An Introduction to Aquatic Toxicology

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â•…â•…â•…â•…â•…
AN INTRODUCTION
TO AQUATIC
TOXICOLOGY
Mikko Nikinmaa
Professor of Zoology,
Department of Biology, Laboratory of Animal Physiology,
University of Turku, Turku, Finland

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15 16 17 18â•… 10 9 8 7 6 5 4 3 2 1
â•…â•…
Contents

Prefaceâ•…ix
Acknowledgmentsâ•…xi

1.╇ Introduction: What is Aquatic 5.╇ The Most Important Experimental

Toxicology? Designs and Organisms in Aquatic
Toxicology
1.1╇The History of Aquatic Toxicology╅ 1
1.2╇The Main Present and Future Challenges╅ 4 5.1╅Model Organisms Used╅ 54
1.3╇What is Measured╅ 5 5.2╅ Micro- and Mesocosms╅ 54
Relevant Literature and Cited Referencesâ•… 16 5.3â•…Ecosystem Manipulationsâ•…60
5.4â•…Biomonitoringâ•…61
2.╇ What Causes Aquatic Contamination? Relevant Literature and Cited References╅ 62

2.1╇Introduction╅ 20 6.╇ Factors Affecting the Bioavailability

2.2╇Metals, Metalloids, and Organometallic
of Chemicals
�Compounds╅ 23
2.3╇Other Inorganic Compounds, Including Factors
� 6.1╅
Introductionâ•…66
Causing Eutrophicationâ•… 29 6.2â•…
Pharmacological Bioavailabilityâ•…66
2.4╇Organic Compounds╅ 29 6.3╅
Environmental Bioavailabilityâ•…68
2.5╇Nanomaterials╅ 35 Relevant Literature and Cited References╅ 71
2.6╇Radiation╅ 36
2.7╇Genetic Modification╅ 38
Relevant Literature and Cited Referencesâ•… 38
7.╇ Chemical Uptake by Organisms
7.1â•…Introductionâ•…73
3.╇ Principles of Water Purification 7.2╅The Uptake of Ionic (Hydrophilic)
�Compounds╅ 76
3.1╇Principles of Wastewater Treatment╅ 41 7.3╅The Uptake of Lipophilic
3.2╇Disinfection Steps for Generating Household Compounds╅78
Waterâ•…44 Relevant Literature and Cited Referencesâ•… 79
3.3╇Sludge Treatment╅ 45
Relevant Literature and Cited Referencesâ•… 46
8.╇ Chemical Distribution
in Organisms
4.╇ Sources and Transport of Chemicals
in Aquatic Systems 8.1â•…Introduction: Distribution of Chemicals in
�Organisms╅ 81
4.1╇The Major Sources of Pollutants╅ 48 8.2╅ Storage Sites of Chemicals in Organisms╅ 82
4.2╇Transport of Pollutants in the Environment╅ 50 8.3╅Cellular Distribution of Chemicals╅ 83
Relevant Literature and Cited Referencesâ•… 51 Relevant Literature and Cited Referencesâ•… 84

v
vi CONTENTS

9.╇Detoxification 13.╇ Interactions between Chemicals

9.1â•…Biotransformation of Organic Compoundsâ•…88 13.1â•…Lack of Interacting Effects

9.2â•…Detoxification by Forming Non-Harmful (Additive Toxicity)â•… 157
�Complexes╅ 94 13.2╅Agonism (potentiation, synergism)╅ 159
9.3â•…Detoxification by Compartmentalizationâ•… 97 13.3â•…Antagonismâ•…162
Relevant Literature and Cited 13.4â•…Has Potentiation or Inhibition of Toxicity by
Referencesâ•…97 Chemical Interactions been Demonstrated in
Natural Environments?â•… 163
Relevant Literature and Cited
10.╇ Excretion of Compounds from �References╅ 163
Organisms
10.1╅Introduction╅100 14.╇ Acute and Chronic Toxicity
10.2â•…Cellular Excretionâ•…101
14.1╇Introduction╅ 165
10.3â•…Excretion from Gillsâ•… 102
14.2╇Differentiating between General Stress
10.4â•…Excretion from the Kidney and Other
Responses and Specific Acute Responses to
Excretory Organsâ•… 106
�Pollutants╅ 166
10.5â•…Excretion in Bile Via the Intestineâ•… 107
14.3╇Time Courses of Toxicant Responses╅ 168
10.6╅Excretion from Multicellular Plants �
14.4╇What Signifies a Chronic Toxicant
(Including Algae)â•… 109
�Response╅ 170
Relevant Literature and
Relevant Literature and Cited Referencesâ•… 171
Cited Referencesâ•… 109

15.╇ Interactions Between Natural

11.╇ Effects on Organisms
Environmental Factors and Toxicity
11.1â•…‘Omics in Aquatic Toxicology—Â�
Ecotoxicogenomics╅112 15.1╇Temperature╅ 174
11.2╅ Genotoxicity╅121 15.2╇Oxygen╅ 176
11.3╅ Oxidative Stress╅124 15.3╇Salinity╅ 179
11.4╅Effects on Reproduction╅ 130 15.4╇Other Abiotic Stresses╅ 180
11.5╅ Neurotoxicity╅133 15.5╇Competition and Predation╅ 181
11.6â•…Effects on Energy Metabolismâ•… 134 Relevant Literature and Cited Referencesâ•… 183
11.7â•… Membrane Effectsâ•…136
11.8╅Apoptosis and Necrosis╅ 138 16.╇ Effects of Chemicals on Aquatic
11.9â•… Immunotoxicologyâ•…139 Populations
11.10╇Effects on Development╅ 141
11.11╇Teratogenesis and 16.1╇Introduction╅ 186
Carcinogenesis╅142 16.2╇Epidemiology╅ 188
11.12╇Behavioral Effects╅ 143 16.3╇Demographic Effects╅ 190
Relevant Literature and 16.4╇Population Genetics╅ 191
Cited Referencesâ•… 144 Relevant Literature and
Cited Referencesâ•… 194
12.╇ Bioindicators and Biomarkers
17.╇ Effects of Chemicals on Aquatic
12.1â•…
Bioindicatorsâ•…147 Communities and Ecosystems
12.2â•…
Biomarkersâ•…149
Relevant Literature and Cited 17.1╇Introduction╅ 198
�References╅ 154 17.2╇Community Ecotoxicology╅ 199
 CONTENTS vii
17.3╇Ecosystem Ecotoxicology╅ 202 18.4╇Toxicokinetic Modeling╅ 215
Relevant Literature and 18.5╇QSAR╅ 215
Cited References╅ 204 18.6╇Modeling the Properties of Water �Affecting
Toxicity (of Metals)â•… 216
18.╇ Modeling Toxicity Relevant Literature and Cited References╅ 217

18.1╇Introduction╅ 208 Glossary╅221

18.2╇Risk Assessment╅ 209 Index╅233
18.3╇Models with Lethality as an End Point╅ 212
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 Preface

Any effects of contaminants on ecosystems in biotic interactions within or between

must be caused by their direct effects on one �species. Further, while �experimental studies
or more organisms in the ecosystem. Thus, are mainly � retrospective, modeling makes
changes in the function (= physiology) of aquatic toxicological predictions possible.
an organism or organisms will be behind Consequently, aquatic toxicology is truly
any ecotoxicological effects. Consequently, integrative, and I hope that I am able to give
understanding the normal physiology of this message to readers of the book. Since the
organisms is at the center of all toxicology. book is introductory, I have tried to find a
Effluent discharges (and thus the measure- balance between making it possible for any
ments of chemical concentrations) are of reader to understand the book and including
no toxicological significance if they cause new concepts to make it interesting reading,
no effects on any organism. Further, a con- even for aquatic toxicology experts.
taminant may cause effects on the genome Because my background is in animal
of an organism without phenotypic effects. physiology, the book is biased towards the
In such a case, the effect on the genome is animal kingdom. However, I hope that it
not toxicological. Even though this premise becomes clear to the reader that effects on
emphasizes the role of functional changes in prokaryotes, fungi, plants, and algae are
individual organisms, it is pointed out that equally important components of aquatic
interactions between organisms, and between toxicology. Which group of organisms
natural environmental and toxicant-induced receives most emphasis depends mainly
changes, occur whenever toxicant responses on the interests of the writer. Regardless of
of organisms in an ecosystem are considered. the group that receives the most attention,
For example, it is emphasized that many of the basic principles of aquatic toxicology
the effects of toxicants in an �ecosystem are are the same. However, as my approach to
indirect: the actual toxic effect is on a species toxicology is biological, the work may be
other than the one that is seen to respond. difficult for any reader without previous
The response takes place because of changes biological knowledge.

ix
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â•…â•…â•…â•…â•…
 Acknowledgments

My thanks go first and especially to my see. Regardless of their final fate, they have
wife, for all the help with practicalities made it possible to evaluate which points
when I have been consumed with different need to be emphasized in an introductory
aspects of writing. Second, all the students book in this field.
who have taken my ecotoxicology classes Every chapter ends with a very limited
have contributed to understanding which selection of relevant literature. I have included
aspects of aquatic toxicology are most inter- a reference only in one chapter, although it
esting and which most difficult. Third, my is clear that several references have material
research group and all the other people and conclusions that would also be relevant
working in the Animal Physiology Labora- for other chapters. The �literature selection is
tory of the Department of Biology at the Uni- by no means exhaustive, and undoubtedly
versity of Turku deserve thanks for making does not even include all the most impor-
the day-to-day working environment good tant references on the topic. I apologize for
and fruitful for a huge project, as the writ- any significant omissions, but hope that the
ing of this book turned out to be. I also want selected articles and books, as well as their
to thank the Elsevier production team, and literature lists, help �readers when they are
especially Molly McLaughlin, for helping to pursuing any topic further. The text also con-
fulfill the project. As a separate note, I was tains a glossary, again not inclusive, of terms
pleasantly surprised when Rhys Griffiths that aquatic �toxicology students �frequently
from Elsevier contacted me suggesting come across. The �figures have been drawn
that I write the book. Finally, and perhaps using SmartDraw 7, � SigmaPlot 12.3, and
most importantly, my sincere thanks go to PowerPoint 2010 software, frequently using
the aquatic toxicologists whose thousands Motifolio templates. Hopefully the � figures
of manuscripts I have been privileged to will clarify the text.

xi
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â•…â•…â•…â•…â•…
 C H A P T E R

1
Introduction: What is Aquatic
Toxicology?

O U T L I N E

1.1╇ The History of Aquatic Toxicology 1 1.3.1╇The Cascade from Subcellular

Genomic Effects to Ecosystem
1.2╇The Main Present and Future
Effects5
Challenges4
1.3.2╇ Toxicity Testing 9
1.3╇ What is Measured 5
Relevant Literature and Cited References 16

Abstract
The chapter first discusses the history of aquatic contamination, highlighting major cases where aquatic con-
tamination has become an issue and cases where efficient solutions to environmental problems have been
reached. Thereafter, the hierarchy of biological functions that can be disturbed by toxicants is briefly intro-
duced. Notably, even when the ultimate goal of toxicological research is to find out how contamination affects
an ecosystem, one must remember that the toxicants affect molecular functions of the most sensitive species.
Toxicological testing and its uses are then introduced. The principal available aquatic toxicology testing meth-
ods, as given by the International Organization for Standardization (ISO) and the Organisation for Economic
Co-operation and Development (OECD), are tabulated and the procedure for validating toxicity tests interna-
tionally is given. An overview of important issues for aquatic toxicological research in the future is also given.

Keywords: acid rain; paper- and pulp-mill effluent; toxicity test; gene expression; DNA methylation; epi-
genetics; direct effect; indirect effect; partial-life-cycle test; early-life-stage test; sediment toxicology; oil pollu-
tion; sublethal effects.

1.1╇ THE HISTORY OF AQUATIC TOXICOLOGY

As long as human populations remained small, anthropogenic influences on aquatic envi-
ronments remained small and local. Any effects were in the vicinity of bigger settlements.

An Introduction to Aquatic Toxicology

http://dx.doi.org/10.1016/B978-0-12-411574-3.00001-3 1 © 2014 Elsevier Inc. All rights reserved.
2 1. INTRODUCTION: WHAT IS AQUATIC TOXICOLOGY?

Probably the first larger-scale aquatic environmental issue resulted from lead water pipes that
were used in large Roman towns.
Later, a major aquatic environmental problem was generated when sewage systems
were built and people started using toilets (WCs). Consequently, contaminated household
water, urine, and feces were disposed of directly to surrounding waters. Although clean-
ing measures are nowadays taken for most large human settlements, at least in Europe,
Japan, North America, and Australia, the eutrophication caused by fertilizing compounds
from human settlements, industry, agriculture (including the production of livestock),
and aquaculture is a major threat to inland and coastal waters. Because gut bacteria can
cause epidemics of intestinal diseases (e.g. cholera), they are still a major component to be
determined when water quality criteria are established. The water quality framework is
defined for Europe in the Water Policy Framework Directive (WFD) of 26 February 1997,
and for the USA in the Clean Water Act and the Water Quality Act, of which the latter is
from 1987.
Upon industrialization, acid rain became an issue. By the end of 1800s, coal burning was
already causing acid rain and consecutive acidification of poorly buffered rivers and lakes
in the British Isles. The immediate solution was to increase the height of chimneys. In the
latter part of the twentieth century, this caused oxides of sulfur and nitrogen to be trans-
ported from central Europe and Britain to Scandinavia. The acid rain generated came down
into poorly buffered streams and lakes in Norway, Sweden, and Finland, where whole fish
stocks, especially of salmonids, were wiped out (see Figure 1.1 for the mechanism of water

FIGURE 1.1â•… Schematic representation of the formation of acid rain. The smoke contains oxides of sulfur and
nitrogen (SOx and NOx), which react with atmospheric water to form H2SO3, H2SO4, and HNO3. These acids are a
part of precipitation and acidify waterways.
 1.1╇ The History of Aquatic Toxicology 3
acidification). Similar acidification was observed in some parts of Canada, where it was
caused mainly by coal burning in the industrial areas of the USA. As clear environmen-
tal disturbances were observed and could be tied to specific polluting sources, in this case
sulfur-containing coal (and oil), and as the problems were observed in the aquatic systems
of democratic industrialized European and North American countries, it was soon required
that, first, the use of fuels containing much sulfur be curbed, second, the use of coal in
energy production be decreased, and, third, the smoke be cleaned, removing sulfur from
the gases. As a result of these measures, acid rain as an environmental problem is now all
but forgotten in Europe and North America. Healthy fish stocks have returned to many for-
merly acidified lakes. However, globally, acidification of freshwater is of major importance,
especially in Asia, where none of the measures that are required in Europe to prevent pollu-
tion are so far applied.
Until the latter part of the twentieth century, wastewater was virtually always uncleaned.
Whenever the vicinity of effluent pipes became fouled, the solution was to increase the length of
the effluent pipe. It was customary to talk about “the self-cleaning capacity of waters.” Because
of the idea that effluents could be fed into surrounding waters without cleaning, many major
catastrophes occurred. For example, the toxic effects of mercury were seen in the Minamata
incident in Japan. Tens or even hundreds of people died of mercury intoxication in 1956, as
untreated effluents from a chemical factory were discharged in a bay where local inhabitants
took their household water and ate the fish. Although the acute catastrophe could be pinpointed
to the single year, the mercury contamination of the bay occurred between 1932 and 1968, and
up to the present, around 2000 people have died with mercury intoxication being at least par-
tially responsible, and more than 10,000 people have received some kind of compensation for
mercury-intoxication-caused damages. Uncleaned paper- and pulp-mill effluents used to be a
major environmental question in western Europe and North America. In the 1960s, the paper-
and pulp-mill industry of Sweden and Finland produced an amount of effluent corresponding
to the effluent produced by 100,000,000 people. At that time, all the water areas close to the
paper and pulp mills were dead. Also, as a result of effluent discharge, the persistent organic
pollutant (POP) concentrations (including polychlorinated biphenyls, PCBs) were so high that
the reproduction of, for example, seals was very markedly affected. Since then, advances in
paper- and pulp-mill technology have enabled the industry to be much more environmentally
friendly: the use of chlorine in bleaching has been virtually discontinued, and the mills reuse
most water. Consequently, the areas earlier uninhabitable for fish now have successful popula-
tions, and the gray seal populations in the Baltic Sea, for example, have increased markedly
(Figure 1.2).
As a general conclusion from the history of aquatic toxicology, one can say that solu-
tions to environmental problems are possible, but remediation and prevention of future
problems require financial commitment. Thus, we should be prepared to pay some extra
cost for products that contribute minimally to the deterioration of the aquatic environment.
The decisions of consumers can ultimately change the ways of production. The directors
of Scandinavian paper- and pulp-mill companies said in the 1960s that cleaning the efflu-
ents would not be possible as it would unacceptably reduce profits. However, when paper
consumers started demanding cleaner paper, and began to leave environmentally costly
products on the shelf, measures for producing environmentally friendlier paper were soon
established.
4 1. INTRODUCTION: WHAT IS AQUATIC TOXICOLOGY?

FIGURE 1.2â•… Approximate population changes of the gray seal in the Baltic Sea from the 1940s to the 2000s.
Up to the 1940s, the population had decreased markedly from about 100,000 before the twentieth century because of
intensive hunting. From the 1940s to the 1960s, the population remained stable, and then decreased in the 1960s and
1970s with the rise of a paper- and pulp-mill industry with poor effluent purification. The pollution of the Baltic Sea
was associated with marked reproductive problems in seals. With the increasing efficiency of effluent cleaning, seal
reproduction has again improved, and the population size is close to the value seen in the 1940s and 1950s. Source:
Harding and Härkönen (1999) and Harding et€al. (2007).

1.2╇ THE MAIN PRESENT AND FUTURE CHALLENGES

Since energy production and cars and other motor vehicles have needed more and more
fuel, the demand for oil has continuously increased. Consequently, oil pollution associated
with its exploration, refining, and transport has become a major challenge to aquatic toxicol-
ogy. The problem becomes even more pronounced as oil exploration occurs increasingly in
aquatic areas, in the Arctic and in deeper water than earlier. This means that major emphasis
needs to be given to interactions with oil contamination and the natural environmental vari-
ables temperature and pressure. Another serious problem is that many different chemicals have
been dumped in various aquatic bodies. The exact chemicals and even the places where dump-
ing has occurred are often unknown. Important questions pertaining to aquatic environments
involve sediment toxicology: how is the toxicity of a chemical affected by its adherence to the
bottom sediment, what is the bioavailability of toxicants in the sediment, and how do toxi-
cants move between the sediment and water? Since toxicants can affect each other’s effects, it
will be increasingly important to characterize these “cocktail effects.” On a global scale, and as
European and North American water purification standards are not used in many areas, the
employment of universal water standards should be a priority, and include the costs involved
in water cleaning. �Water-cleaning units will be required everywhere, both for preventing the