONTRIBUTORS
The numbers in parenthesis indicate the pages on which the authors
contributions begin.
BERNADITA F. ANULACION (53, 195), Environmental and Fisheries Science
Division, Northwest Fisheries Science Center, National Marine Fisheries
Service, National Oceanic and Atmospheric Administration, Seattle, WA,
USA
MARY R. ARKOOSH (53, 195), Environmental and Fisheries Science Division,
Northwest Fisheries Science Center, National Marine Fisheries Service,
National Oceanic and Atmospheric Administration, Newport, OR, USA
NILADRI BASU (141), Department of Environmental Health Sciences,
University of Michigan, Ann Arbor, MI, USA
DOUGLAS G. BURROWS (53), Environmental Conservation Division, Northwest
Fisheries Science Center, National Marine Fisheries Service, National
Oceanic and Atmospheric Administration, Seattle, WA, USA
TRACY K. COLLIER (195), Science Director, Puget Sound Partnership,
Tacoma, WA, USA
DENIS A.M. DA SILVA (53), Environmental and Fisheries Science Division,
Northwest Fisheries Science Center, National Marine Fisheries Service,
National Oceanic and Atmospheric Administration, Seattle, WA, USA
DICK DE ZWART (483), RIVM, Centre for Sustainability, Environment and
Health, The Netherlands
MARIE E. DELORENZO (309), Center for Coastal Environmental Health and
Biomolecular Research, National Ocean Service, National Oceanic and
Atmospheric Administration, Charleston, SC, USA
xi
xii CONTRIBUTORS
KRISTOFFER DALHOFF (371), Faculty of Science, University of Copenhagen,
Frederiksberg, Denmark
JOSEPH P. DIETRICH (53, 195), Environmental and Fisheries Science Division,
Northwest Fisheries Science Center, National Marine Fisheries Service,
National Oceanic and Atmospheric Administration, Newport, OR, USA
MICHAEL H. FULTON (309), Center for Coastal Environmental Health and
Biomolecular Research, National Ocean Service, National Oceanic and
Atmospheric Administration, Charleston, SC, USA
MELISSA GLEDHILL (1), Environment Canada, Pacific and Yukon Water
Quality Monitoring, Vancouver, BC, Canada
FRANK GOBAS (1), Faculty of Environment, School of Resource & Environ-
mental Management, Simon Fraser University, Burnaby, BC, Canada
GREG G. GOSS (441), Department of Biological Sciences and School of Public
Health, Office of Environmental Nanosafety, University of Alberta, BC,
Canada
HAMID R. HABIBI (413), Department of Biology, University of Calgary,
Calgary, AB, Canada
RICHARD D. HANDY (441), Ecotoxicology Research and Innovation Centre,
School of Biomedical and Biological Sciences, University of Plymouth,
Plymouth, UK
ALICE HONTELA (413), Department of Biological Sciences, Alberta Water and
Environmental Science Bldg., University of Lethbridge, Lethbridge, AB,
Canada
JOHN P. INCARDONA (195), Environmental and Fisheries Science Division,
Northwest Fisheries Science Center, National Marine Fisheries Service,
National Oceanic and Atmospheric Administration, Seattle, WA, USA
DAVID M. JANZ (141), Department of Veterinary Biomedical Sciences,
University of Saskatchewan, Saskatoon, SK, Canada
LYNDAL L. JOHNSON (53, 195), Environmental and Fisheries Science Division,
Northwest Fisheries Science Center, National Marine Fisheries Service,
National Oceanic and Atmospheric Administration, Seattle, WA, USA
CHRISTOPHER J. KENNEDY (1, 257), Department of Biological Sciences, Simon
Fraser University, Burnaby, BC, Canada
PETER B. KEY (309), Center for Coastal Environmental Health and
Biomolecular Research, National Ocean Service, National Oceanic and
Atmospheric Administration, Charleston, SC, USA
CONTRIBUTORS xiii
TYSON J. MACCORMACK (441), Department of Chemistry and Biochemistry,
Mount Allison University, Sackville, NB, Canada
MARK S. MYERS (53, 195), Environmental and Fisheries Science Division,
Northwest Fisheries Science Center, National Marine Fisheries Service,
National Oceanic and Atmospheric Administration, Seattle, WA, USA
HEATHER L. OSACHOFF (257), Department of Biological Sciences, Simon
Fraser University, Burnaby, BC, Canada
LEO POSTHUMA (483), RIVM, Centre for Sustainability, Environment and
Health, The Netherlands
MARK SEKELA (1), Environment Canada, Pacific and Yukon Water Quality
Monitoring, Vancouver, BC, Canada
LESLEY K. SHELLEY (257), Department of Biological Sciences, Simon Fraser
University, Burnaby, BC, Canada
KEITH R. SOLOMON (371), Centre for Toxicology, School of Environmental
Sciences, University of Guelph, Guelph, ON, Canada
JULANN SPROMBERG (53), Environmental and Fisheries Science Division,
Northwest Fisheries Science Center, National Marine Fisheries Service,
National Oceanic and Atmospheric Administration, Seattle, WA, USA
KEITH B. TIERNEY (1), University of Alberta, Department of Biological
Sciences, Edmonton, AB, Canada
GLEN VAN DER KRAAK (371), Department of Integrative Biology, University
of Guelph, Guelph, ON Canada
DAVID VOLZ (371), Department of Environmental Health Sciences, Arnold
School of Public Health, University of South Carolina, Columbia, SC,
USA
GINA M. YLITALO (53, 195), Environmental and Fisheries Science Division,
Northwest Fisheries Science Center, National Marine Fisheries Service,
National Oceanic and Atmospheric Administration, Seattle, WA, USA
ABBREVIATIONS AND ACRONYMS
Abbreviations used throughout this volume are listed below. Standard
abbreviations are not defined in the text. Nonstandard abbreviations are
defined in each chapter and listed below for reference purposes.
11-KT 11-ketotestosterone
2,3,7,8 TCDD 2,3,7,8-tetrachlorodibenzo-p-dioxin
2,4,5-T 2,4,5-trichlorophenoxyacetic acid
2,4-D 2,4-dichlorophenoxyacetic acid
ABC ATP binding cassette
AChE acetylcholinesterase
ACTH adrenocorticotropic hormone
ADME absorption, distribution, metabolism (biotransforma-
tion), and excretion
Ag silver
Ag-ENM-C citrate-capped silver engineered nanomaterials
Ag-ENM-PVP polyvinylpyrrilodone-capped silver engineered nanoma-
terials
AhR aryl hydrocarbon receptor
AhRE aryl hydrocarbon responsive element (interchangeable
with xenobiotic responsive element; XRE)
AHTN 6-acetyl-1,1,2,4,4,7 hexamethyltetraline
ANSCO Alaska north slope crude oil
AOP adverse outcome pathway
AP-1 activator protein-1
APEs alkylphenol ethoxylates
AR androgen receptor
ARE antioxidant response element (interchangeable with elec-
trophile response element, EpRE)
xv
xvi ABBREVIATIONS AND ACRONYMS
ARNT aryl hydrocarbon receptor nuclear translocator
BAF bioaccumulation factor
BaP benzo[a]pyrene
BCF bioconcentration factor
BCRP breast cancer resistance protein
BMF biomagnification factor
BNF b-naphthoflavone
BPA bisphenol A
BSA bovine serum albumin
BSAF biota to sediment accumulation factor
C60 buckyball, carbon fullerene
CA concentration addition
cAMP cyclic adenosine monophosphate
CAR constitutive androstane receptor
CBG corticosteroid-binding globulin
CCAAT cytidine-cytidine-adenosine-adenosine-thymidine
CEBPs CCAAT/enhancer-binding proteins
CH chlorinated hydrocarbon
CNT carbon nanotube
CRH corticotropin releasing hormone
Cu copper
CYP cytochrome P-450
CYP19A1 an isoform of aromatase, predominantly in the ovary
CYP19A2 an isoform of aromatase, predominantly in the brain
CYP1A cytochrome P4501A
DCDD dichlorodibenzo-p-dioxin
DDD dichlorodiphenyldichloroethane
DDE 1,1-dichloro-2,2-bis(p-dichlorodiphenyl)ethylene
DDT 1,1,1-trichloro-2,2-di(4-chlorophenyl)ethane, or dichloro-
diphenyltrichloroethane
DEHP di(2-ethylhexyl) phthalate
DES diethylstilbesterol
DHAA dehydroabietic acid
DMBA 7,12-dimethylbenz[a]anthracene
DNA deoxyribonucleic acid
Dpf days post-fertilization
DWH deepwater horizon
E1 estrone
E2 17b-estradiol
E3 estriol
EAC endocrine active chemical
ABBREVIATIONS AND ACRONYMS xvii
EC50 effective concentration that causes a 50% change in a
response
EDC endocrine disrupting compound
EE2 17a-ethinylestradiol
EER expected ecological risk (calculated with the ETX 2.0-
software)
ENMs engineered nanomaterials
EPA USA Environmental Protection Agency
EPC effect-and-probable cause (pie diagrams)
EpRE electrophile response element (interchangeable with anti-
oxidant response element, ARE)
ER endoplasmic reticulum or estrogen receptor
EREs estrogen-responsive elements
EROD ethoxyresorufin-O-deethylase
ERR estrogen-related receptor
ERRE ERR-response element
EU European Union
F1 the first filial generation comprised of offspring(s)
resulting from a cross between strains of distinct
genotypes
FA fatty acid
FACs fluorescent aromatic compounds
FCA foci of cellular alteration
FCA/AHF foci of cellular alteration or altered hepatocellular foci
FSH follicle-stimulating hormone
FXR farnesoid X receptor
GC/MS gas chromatography/mass spectrometry
GFR glomerular filtration rate
GH growth hormone
GHR growth hormone receptor
GnRH gonadotropin-releasing hormone
GPER G-protein linked estrogen receptor
GSH glutathione (tripeptide; gamma-glutamyl-cysteinyl-gly-
cine)
GSI gonadosomatic index or gonadal somatic index ([gonad
mass/body mass] 100%)
GST glutathione-S-transferase
GTH gonadotropic hormone
HAHs higher molecular weight polycyclic aromatic hydrocar-
bons
HC hydrocarbon
xviii ABBREVIATIONS AND ACRONYMS
HC5 hazardous concentration for 5% of the test species
HC5-NOEC an HC5 exactly defined by using no observed effect
concentrations in the SSD model used to derive it
HCB hexachlorobenzene
HHCB 1,3,4,6,7,8-hexahydro-4,6,6,7,8,8-hexamethylcyclopenta
(g)-2-benzopyran (aka galaxolide)
HI hazard index (interchangeable with RCR or HQ)
HNF4A hepatocyte nuclear factor 4 alpha
HP/MH hepatomegaly/megalocytic hepatosis
HPA axis hypothalamic-pituitary-adrenal axis
Hpf hours post-fertilization
HPG hypothalamus-pituitary-gonad
HPLC high-performance liquid chromatography
HPT hypothalamic-pituitary-thyroid
HQ hazard quotient (interchangeable with RCR or HI)
HIS hepatosomatic index ([liver mass/body mass] 100%)
HydVac hydropic vacuolation of biliary epithelial cells and
hepatocytes
IC50 inhibitory concentration that inhibits 50% of the response
ICP-OES inductively coupled plasma emission spectrophotometry
IGF insulin-like growth factor
kDa kilodaltons
KOA octanol-air partition coefficient
KOC octanol-carbon partition coefficient
KOW octanol-water partitioning coefficient
LAHs lower molecular weight polycyclic aromatic hydrocarbons
LC50 lethal concentration that causes death of 50% of the
population
LD50 lethal dose that causes death of 50% of the population
LH luteinizing hormone
LXR liver X receptor
MDR multidrug resistance
mER membrane estrogen receptor
MFO mixed function oxidase
mg l 1 milligrams per liter
MoA mode of action
mRNA messenger ribonucleic acid
MRP multidrug resistance protein
MRP1 multidrug resistance-associated protein
msPAF multisubstance potentially affected fraction
MTCS methyltriclosan
MWCNT multi-walled carbon nanotubes
ABBREVIATIONS AND ACRONYMS xix
MXR multixenobiotic resistance
NA naphthenic acids
NCC nanocrystalline cellulose
NCOA3 nuclear receptor coactivator 3
NFC nanofibrillar cellulose
NF-kB nuclear factor kappa B
ng l 1 nanograms per liter
NOAA national oceanic and atmospheric administration
NOAEL no observable adverse effect level
NOEC no observed effect concentration
NP nonylphenol
NP/MH nuclear pleomorphism/hepatocellular megalocytosis
NPE nonylphenol ethoxylate
NSAID non-steroidal anti-inflammatory drug
OC organochlorine
OECD organization for economic cooperation and development
OH-PBDEs hydroxylated PBDEs
OP organophosphate
PAA polyacrylic acid
PAF potentially affected fraction of species
PAH polycyclic aromatic hydrocarbon
PAMP pathogen-associated molecular patterns
PAPS 3u-phosphoadenosine-5u-phosphosulfate
PBDEs polybrominated diphenyl ethers
PCB polychlorinated biphenyl
PCDDs polychlorinated dibenzodioxins
PCDFs pentachlorodibenzo-p-furans
PEC predicted environmental concentration
PeCDF 2,3,4,7,8-pentachlorodibenzo-p-furan
PERA probabilistic ecological risk assessment
PFC plaque-forming cell
P-gp permeability glycoprotein
Phase I biotransformation reactions—functionalization reactions,
e.g. oxidation and reduction reactions
Phase II biotransformation reactions—conjugation (synthetic)
reactions
Phase III membrane efflux transporters
PHH polyhalogenated hydrocarbon
PME pulp mill effluent
PNEC predicted no effect concentration
POP persistent organic pollutant
PPAR peroxisome proliferator activated receptors
xx ABBREVIATIONS AND ACRONYMS
PPCP pharmaceutical and personal care product
PRP pattern recognition proteins
PRR pattern recognition receptors
PSAMP Puget Sound assessment and monitoring program
PVP polyvinylpyrrolidone
PXR pregnane X receptor
Pzp pregnancy zone protein
RA retinoic acid
RAR retinoic acid receptor
RCR risk characterization ratio or risk quotient (interchange-
able with HI and HQ)
REACH registration, evaluation, authorization, and restriction of
chemical substances
ROS reactive oxygen species
RXR 9-cis retinoic acid receptor
RyR ryanodine receptor
SAM S-adenosylmethione
SLC solute carrier proteins
SLC15 solute organic oligopeptide transporter
SLC22 solute organic anion/cation/zwitterion transporter
SLC47 solute organic cation transporter
SLCO solute organic anion transporter
SLP solute transport proteins
SPEAR species at risk approach
SP-ICP-MS single-particle inductively coupled mass spectroscopy
SSBG sex steroid-binding globulin
SSD species sensitivity distribution
SSD-EC50 an SSD model derived from EC50 data
SSD-NOEC an SSD model derived from no observed effect concen-
tration data
ssPAF single-substance potentially affected fraction
StAR steroidogenic acute regulatory
STP sewage treatment plant
SULT sulfotransferases
SWCNT single-walled carbon nanotubes
T3 triiodothyronine, a thyroid hormone
T4 thyroxine, a thyroid hormone
TAG triacylglycerol
TAG:ST triacylglycerol to structural lipids ratio
TBT tributyl tin
TCDD 2,3,7,8-tetrachlorodibenzo-p-dioxin
TCS triclosan
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