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Ecotoxicology and
Genotoxicology
Non-traditional Terrestrial Models
Published on 12 June 2017 on http://pubs.rsc.org | doi:10.1039/9781788010573-FP001

Edited by

Marcelo L. Larramendy
National University of La Plata, Argentina
Email: [email protected]
Published on 12 June 2017 on http://pubs.rsc.org | doi:10.1039/9781788010573-FP001 View Online

Issues in Toxicology No. 32

Print ISBN: 978-1-78262-811-8

PDF eISBN: 978-1-78801-057-3
EPUB eISBN: 978-1-78801-174-7
ISSN: 1757-7179

A catalogue record for this book is available from the British Library

r The Royal Society of Chemistry 2017

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Preface

Many important ecosystems around the world are being constantly

challenged owing to the growing human and industrial pressure exerted
upon them. The use of various biomarkers in local, easily available species
can be applied to evaluate the response of the biota to such pollutants.
Several biological parameters mirror the interactions between toxic agents
and biotic matrices. These are powerful tools that can be applied to
environmental monitoring tests and studies. Their responses may reveal
general deleterious effects to the organism, pinpointing alterations at a
cellular, biochemical and molecular level, as well as higher levels of
organisation.
Our global society needs to table down actions and set rules to evaluate
and considerably reduce the real and potentially hazardous factors in the
environment that can, as previously stated, result in health risks for all
forms of life (including Homo sapiens sapiens). Despite major positive con-
tributions in the field of health, owing to the immense progress achieved in
science, technology and industrialization, the interaction between environ-
mental risk and health is an often intricate equation, not self-evident, that
involves a variety of not only social, political and economic, but also lifestyle
factors. This cannot be emphasized enough. Health depends on the good
quality of environmental ‘‘basic ingredients’’, such as air, water, soil and
food, among others. We believe that the ultimate challenge in this matter is
to weigh-in short-term positive gains, while, at the same time, taking into
account long-term effects of substances used. Available information about
the toxic effects of heterogeneous xenobiotics, continuously released into
human habitats, inadvertently, deliberately, or by non-regulated industrial
discharges on biological components of the environment, is inconclusive.
There is not a clear-cut definition of the concept of Environmental Health.
Various openings help us in the understanding of this concept. According to

Issues in Toxicology No. 32

Ecotoxicology and Genotoxicology: Non-traditional Terrestrial Models
Edited by Marcelo L. Larramendy
r The Royal Society of Chemistry 2017
Published by the Royal Society of Chemistry, www.rsc.org

vii
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viii Preface

the World Health Organization, it is defined by ‘‘all the physical, chemical

and biological factors external to a person and all the related factors
impacting upon behaviours. It encompasses the assessment and control of
those environmental factors that can potentially affect health. It is targeted
towards preventing disease and creating health-supportive environments. . .’’
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For the National Environmental Health Association, this concept refers to

‘‘the protection against environmental factors that may adversely impact
human health or the ecological balances essential to long-term human
health and environmental quality, whether in the natural or man-made
environment.’’ A third definition by the National Institute of Environmental
Health Science also involves the criteria that ‘‘the social environment
encompasses lifestyle factors like diet and exercise, socioeconomic status,
and other societal influences that may affect health.’’
In general terms, our health and the health of many other species are
negatively affected by five broad categories of environmental hazards,
namely, electromagnetic fields (produced by high power lines, electrical
wiring, appliances, mobile phones, computers, and TV sets, etc.), radiation
(including nuclear fallout from weapons testing, fission materials from
nuclear power plants and their respective accidents, leaking radioactive
disposal sites, air travel and x-rays), toxic chemicals (some organochlorines,
phthalates, polybrominated flame retardants, perfluorinated substances,
bisphenol-A) and several toxic metals, among others, which have been
shown to have endocrine-disrupting properties, and finally soil mineral
depletion as a complex environmental hazard.
By definition, health risk assessment in its quantitative and/or qualitative
determinations includes variants such as the type of risk involved and the
severity of response, within or without a probabilistic context. In this regard,
risk-based methods of analysis play a strategic role in identifying and
ranking adverse responses or the structure of the effects of exposure vis-à-vis
environmental factors.
Many compounds can be hazardous if not used appropriately and may
present a real risk to the environment, contaminating soil, water and air.
Most of the pollutants in the different environmental compartments exert
their effects through cytotoxic, genotoxic and metabolically toxic mech-
anisms. In pollution studies, there is an increasing interest in biomonitoring
markers of biological exposure to pollutants. To achieve this goal, several
end-points for the three above-mentioned factors have been used in aquatic
and terrestrial invertebrate and vertebrate species on contaminated areas
(in situ assays) and to screen for xenobiotics after direct or indirect exposure
(in vivo assays).
The use of invertebrate and vertebrate autochthonous species as indi-
cators for monitoring pollutant-induced deleterious environmental effects
will raise the current awareness of real and potential hazards. It is also
known that most of the environmental pollutants not only affect target
organisms, but concomitantly exert negative effects on non-target species
as well.
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Preface ix

Invertebrate and vertebrate animal models have been used for decades in
acute and chronic toxicity tests for hazard identification. They can be very
efficient screening systems that have a major role to play in toxicity research,
because certain aspects of their biology, physiology and genetic character-
istics make them suitable models in ecotoxicological and genotoxicological
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studies.
These two books intend to provide an overview of the use of non-
conventional, locally available, invertebrate and vertebrate species as
experimental models for the study of different toxicological aspects induced
by environmental pollutants in both aquatic and terrestrial ecosystems.
Volume One, Ecotoxicology and Genotoxicology: Non-traditional Aquatic
Models includes examples of the use of aquatic species or aquatic stages of
terrestrial species and Volume Two, Ecotoxicology and Genotoxicology: Non-
traditional Terrestrial Models, is committed to terrestrial non-conventional
animal models.
Both volumes aim to shed some light on the matter, whilst offering
relevant tools for evaluating risk and to provide a framework for practical
discussions. These will foster decisions and actions required to reduce
environmental health risk against environmental factors. This piece of work
has been systematized for the sake of clarity, presenting some real-life
examples and extending concepts (of hazardous factors) to living species
that may stimulate new research ideas and trends in the relevant fields.
Available information has been compiled from a diversity of sources,
trying to achieve a representative global and geographical balance, as far as
possible, whilst at the same time aiming at high-quality studies. We believe
that this piece of work is unique in this sense.
Many researchers from different parts of the world have contributed to the
publication of this book. Given the fast pace of new scientific publications
shedding more light on the matter, these books will probably be outdated
very soon. We regard this as a positive and healthy fact. We hope that these
books will meet the expectations and needs of all those interested in the
environmental risk assessment field of study by the use of widely available
species worldwide. Finally, we also hope that the examples included in the
different chapters of these books will awaken the ability to search for new
organisms in local and regional ecosystems to pursue further studies in
ecotoxicology and genotoxicology. If our wishes are granted, we shall be
happy to oblige and edit the next edition of this series.

Prof. Dr Marcelo L. Larramendy

and Dr Guillermo Eli Liwszyc
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Contents

Section I: Terrestrial Invertebrates as Experimental Models

Chapter 1 The Use of Non-standardized Invertebrates in Soil
Ecotoxicology 3
Paulo Roger Lopes Alves, Julia Carina Niemeyer and
Elke Jurandy Bran Nogueira Cardoso

1.1 Soil Invertebrates 3

1.2 The Use of Invertebrates in Soil Ecotoxicology 6
1.3 Key Groups of Invertebrates for Soil Ecotoxicological
Testing 13
1.3.1 Earthworms 13
1.3.2 Collembolans 16
1.3.3 Enchytraeids 17
1.3.4 Isopods 18
1.3.5 Others 19
Acknowledgements 19
References 20

Chapter 2 Higher-tier Multi-species Studies in Soil: Prospects and

Applications for the Environmental Risk Assessment of
Pesticides 31
Björn Scholz-Starke, Sina Egerer, Andreas Schäffer,
Andreas Toschki and Martina Roß-Nickoll

2.1 Introduction 31

Issues in Toxicology No. 32

Ecotoxicology and Genotoxicology: Non-traditional Terrestrial Models
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r The Royal Society of Chemistry 2017
Published by the Royal Society of Chemistry, www.rsc.org

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xii Contents

2.2 Ecological Relevance of Soil Organisms in

Agro-ecosystems 33
2.2.1 Structure and Function of Soils and
Soil Organism Communities 33
2.2.2 Losses of Soil Biodiversity in Agricultural
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Landscapes 35
2.3 Status Quo and Developments of Risk Assessment
for In-soil Organisms 35
2.3.1 Status Quo 35
2.3.2 Transition 36
2.3.3 New Developments 37
2.3.4 Challenges 38
2.3.5 Future Demands 39
2.4 Methodologies for Multispecies Tests in Soil 40
2.4.1 Ontology and History of Test Systems 40
2.4.2 Methodological Challenges of Multispecies
Tests 43
2.5 Exposure of Soil Organisms Resulting From the
Fate of Pesticides 46
2.6 Calibration of Soil Risk Assessment Using
Semi-field Studies as Surrogate Reference Tiers 48
2.6.1 Specific Protection Goals 48
2.6.2 Derivation of Assessment Factors 49
2.6.3 TME as Surrogate Reference Tier 50
2.7 Conclusions 51
References 51

Chapter 3 Aporrectodea longa (Annelida, Lumbricidae): A Suitable

Earthworm Model for Genotoxicity Evaluation in the
Environment 59
Kirk T. Semple and Francis L. Martin

3.1 Introduction 59
3.2 Experimental 62
3.2.1 Earthworm Collection and Storage 62
3.2.2 Soil Collection and Amendment 62
3.2.3 Exposure Following Amendment with
Differing Pesticides or B[a]P 62
3.2.4 Coelomic Fluid Collection 63
3.2.5 The Alkaline Single Cell-gel Electrophoresis
(‘comet’) Assay 63
3.2.6 Exposure to Aged Cypermethrin Residues 64
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Contents xiii

3.3 Results and Discussion 64

3.3.1 Comet Generation from Differing
Compounds 66
3.3.2 Changes in Comet Formation Following
Exposure to Aged Cypermethrin Residues 68
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3.3.3 Uptake of 14C-Compound 71

3.4 Conclusion 71
Acknowledgements 72
References 72

Chapter 4 Evaluation of the Genotoxic Potential of Contaminated Soil

Employing the Snail Helix aspersa 76
J. Da Silva, M. R. de Souza, A. P. Nordin and F. R. Da Silva

4.1 Introduction 76
4.2 The Major Groups of Soil Contaminants 78
4.2.1 Heavy Metal 78
4.2.2 Organic Contaminants 79
4.2.3 Sewage Sludge 80
4.3 Helix aspersa for Biomonitoring of Contaminated
Soil 80
4.4 Genotoxicity Tests with H. aspersa and Contribution
to Environmental Research 84
4.5 Conclusions 88
Acknowledgements 89
References 89

Chapter 5 The Use of Spiders in the Assessment of Cellular Effects of

Environmental Stressors 96
G. Wilczek

5.1 Introduction 96
5.2 Spiders in Ecosystems Contaminated with
Heavy Metals 98
5.2.1 Cellular Defence Reactions in Spiders
from Areas Affected by Industrial
Pollution 101
5.3 Spider Sensitivity to Pesticides 107
5.3.1 Changes in AChE Activity 109
5.3.2 Enzymatic Detoxifying Reactions 110
5.3.3 Genotoxic and Cytotoxic Effects of Plant
Protection Agents in Spiders 111
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xiv Contents

5.4 Starvation Stress 114

5.5 Conclusions 115
References 116

Section II: Terrestrial Vertebrates as Experimental Models

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Chapter 6 Use of Melanin-pigmented Cells as a New Tool to Evaluate

Effects of Agrochemicals and Other Emerging
Contaminants in Brazilian Anurans 125
C. De Oliveira, L. Franco-Belussi, L. Z. Fanali and L. R. S. Santos

6.1 Color in Animals 125

6.2 Internal Melanin-pigmented Cells 128
6.3 Environmental Contamination and Its Effects on
Visceral Pigmentation 129
6.4 Response of Cutaneous Melanocytes to Aquatic
Contaminants 129
6.5 Response of Internal Melanocytes to Aquatic
Contaminants 130
6.6 Response of Melanomacrophages to Aquatic
Contaminants 134
6.7 Conclusion 138
Acknowledgements 138
References 138

Chapter 7 The Use of Terrestrial Life-stages of European Amphibians

in Toxicological Studies 143
Norman Wagner and Carsten A. Brühl

7.1 Introduction 143

7.2 Toxicological Studies on the Impact of Pesticides on
Terrestrial Life-stages of European Amphibians 145
7.3 Risk Assessments for Terrestrial Life-stages of
Amphibians in Pesticide Approval 149
7.3.1 Surrogate Species for Terrestrial Life-stages
of Amphibians 150
7.3.2 Indirect Effects 155
7.4 Pesticide Formulations—Toxicity in the Mix? 155
7.5 Conclusions 156
Acknowledgements 157
References 157
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Contents xv

Chapter 8 Impacts of Agriculture and Pesticides on Amphibian

Terrestrial Life Stages: Potential Biomonitor/Bioindicator
Species for the Pampa Region of Argentina 163
J. C. Brodeur and J. Vera Candioti
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8.1 Introduction 163

8.2 Amphibian Diversity, Life History and Global
Declines 164
8.2.1 Amphibian Diversity and Life History 164
8.2.2 Amphibian Declines 165
8.3 The Pampa Region of Argentina 166
8.3.1 Location, Geography and Characteristics 166
8.3.2 Evolution of Agricultural Practices and
Environmental Impacts 167
8.4 Agriculture and Amphibian Declines: The Need for
Biomonitoring 169
8.4.1 Agriculture and Amphibian Declines 169
8.4.2 Amphibians as Bioindicators and
Biomonitors 170
8.4.3 Suggested Amphibian Model Species for
Biomonitoring the Pampa Region of
Argentina 171
8.5 Description and Life Histories of Model
Amphibian Species for the Pampa Region of
Argentina 173
8.5.1 Leptodactylus latinasus (Jiménez de la
Espada, 1875) 173
8.5.2 Leptodactylus latrans (Steffen, 1815) 174
8.5.3 Hypsiboas pulchellus (Duméril and Bibron,
1841) 176
8.5.4 Rhinella dorbignyi (Dumeril and Bibron,
1841) and Rhinella fernandezae
(Gallardo, 1957) 177
8.5.5 Rhinella arenarum (Hensel, 1867) 178
8.6 Previous Biomonitoring Studies Conducted with
Proposed Amphibian Model Species 180
8.6.1 Studies Using Model Species as
Bioindicators 180
8.6.2 Studies Using Model Species as
Biomonitors 181
References 184
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xvi Contents

Chapter 9 Odontophrynus cordobae (Anura, Cycloramphidae):

A Suitable Model for Genotoxicity in Environmental
Monitoring Studies 195
F. Mañas, B. Bosch, N. Salas and D. Aiassa
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9.1 Biomarkers as a Tool to Assess the Impact of

Environmental Contamination 195
9.2 Amphibians are Suitable Organisms to Evaluate
the Genotoxic Effects of Environmental
Contaminants 197
9.3 Relevant Features of Odontophrynus cordobae
for Genotoxicity Studies in Environmental
Monitoring 198
9.4 Conclusions 202
References 204

Chapter 10 The Direct-developing Frog Eleutherodactylus johnstonei

(Eleutherodactylidae) as a Biological Model for the Study
of Toxic, Cytotoxic, and Genotoxic Effects of
Agrochemicals 211
Fabio Leonardo Meza-Joya, Martha Patricia Ramı́rez-Pinilla
and Jorge Luis Fuentes

10.1 Introduction 211

10.2 Natural History of the Antillean Coqui 212
10.3 Geographic Distribution 213
10.4 The Antillean Coqui as an Invasive Species 215
10.5 Conservation Status and Concerns 215
10.6 The Antillean Coqui as a Model in
Ecotoxicology 216
10.7 Collection, Maintenance, and Reproduction in
Captivity 218
10.7.1 Collection and Sex Determination 218
10.7.2 Taxonomic Identification 218
10.7.3 Maintenance and Reproduction in
Captivity 219
10.7.4 Handling Embryos 220
10.8 Applications for Testing Environmental
Xenobiotics 220
Acknowledgements 222
References 223
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Contents xvii

Chapter 11 The Lizard Salvator merianae (Squamata, Teiidae) as a

Valid Indicator in Toxicological Studies 228
P. A. Siroski, G. L. Poletta and M. D. Mudry

11.1 Introduction 228

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11.2 Evaluation of Effects of Environmental Agent 232

11.3 A Pathway to the Truth 232
11.4 Goals of Biological Monitoring 234
11.5 Studies In Ovo 236
11.6 Studies In Vivo under Controlled Conditions 241
11.7 Genotoxic Evaluation of Tegu Lizard
Environmentally Exposed to Pesticides 243
References 245

Chapter 12 The Terrestrial Lizard Podarcis sicula as Experimental

Model in Emerging Pollutants Evaluation 252
M. Verderame, E. Limatola and R. Scudiero

12.1 Introduction 252

12.2 Who is the Lizard Podarcis sicula? 253
12.3 Pollution by Organic Contaminants with
Estrogen-like Action: Fertilizers and Manure 254
12.4 Pollution by Heavy Metals: Cadmium 256
12.5 Podarcis sicula as Sentinel Lizard 256
12.6 Soil Pollution by Estrogen-like Substances 257
12.7 Soil Pollution by Pesticides 259
12.8 Soil Pollution by Cadmium 260
12.9 Conclusions 262
References 262

Chapter 13 The Yellow-legged Gull Larus michahellis

(Charadriiformes, Laridae) as a Model Species in
Ecotoxicology: Application in Monitoring and Toxicity
Assessment of Environmental Pollutants 269
Marco Parolini, Cristina Daniela Possenti and Nicola Saino

13.1 Introduction 269

13.2 Materials and Methods 273
13.2.1 Study Area 273
13.2.2 In Ovo PFOS Manipulation 273
13.2.3 PFOS Determination in Yolk Sac from
Control Eggs 274
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xviii Contents

13.2.4Oxidative and Genetic Biomarker Methods 275

13.2.5Statistical Analysis 276
13.3 Results
and Discussion 276
13.3.1PFOS Concentrations in Control Eggs 276
13.3.2PFOS Effects on Embryo Development and
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Morphometric Traits 277

13.3.3 PFOS Effect on Oxidative Stress and
Genetic Biomarkers 278
13.4 Conclusions 282
Acknowledgements 283
References 283

Chapter 14 South American Cowbirds as Avian Models for

Environmental Toxicity Testing 289
J. C. Brodeur and M. B. Poliserpi

14.1 Introduction 289

14.2 Actual and Historical Use of Birds in Science and
Regulatory Toxicology 290
14.2.1 Birds as Animal Models in Toxicology and
Scientific Research 290
14.2.2 Avian Models in Regulatory
Environmental Toxicity Testing 291
14.2.3 Pesticide Registration and Avian Toxicity
Testing in South America 292
14.3 South American Cowbirds’ Diversity, Distribution
and Life History 293
14.3.1 Shiny Cowbird 294
14.3.2 Bay-winged Cowbird 295
14.3.3 Screaming Cowbird 296
14.4 Cowbirds as an Avian Model for Environmental
Toxicity Testing 297
14.5 Methods for Maintaining and Using Cowbirds in
the Laboratory for Environmental Toxicity Testing 298
14.5.1 Capture and Transport 298
14.5.2 Housing, Acclimation and Feeding 299
14.5.3 Acute Oral Toxicity Testing 300
References 301

Chapter 15 Epilogue and Final Remarks 307

Marcelo L. Larramendy and Guillermo Eli Liwszyc

Subject Index 314