MERTENSIELLA Studies on Anomalies in Natural Populations of Amphibians Untersuchungen zu

265 Pages·2017·12.22 MB·English

Preface
MERTENSIELLA
Studies on Anomalies
in Natural Populations of Amphibians
Untersuchungen zu Anomalien
in natürlichen Populationen von Amphibien
Herausgegeben von
Klaus Henle & Alain Dubois
im Autrag der
Deutschen Gesellschaft für Herpetologie und Terrarienkunde e.V.
Mertensiella 25
Supplement zu Salamandra
Mannheim, 15. August 2017
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A catalogue record for this publication is available from the German National Library (Deutsche Nationalbibliothek) at
http://dnb.dnb.de
Studies on Anomalies in Natural Populations of Amphibians
Edited by Klaus Henle & Alain Dubois
Distributor: Chimaira Buchhandelsgesellschaft mbH
Heddernheimer Landstr. 20
60439 Frankfurt am Main, Germany
Telefon: [phone]
Fax: [phone]
E-Mail: [email protected]
Internet: www.chimaira.de
Layout: Andreas Mendt, Office of the DGHT
Typesetter: Ogarit Uhlmann, Leipzig
using Minion Pro
Cover design: Darina Schmidt, with photos of: Front cover top: Pelophylax ridibundus with polydactyly, Ekaterinburg, Russia (photo:
Vladimir Vershinin). Front cover bottom left: captive bred erythristic Salamandra salamandra (photo: Benny Trapp). Front cover
center: adactyly in a juvenile Bufotes viridis, Magnitogorsk, Russia (photo: Vladimir Vershinin). Back cover top left: juvenile Bufotes
viridis with polymely from an anomaly hotspot near Roßwag, Germany (photo: Klaus Henle). Back cover top right: Captive bred
Dendrobates auratus with polymely (photo: Harald Divossen). Back cover centre: incomplete duplication of the hand in a Salamandra
atra, Hintersteiner Tal, Germany, July 2009 (photo: Ulrich Schulte).
Printed and bound by: Westermann Druck Zwickau GmbH, Zwickau, Germany
© Deutsche Gesellschaft für Herpetologie und Terrarienkunde e. V. (DGHT)
N4, 1, D-68161 Mannheim, Tel.: [phone]; Fax: [phone]
www.dght.de, [email protected]
All rights reserved
ISBN 978-3-89973-570-3
ISSN 0934-6643
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Table of contents
Table of contents
Preface ................................................................................................................................................................................................. 7–8
Commented glossary, terminology and synonymies of anomalies in natural populations of amphibians
Klaus Henle, Alain Dubois & Vladimir Vershinin ............................................................................................................. 9–48
1 Introduction .................................................................................................................................................................................. 10
2 Terms, definitions and synonyms .............................................................................................................................................. 11
2.1 Anomalies of colouration and pattern .............................................................................................................................. 11
2.2 Morphological anomalies ................................................................................................................................................... 20
2.2.1 Anomalies of limbs ..................................................................................................................................................... 21
2.2.2 Anomalies of the head, body or tail .......................................................................................................................... 36
2.3 Edema, tumour and similar types of anomalies .............................................................................................................. 41
2.4 Anomalies of eggs and early embryonic stages ................................................................................................................. 42
2.5 Other terms ........................................................................................................................................................................... 43
3 Acknowledgments ........................................................................................................................................................................ 44
4 References ...................................................................................................................................................................................... 45
Rostand’s anomaly P in Palaearctic green frogs (Pelophylax) and similar anomalies in amphibians
Alain Dubois ..................................................................................................................................................................................... 49–56
1 Introduction .................................................................................................................................................................................. 50
2 The anomaly P syndrome ............................................................................................................................................................ 50
3 The search for the cause ............................................................................................................................................................... 51
4 Ecological significance of anomaly P ......................................................................................................................................... 53
5 Species affected ............................................................................................................................................................................. 53
6 Conclusion .................................................................................................................................................................................... 53
7 Acknowledgements ...................................................................................................................................................................... 54
8 References ...................................................................................................................................................................................... 54
A review of anomalies in natural populations of amphibians and their potential causes
Klaus Henle, Alain Dubois & Vladimir Vershinin ...................................................................................................... 57–164
1 Introduction .................................................................................................................................................................................. 60
2 Methods ......................................................................................................................................................................................... 60
2.1 Data collation ........................................................................................................................................................................ 60
2.2 Causal inference ................................................................................................................................................................... 61
3 Occurrence of anomalies in natural populations .................................................................................................................... 62
3.1 Hotspots of anomalies .............................................................................................................................................................. 66
3.1.1 Europe ........................................................................................................................................................................... 67
3.1.2 Asia ................................................................................................................................................................................ 69
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Table of contents
3.1.3 Australia and Oceania ................................................................................................................................................ 72
3.1.4 Africa ............................................................................................................................................................................. 72
3.1.5 South and Central America ........................................................................................................................................ 73
3.1.6 The Caribbean islands and Bermuda ........................................................................................................................ 73
3.1.7 North America ............................................................................................................................................................. 74
3.2 Skeletal anomalies ............................................................................................................................................................... 83
3.2.1 Supernumerary elements ............................................................................................................................................ 83
3.2.2 Absence and reduction of skeletal elements ............................................................................................................. 89
3.2.3 Other externally visible skeletal anomalies .............................................................................................................. 100
3.3 Non-skeletal morphological anomalies ............................................................................................................................ 105
3.3.1 Duplications and absence of structures .................................................................................................................... 105
3.3.2 Other non-skeletal morphological anomalies .......................................................................................................... 107
3.3.3 Abnormal size ............................................................................................................................................................... 110
3.3.4 Edema and bloatedness, tumours and nodules, cysts and swellings ................................................................... 111
3.3.5 Colour anomalies ......................................................................................................................................................... 115
4 Species differences in sensitivity ............................................................................................................................................... 124
5 Individual and population level effects ................................................................................................................................... 128
5.1 Individual level effects ........................................................................................................................................................ 128
5.2 Population level effects ........................................................................................................................................................ 130
6 Temporal patterns in the occurrence of anomalies and their reporting ........................................................................ 131
6.1 Historical collections .......................................................................................................................................................... 131
6.2 Resurveys .............................................................................................................................................................................. 132
6.3 Long-term monitoring of sites .......................................................................................................................................... 133
6.4 Prevalence of anomalies in large-scale surveys and background rates ..................................................................... 133
6.5. Mechanistic explanations linking an increased frequency of anomalies to environmental changes ............................. 134
7 Conclusion and perspective ....................................................................................................................................................... 135
8 Acknowledgments ........................................................................................................................................................................ 136
9 References ...................................................................................................................................................................................... 137
The Roßwag affair: history and controversy of the discovery of mass anomalies in the green toad (Bufotes viridis)
in a German quarry
Klaus Henle, Kurt Rimpp, Josef Margraf & Alain Dubois ............................................................................................... 165–184
1 Introduction .................................................................................................................................................................................. 166
2 History of the affair .................................................................................................................................................................... 167
3 Discussion ..................................................................................................................................................................................... 174
3.1 Lessons learnt ...................................................................................................................................................................... 174
3.1.1 Handling sensitive discoveries ................................................................................................................................... 175
3.1.2 Involvement of the mass media .................................................................................................................................. 176
3.1.3 The role of science and scientists ............................................................................................................................... 176
3.1.4 Management of the affair by responsible authorities ................................................................................................ 177
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Table of contents
3.2 Open questions ..................................................................................................................................................................... 178
4 Acknowledgments ........................................................................................................................................................................ 178
5 References ..................................................................................................................................................................................... 178
6 Appendix I – Background information relevant for understanding the development of the conflict .............................. 183
6.1 German quarries: operations and characteristics ........................................................................................................... 183
6.2 Administrative structures and political responsibilities ................................................................................................ 183
6.3 Institut für Energie- und Umweltforschung (IFEU) ..................................................................................................... 183
6.4 Involvement of the Federal Government ......................................................................................................................... 183
Mass anomalies in green toads (Bufotes viridis) at a quarry in Roßwag, Germany: inbred hybrids, radioactivity or
an unresolved case?
Klaus Henle, Alain Dubois, Kurt Rimpp & Vladimir Vershinin ...................................................................................... 185–242
1 Introduction .................................................................................................................................................................................. 187
2 Habitat of the abnormal toad population – The Roßwag quarry .......................................................................................... 188
3 Amphibian surveys in the Roßwag quarry ............................................................................................................................ 188
4 Assessment of anomalies ............................................................................................................................................................ 190
4.1 Methods ................................................................................................................................................................................ 190
4.2 Frequency of anomalies ...................................................................................................................................................... 191
4.3 Types of anomalies observed in the Roßwag population ............................................................................................. 192
4.3.1 Recently metamorphosed and adult individuals ................................................................................................... 192
4.3.2 Tadpoles ........................................................................................................................................................................ 196
4.4 Individual variability in anomalies .................................................................................................................................. 197
5 Investigations into potential causes .......................................................................................................................................... 198
5.1 Amphibian surveys in the wider vicinity of the Roßwag quarry ............................................................................ 198
5.2 Laboratory studies of anomalies ...................................................................................................................................... 198
5.3 Hybridization ....................................................................................................................................................................... 199
5.4 Potential predators ............................................................................................................................................................... 201
5.5 Chemical analyses ............................................................................................................................................................... 201
5.6 Radioactivity studies ........................................................................................................................................................... 202
5.6.1 Assessment methods ................................................................................................................................................... 202
5.6.2 Assessment results ........................................................................................................................................................ 202
5.6.3 Experimental studies on the effects of radioactivity on amphibians .................................................................... 204
6 Discussion ..................................................................................................................................................................................... 205
6.1 Evaluation of hypotheses suggested for the Roßwag population ................................................................................ 206
6.1.1 Normal natural occurrence ....................................................................................................................................... 206
6.1.2 Non-genetic factors ..................................................................................................................................................... 208
6.1.3 Factors revealing or inducing genetic-based anomalies ......................................................................................... 218
6.2 Conclusion ........................................................................................................................................................................... 225
7 Acknowledgements ...................................................................................................................................................................... 227
8 References ..................................................................................................................................................................................... 227
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Table of contents
Methodological recommendations for studying the causes of anomalies in natural populations of amphibians
Alain Dubois & Klaus Henle ...................................................................................................................................................... 243–260
1 Introduction .................................................................................................................................................................................. 244
2 Field survey protocol ................................................................................................................................................................... 245
3 Patterns of anomalies as clues to potential causes .................................................................................................................. 247
3.1 Frequency .............................................................................................................................................................................. 247
3.1.1 Isolated cases of anomalies or injuries .................................................................................................................... 247
3.1.2 Anomalies observed in a few individuals per hundred ......................................................................................... 250
3.1.3 Mass anomalies ............................................................................................................................................................. 250
3.2 Distribution of anomalies among sexes and age classes ................................................................................................. 250
3.3 Variation of anomalies in time and space .......................................................................................................................... 251
3.4 Morpho-anatomy of anomalies .......................................................................................................................................... 251
3.4.1 Particularities of anomalies ......................................................................................................................................... 251
3.4.2 Bilaterality and symmetry .......................................................................................................................................... 251
3.4.3 Gradients of severity ................................................................................................................................................... 251
3.4.4 Syndromes of anomalies .............................................................................................................................................. 252
3.4.5 Association of various anomalies that do not constitute a syndrome .................................................................. 252
3.5 Similar anomalies concerning several sympatric species ................................................................................................ 253
4 Study of environmental factors ................................................................................................................................................... 253
5 Direct study of the causes ............................................................................................................................................................ 253
5.1 Detailed anatomy ................................................................................................................................................................. 254
5.2 Long-term observation of phenotype ............................................................................................................................... 254
5.3 Regeneration experiments ................................................................................................................................................... 254
5.4 Breeding experiments .......................................................................................................................................................... 254
5.5 Experimental gynogenesis ................................................................................................................................................... 254
5.6 Experimental teratology ...................................................................................................................................................... 255
5.7 Long-term studies of populations ....................................................................................................................................... 255
6 Conclusion ..................................................................................................................................................................................... 255
7 Acknowledgements ....................................................................................................................................................................... 255
8 References ...................................................................................................................................................................................... 255
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MERTENSIELPLreAfa 2c5e | 7–8 | 2017
Preface
Anomalies in humans and animals have attracted cu- on this topic. The junior editor of this volume, Alain
riosity for centuries. Long ago scientific writers started Dubois, was called in as a witness for the suggestion
to collate their observations of anomalies (primarily of that the anomalies observed in Roßwag had a natural
humans and their domesticated animals). Apart from cause and that the case was nothing unusual. He was
the odd early observation, amphibian anomalies in nat- introduced to the study of anomalies in amphibians by
ural populations only really came on the scene about Jean Rostand, an amateur naturalist. At that time Jean
150 years ago. Many amphibians develop externally and Rostand was the world’s leading expert on anomalies
therefore abnormal development during ontogeny is in natural populations of amphibians and the first per-
comparably easy to detect. It is largely because of this son to systematically investigate the cause of a certain
that amphibians have played, and still play, such a piv- type of mass anomalies affecting European water frogs
otal role in the emerging science of developmental biol- (Pelophylax species), which he termed anomaly P. At
ogy. However, natural history and developmental biol- some stages during the debate about the Roßwag case,
ogy were only merged in the early phases of research it was suggested that the mass anomalies observed in
on anomalies in natural populations of amphibians and, Roßwag were also a form of anomaly P in spite of very
until recently, the latter largely remained the domain of incompatible patterns of anomalies as was immediately
non-professional naturalists and the spare time of pro- clear to A. Dubois.
fessional herpetologists, without entering mainstream The contributions to this volume of MERTENSIEL-
science. Nevertheless, an impressive amount of litera- LA reflect the experiences that we made during the de-
ture has accumulated on anomalies in natural popula- bates about the causes of the anomalies of the green
tions. toads from the quarry near Roßwag, as well as the dif-
More recently, increased environmental awareness, ficulties we encountered in reviewing and analysing the
the global decline in amphibians and the increased relevant literature, and the observations that others in
number of observations of populations exhibiting mass other parts of the world have faced similar challenges.
anomalies have created renewed interest in amphib- One of the challenges was the absence of a comprehen-
ian anomalies as potential indicators for environmen- sive terminology with synonyms, as terminology is often
tal perturbations. Observations of mass anomalies have inconsistently used and changed over time. We there-
started to raise questions about why and what it means fore begin with a contribution on this topic. The second
for the affected individual, humans and the environ- contribution provides an updated review of anomaly P.
ment. The same applies to the senior editor of this issue Although there have been a large number of reviews
of MERTENSIELLA, when he stumbled by accident on of specific issues within the research field of amphibi-
a population of green toads (Bufotes viridis) in a quar- an anomalies, there was no comprehensive overview at
ry near Roßwag in southern Germany that exhibited the time of our discovery in Roßwag. Even today, it is
a range of different types of anomalies and a high fre- challenging to find an appropriate overview of what has
quency of affected individuals that later turned out to been observed about amphibian anomalies in the wild
make it one of the hottest hotspots of anomalies in am- and what the assumed causes are. We therefore provide
phibians ever discovered. a comprehensive review of these issues in the form of
This discovery was the start of a long and heated con- a compendium with the aim of helping others to find
troversial discussion about the causes of these anoma- their way to the relevant literature.
lies. The final official conclusion of the German authori- The lack of a comprehensive overview at the time of
ties was that these anomalies were of a natural and not our discovery also created challenges to develop and test
anthropogenic origin, being a combination of inbreed- hypotheses about potential causes. The same difficulties
ing, hybridization and atavism. While it was clear that reappeared when North American scientists started to
this explanation does not have a sound scientific basis, study North American anomaly hotspots and the last-
the widely scattered literature on the subject has made ing controversy about potential causes stress how dif-
it challenging to evaluate the case appropriately. Biolo- ficult it still is to get to the bottom of them. This con-
gists in North America experienced the same difficulty troversy also highlights the urgent need for a compre-
when they rediscovered mass anomalies in amphibians hensive reference to the types of anomalies that can be
in the mid–1990s. caused by various factors. By presenting the research on
At the time when the case near Roßwag was discov- the Roßwag case we summarize the results of experi-
ered in 1980, specialists on anomalies in natural pop- mental studies including all factors that have so far been
ulations of amphibians were almost non-existent and suggested as potential culprits for anomalies in natural
even today very few scientists or research groups focus populations of amphibians.
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Preface
Addressing mass anomalies in natural populations years of work in compiling this volume, either in the
creates challenges well beyond science, often involving field, with the literature or by commenting on various
very sensitive issues in politics and society. Natural sci- parts of our manuscripts. Above all, we would like
entists are not trained to handle such issues, but rather to thank Jean-Claude Beetschen, Toulouse, and
have to learn these skills by trial and error, usually with- Alain Collenot, Paris, for the painstaking work
out guidance. The experiences of Judy Helgen in her of carefully reviewing and commenting on all of our
book ‘Perils in the Pond’ demonstrate this for the work manuscripts. Their life-long research experience on
on North American hotspots. Our experiences were anomalies in amphibians has considerably helped to
very similar. To help others that might encounter similar improve our manuscripts. Vladimir Vershinin fa-
problems, whether with amphibians or other species, we cilitated access to the Russian literature. KH cordially
wrote about our failures and success and provide recom- thanks Marlies Uhlig, Leipzig, for the tremendous
mendations that could help to avoid the worst pitfalls. help in finding and acquiring literature on amphib-
Finally, as appropriate study designs are a prerequi- ian anomalies, cataloguing it in databases and help-
site for improving our knowledge of anomalies in natu- ing to check the reference lists in our manuscripts.
ral populations and their causes, we provide guidelines He is also most grateful to Natalia Rumyantseva,
for such studies. Leipzig, for help with translations of Russian publica-
We would like to use this opportunity to thank all tions and for enduring endless hours of his work on
of our friends and colleagues that helped us over the the manuscripts.
Klaus Henle Alain Dubois
Leipzig, August 2017 Paris, August 2017
8
MERTTeErmNiSnIoElLoLgAy a2n5d |g 9lo–s4s8a r|y 2017
Commented glossary, terminology and synonymies of anomalies in
natural populations of amphibians
Klaus Henle1, Alain Dubois2 & Vladimir Vershinin3,4
1UFZ – Helmholtz Centre for Environmental Research,
Department of Conservation Biology, Permoserstr. 15, 04318 Leipzig, Germany; email: [email protected]
2Institut de Systématique, Évolution, Biodiversité ISYEB – UMR 7205 – CNRS, MNHN, UPMC, EPHE Muséum natio-
nal d’Histoire naturelle, Sorbonne Universités, 57 rue Cuvier, CP 30, 75005, Paris, France; email: [email protected]
3Institute of Plant and Animal Ecology, Uralian Division, Russian Academy of Science,
8 Marta St 202, 620144, Ekaterinburg, Russia; email: [email protected]
4Ural Federal University, Ekaterinburg, Mira St 19, 620002, Russia
Abstract. To allow comparison of observations an unequivocal definition of terms is essential. While early scholars
of amphibian anomalies already introduced specific terms and provided extensive definitions, some of these terms
have changed their meaning over time, some are no longer used and others have been replaced more recently with al-
ternative terms by some but not all authors. Most of the more recently published glossaries are rather narrow in their
coverage, addressing primarily a limited set of skeletal anomalies, few provide synonyms and none of them discuss
inconsistencies among different terminologies. To facilitate an understanding of the contributions in this volume and
to facilitate comparison of publications in general, we provide an extensive glossary and synonymy of the terms used
to describe external anomalies of amphibians. This includes colour and pattern anomalies, morphological anomalies,
anomalies related to edema or tumours and anomalies of embryos. We discuss the inconsistencies among different
terminologies and make recommendations for a future standardized use of terms. Our most important recommen-
dation is to explicitly refer to a particular terminology and to describe the anomaly sufficiently to enable readers to
understand what has been observed even if they are accustomed to using another terminology.
Keywords. Amphibia, anomalies, colour anomalies, skeletal anomalies, synonymies, terminology
Zusammenfassung. Eine eindeutige Definition von Begriffen ist für den Vergleich von Beobachtungen essentiell.
Zwar haben bereits die ersten Forscher, die sich mit Anomalien in natürlichen Populationen von Amphibien be-
schäftigt haben, Begriffe zur Differenzierung verschiedener Typen von Anomalien eingeführt und dafür ausführliche
Definitionen gegeben, jedoch haben einige Begriffe im Laufe der Zeit ihre Bedeutung geändert, andere fielen in Ver-
gessenheit und wieder andere wurden von manchen, jedoch nicht allen neueren Autoren durch neue Begriffe ersetzt.
Die meisten neueren publizierten Glossare sind im Umfang relativ beschränkt und beziehen sich vorwiegend auf eine
kleine Auswahl von Skelettanomalien. Die meisten von ihnen gehen weder auf Synonyme noch auf unterschiedliche
Definitionen von Begriffen durch verschiedene Autoren ein. Um das Verständnis der folgenden Beiträge in diesem
Band und den Vergleich unterschiedlicher Publikationen zu erleichtern, stellen wir hier ein umfangreiches Glossar
inklusive Synonyme zusammen. Dies umfasst Farb- und Musteranomalien, morphologische Anomalien, ödem- so-
wie tumorähnliche Anomalien und Anomalien von Embryonen. Wir diskutieren abweichende Verwendungen von
Begriffen durch verschiedene Autoren und machen Vorschläge für eine konsistente Begriffsverwendung. Die wich-
tigste Empfehlung besteht darin, sich eindeutig auf eine bestimmte Terminologie zu beziehen und Beobachtungen
ausführlich genug zu beschreiben, dass Leser die Art der Anomalie eindeutig identifizieren können, auch wenn sie
eine andere Terminologie gewöhnt sind.
Schlagwörter. Amphibia, Anomalien, Farbanomalien, Skelettanomalien, Synonyme, Terminologie
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