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The Biology of Caves and Other
Subterranean Habitats
THE BIOLOGY OF HABITATS SERIES
This attractive series of concise, affordable texts provides an integrated overview of the design,
physiology, and ecology of the biota in a given habitat, set in the context of the physical
environment. Each book describes practical aspects of working within the habitat, detailing the
sorts of studies which are possible. Management and conservation issues are also included.
The series is intended for naturalists, students studying biological or environmental science,
those beginning independent research, and professional biologists embarking on research in
a new habitat.

The Biology of Streams and Rivers

Paul S. Giller and Björn Malmqvist
The Biology of Soft Shores and Estuaries
Colin Little
The Biology of the Deep Ocean
Peter Herring
The Biology of Soil
Richard D. Bardgett
The Biology of Polar Regions, 2nd Edition
David N. Thomas et al.
The Biology of Caves and Other Subterranean Habitats, 2nd Edition
David C. Culver and Tanja Pipan
The Biology of Alpine Habitats
Laszlo Nagy and Georg Grabherr
The Biology of Rocky Shores, 2nd Edition
Colin Little, Gray A. Williams, and Cynthia D. Trowbridge
The Biology of Disturbed Habitats
Lawrence R. Walker
The Biology of Freshwater Wetlands, 2nd Edition
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The Biology of Peatlands, 2nd Edition
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The Biology of Mangroves and Seagrasses, 3rd Edition
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The Biology of Deserts, 2nd Edition
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The Biology of Lakes and Ponds, 3rd Edition
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Charles R.C. Sheppard, Simon K. Davy, Graham M. Pilling, and Nicholas A.J. Graham
The Biology of Grasslands
Brian J. Wilsey
The Biology of Urban Environments
Philip James
The Biology of
Caves and Other
Subterranean
Habitats
SECOND EDITION

David C. Culver and Tanja Pipan

1
1
Great Clarendon Street, Oxford, OX2 6DP,
United Kingdom
Oxford University Press is a department of the University of Oxford.
It furthers the University’s objective of excellence in research, scholarship,
and education by publishing worldwide. Oxford is a registered trade mark of
Oxford University Press in the UK and in certain other countries
© David C. Culver & Tanja Pipan 2019
The moral rights of the authors have been asserted
First Edition published in 2009
Second Edition published in 2019
Impression: 1
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ISBN 978–0–19–882076–5 (hbk.)
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Preface to the Second Edition

We are in a golden age of the study of subterranean biology. Thirty-five years

ago, when one of us (DCC) wrote a book on the biology of caves, it was easy
to read and discuss all the non-taxonomic literature on cave biology written
in English. Today, there are well over 200 papers per year published on
the biology of subterranean habitats. Thirty-five years ago, for American
speleobiologists, but much less so for European biologists, speleobiology meant
the biology of caves. There was scarcely any recognition or awareness of non-
cave subterranean environments among American speleobiologists. The
scope of speleobiology has expanded to include those subterranean1 habitats
whose inhabitants include blind, depigmented species with compensatory
increases in other sensory structures. In fact, there has been so much
research on these non-cave subterranean habitats, that five years ago we
wrote a book devoted to these habitats that are very close to the Earth’s sur-
face—Shallow Subterranean Habitats: Ecology, Evolution, and Conservation.
Since the publication of the first edition, a number of books on various aspects
of speleobiology have been published, including general treatments by Romero
(2009) and Fenolio (2016), a book on the microbiology of caves (Engel 2016),
four! books on cavefish—Keene et al. (2016), Trajano et al. (2010), Wilkens
and Strecker (2017), and Zhao and Zhang (2009), and a second edition of the
Encyclopedia of Caves (White and Culver 2012). In addition, there have been
more than 1000 research papers on speleobiology published since the first
edition of this book.
Our strategy in the second edition has been to update information in the
first edition, while still focusing on a relatively small number of well-studied
cases. We have replaced some of the case studies from the first edition but
have not changed others just because there have been more recent publications
on the topic. The growth of information has, of course, not been uniform
across subdisciplines. Phylogeography, biodiversity, and evo-devo have in
particular experienced a growth spurt. All in all, we have added approxi-
mately 125 references published since the first edition.

1
We use subterranean in the sense of organisms living in natural spaces. The word subter-
ranean is also frequently applied to organisms that create their own spaces—especially mam-
mals such as mole rats, termites, and plant roots. The word hypogean is sometimes used in the
sense we use subterranean, but its use is uncommon, and we use enough uncommon words as
it is. There are many precedents for the way we use the word, such as the International Society
for Subterranean Biology and its journal Subterranean Biology.
vi PREFACE TO THE SECOND EDITION

We hope that this book is accessible to a wide variety of readers. We have

assumed no training in biology beyond a standard university year-long
course, and we have tried to make the geological and chemical incursions
self-contained. An extensive glossary should help the readers through any
terminological rough spots.
We have organized this book around what seem to us to be the major
research areas and research questions in the field. To provide a context for
these questions, we review the different subterranean environments (Chapter 1),
what the energy sources are for subterranean environments given that the
main energy source in surface environments—photosynthesis—is missing
(Chapter 2), and the main inhabitants of these underground domains
(Chapter 3). The research areas that we focus on are as follows:
• How are subterranean ecosystems defined and organized, and how in par-
ticular does organic carbon move through the system (Chapter 4)?
• How do species interact and how do these interactions, such as compe-
tition and predation, organize and constrain subterranean communities
(Chapter 5)?
• How did subterranean organisms evolve the bizarre morphology of
elongated appendages, no pigment, and no eyes (Chapter 6)?
• What is the evolutionary and biogeographical history of subterranean
species? Are they in old, relic lineages (Chapter 7)? How does their distri-
bution relate to past geological events?
• What is the pattern of diversity of subterranean faunas over the face of the
Earth (Chapter 8)?
We close by ‘putting the pieces together’ and examining some representative
and exemplary subterranean communities (Chapter 9), and how to conserve
and protect them (Chapter 10).
With the exception of Chapters 1–3, where we have attempted to provide a
comprehensive geographical and taxonomic review of the basics, we have
focused on a few particularly well-studied cases. Although we have provided
case studies from throughout the world, readers from Africa, South America,
and Asia will no doubt find a North American and European bias. Of this we
are certainly guilty, but in part this bias is because of longer traditions of study
of subterranean life in Europe and North America. We have added several
case studies from Asia and South America. We have provided an extensive
bibliography and hope that interested readers will pursue the subjects fur-
ther. Where English language articles are available, we have highlighted
them, but we also have not hesitated to include particularly important or
unique papers in other languages.
A cautionary word about place names. Many species are limited to a single
cave, well, or underflow of a brook, and, if for no other reason, this makes it
important to accurately give place names. Throughout the book we have
 PREFACE TO THE SECOND EDITION vii

identified the country and state or province in which a site is located. We

have, whenever possible, retained the spelling of the local language. Translation
runs the risk of confusing anyone trying to identify a particular cave or site,
and also runs the risk of repeating the word cave in different languages, as in
Postojnska jama Cave (Postojna Cave Cave). Postojnska jama already has
names in three languages (Slovene, Italian, and German) and there is no
need to add a fourth. A list of sites mentioned in the text is provided.
Even to us, the field of subterranean biology seems especially burdened with
obscure terminology. While there is a temptation to ignore it as much as
possible, it is widespread in the literature and some of it is even useful. We
have defined many terms in the text when we first use them, and have
included an extensive glossary to aid readers.
Besides the fascination of their bizarre morphology (which cannot really be
overrated), there are two main reasons for biologists to be interested in sub-
terranean faunas. One is numerical. Nearly all rivers and streams have an
underlying alluvial system in which its residents never encounter light.
Approximately 15 per cent of the Earth’s land surface is honeycombed with
caves and springs, part of a landscape called karst that is moulded by the
forces of dissolution rather than erosion of rock and sediment. In countries
such as Cuba and Slovenia, this is the predominant landform.
But there is a more profound reason for biologists to study subterranean
biology. Subterranean species can serve as model systems for several
important biological questions. As far as we can determine, it was Poulson
and White (1969) who first made this notion explicit but it is implicit in the
writings of many subterranean biologists. This is a recurring theme through-
out this book, and we list just some of the possibilities here:
• Subterranean ecosystems can serve as models of carbon (rather than
nitrogen and phosphorus) limited ecosystems and ones where most inputs
are physically separated from the community itself.
• Subterranean communities can serve as a model of species interactions
because the number of species is small enough that all pairwise interactions
can be analysed and then combined into a community-wide synthesis.
• The universal feature of loss of structures (regressive evolution) is espe-
cially obvious in subterranean animals, with a clear basis that in turn can
allow for detailed studies of adaptation.
• The possibilities of dispersal of subterranean species are highly con-
strained and so the species (and lineages) can serve as models for vicariant
biogeography.
• The highly restricted ranges and specialized environmental requirements
can serve as a model for the protection of rare and endangered species.
Whatever reasons you have for reading this book, we hope it leads you to a
fascination with subterranean biology, one that lasts a lifetime.
Acknowledgements

The field of subterranean biology is blessed with a strong, cooperative

group of scholars from all over the world, and we could not have written
this book without the help of many of them. We especially thank Peter
Kozel for reading the entire manuscript of the second edition and making
many helpful suggestions. Cene Fišer, Daniel W. Fong, and Mike Slay all
read selected chapters and helped us avoid many mistakes. Several col-
leagues provided photographs and drawings for the first and/or second
editions—Gregor Aljančič, Magda Aljančič, Matej Blatnik, Marie-Jose
Dole-Olivier, Annette Summers Engel, the late Horton H. Hobbs III,
Hannelore Hoch, William R. Jeffery, Arthur N. Palmer, Borut Peric, Slavko
Polak, Megan Porter, Mitja Prelovšek, Nataša Ravbar, Andreas Wessel, Jill
Yager, and Maja Zagmajster. Colleagues also provided us with preprints and
answered sometimes naive questions—Gergely Balázs, Louis Deharveng,
Marie-Jose Dole- Olivier, Stefan Eberhard, David Eme, Annette Summers
Engel, Daniel W. Fong, Franci Gabrovšek, Janine Gibert, Benjamin Hutchins,
Lee Knight, Florian Malard, Georges Michel, Pedro Oromí, Metka Petrič,
Megan Porter, Graham Proudlove, Katie Schneider, Trevor Shaw, Boris
Sket, Peter Trontelj, Rudi Verovnik, and Maja Zagmajster. Franjo Drole of
the Karst Research Institute ZRC SAZU devoted many hours to scanning
and producing diagrams. Maja Kranjc, and later Janez Mulec, in charge of
the magnificent library at the Karst Research Institute, have helped with
our requests for books and journals.
We are especially grateful to the Karst Research Institute ZRC SAZU, espe-
cially the head of the institute, Dr Tadej Slabe and the administrative
assistant, Sonja Stamenković, for making the writing go as smoothly as pos-
sible. Tadej Slabe provided time for TP to work, space for DCC to work, and
an appointment to DCC as Associate Researcher. Financial support was pro-
vided by Ad Futura (Javni sklad Republike Slovenije za razvoj kadrov in
štipendije) to DCC during his stay in Slovenia.
We thank Ian Sherman of Oxford University Press for providing us with the
opportunity to write both editions of the book, Helen Eaton for shepherding
through the first edition, and Bethany Kershaw for shepherding through the
second edition.
x ACKNOWLEDGEMENTS

A project of this magnitude was a burden on both of our families, and we are
especially grateful to our spouses, Gloria Chepko and Miran Pipan, for pro-
viding both understanding and support.
Postojna, Slovenia
April, 2018
 Contents

List of Sites xv

1 The Subterranean Domain 1

1.1 Introduction 1
1.2 Caves 4
1.3 Small-cavity subterranean habitats 15
1.4 Shallow subterranean habitats 17
1.5 Summary 23

2 Sources of Energy in Subterranean

Environments 24
2.1 Introduction 24
2.2 Sources of energy 24
2.3 Summary 40

3 Survey of Subterranean Life 43

3.1 Introduction 43
3.2 Temporary subterranean visitors 43
3.3 Residents of cave entrances 46
3.4 Ecological and evolutionary classifications 48
3.5 Taxonomic review of obligate subterranean species 50
3.6 Subterranean organisms in the laboratory 74
3.7 Collecting stygobionts and troglobionts 75
3.8 Summary 79

4 Ecosystem Function 80
4.1 Introduction 80
4.2 Scale and extent of subterranean ecosystems 81
4.3 Stream reaches 83
4.4 Caves 87
4.5 Karst basins 93
4.6 Summary 96
xii CONTENTS

5 Biotic Interactions and Community Structure 98

5.1 Introduction 98
5.2 Species interactions—generalities 98
5.3 Predator–prey interactions—beetles and cricket eggs in
North American caves 100
5.4 Competition and other interactions in Appalachian cave streams 104
5.5 Morphological consequences of competition 108
5.6 Competition as a result of eutrophication 111
5.7 Community analysis—generalities 112
5.8 Epikarst communities 113
5.9 Interstitial groundwater aquifers 115
5.10 Overall subterranean community structure in
the Jura Mountains 116
5.11 Summary 118

6 Adaptations to Subterranean Life 119

6.1 Introduction 119
6.2 History of concepts of adaptation in subterranean environments 120
6.3 Adaptation in amblyopsid cave fish 124
6.4 Adaptation in the amphipod Gammarus minus 130
6.5 Adaptation in the cave fish Astyanax mexicanus 138
6.6 Experimental studies of adaptation in other subterranean
organisms 143
6.7 How long does adaptation to subterranean life take? 144
6.8 Revisiting the selection–neutrality controversy 145
6.9 Summary 146

7 Colonization and Speciation in Subterranean

Environments 147
7.1 Introduction 147
7.2 Colonization of subterranean environments 149
7.3 What determines success or failure of colonizations? 151
7.4 Allopatric and parapatric speciation 152
7.5 Vicariance and dispersal 158
7.6 Cryptic speciation 165
7.7 Age of lineages 169
7.8 Phylogeography of three different subterranean lineages 170
7.9 Summary 175

8 Geography of Subterranean Biodiversity 179

8.1 Introduction 179
8.2 The struggle to measure subterranean biodiversity 180
 CONTENTS xiii

8.3 Caves as islands 186

8.4 Global species richness 190
8.5 Regional species richness 195
8.6 Summary 205

9 Some Representative Subterranean

Communities 206
9.1 Introduction 206
9.2 Shallow subterranean habitats 207
9.3 Deep non-cave habitats 216
9.4 Cave habitats 218
9.5 Summary 225

10 Conservation and Protection of

Subterranean Habitats 226
10.1 Introduction 226
10.2 Rarity 227
10.3 Other biological risk factors 230
10.4 Threats to the subterranean fauna 231
10.5 Site selection 240
10.6 Protection strategies 243
10.7 Preserve design 244
10.8 Summary 246

Glossary 247
Literature Cited 255
Index 291
List of Sites

A list of sites from 29 countries mentioned in the text. General references to

countries or large regions are omitted. Specific reference to the sites can be
found in the appendix. While most of the sites are caves, there are a number
of specific regions, e.g. Cape Range in Australia, that are listed.

Abkhazia (Georgia)
• Veryovkina

Australia
• Bayliss Cave (Queensland)
• Bundera sinkhole (Western Australia)
• Bungonia Cave (New South Wales)
• Cape Range (Western Australia)
• Pilbara (Western Australia)
• Robe River (Western Australia)
• Sturt Meadows (Western Australia)
• Tantabiddi well (Western Australia)
• Yilgarn (Western Australia)

Austria
• Danube Flood Plain National Park
• Lobau wetlands

Belgium
• Walloon

Bermuda
• Walsingham Cave

Bosnia & Hercegovina

• Dabarska pećina
• Popovo polje
• Trebišnjica River System
• Vjetrenica
xvi LIST OF SITES

Brazil
• Atlantic Coastal Rain Forest
• Lapa da Fazienda Extrema I (Goiás)
• São Mateus Cave (Goiás)

Burma
• Farm caves

China
• Ma San Dong Cave
• Shihua Cave

Croatia
• Krk Island
• Markarova pećina
• Miljacka pećina
• Pincinova jama
• Rupeciča
• Šipun

France
• Ardèche
• Ariège
• Baget basin
• Bellissens
• Canal di Mirabel
• Col des Marrous
• Dorvan-Cleyzieu
• Grand Gravier
• Grotte du Cormoran
• Grotte du Pissoir
• Grotte de Sainte-Catherine
• Heraut
• Isère River
• Jura Mountains
• Lachein Creek
• Las Hountas
• Rhône River at Lyon
• Roussilon
• Tour Laffont

Germany
• Aach Spring
• Segeberger Höhle
 LIST OF SITES xvii

Indonesia
• Batu Lubang (Halmahera)
• Gua Sulukkan (Sulawesi)
• Niah Caves (Sarawak)

Israel
• Ayalon Cave

Italy
• Abisso di Trebiciano
• Grotta Azzurra
• Grotta di Frasassi
• Lessinian Mountains

Malaysia
• Lubang Nasib Bagus (Sarawak)
• Sarang karst (Borneo)
• Subis karst (Borneo)

Mexico
• Cueva Chica
• Cueva de la Curva
• Cueva de Los Sabinos
• Cueva da Villa Luz
• Cueva de El Pachón
• Sierra del Abra
• Sistema Zacatón
• Sotano de al Tinaja
• Sotano de las Golandrinas

Montenegro
• Dormitor National Park

Papua New Guinea

• Kavakuna Matali system

Phillipines
• Bohol Island caves
• Montalban caves
• Taninthayri caves

Portugal
• Azores lava tubes
• Serra da Estrela
xviii LIST OF SITES

Romania
• Peştera Movile
• Peştera Urşilor

Slovakia/Hungary
• Baradla/Domica

Slovenia
• Črna jama
• Huda luknja
• Jelševnik
• Kompolska jama
• Krim
• Križna jama
• Mejama
• Otovski breg
• Logarček
• Malo okence
• Paka karst
• Pivka jama
• Pivka River
• Planinska jama
• Postojna–Planina Cave System
• Postojnska jama
• Rak River
• Šica–Krka system
• Škocjanske jame
• Tular

Spain
• Cantabrica
• Cueva del Felipe Reventón (Canary Islands)
• Cueva del Mattravies
• Cueva del Naciemento del Arroyo de San Blas
• Cueva del Viento (Canary Islands)
• Jameos del Agua (Canary Islands)

Thailand
• Central Plain
• Tham Chiang Dao
• Tham Phulu
• Tham Thon

Ukraine
• Zoloushka Cave
 LIST OF SITES xix

United Kingdom
• Otter Hole Cave (Wales)
• Swildon’s Hole (England)

United States
• Alpena Cave (West Virginia)
• Blue Lake Rhino Cave (Oregon)
• Bracken Cave (Texas)
• Carlsbad Caverns (New Mexico)
• Cave Spring Cave (Arkansas)
• Cesspool Cave (Virginia)
• Classic Cave (New Mexico)
• Coldwater Cave (Iowa)
• Columbia River basalt (Washington)
• Devil’s Hole (Nevada)
• Dillion Cave (Indiana)
• Edwards Aquifer (Texas)
• Fern Cave (Alabama)
• Fisher Cave (Missouri)
• Flathead River (Montana)
• Floridan Aquifer (Florida)
• Glenwood Caverns (Colorado)
• Greenbrier Valley (West Virginia)
• Hellhole (West Virginia)
• Hering Cave (Alabama)
• Hidden River Cave (Kentucky)
• Howe Caverns (New York)
• Inner Space Caverns (Texas)
• Kartchner Caverns (Arizona)
• Kazumura Cave (Hawaii)
• Lanikai Cave (Hawaii)
• Lava Tubes National Monument (California)
• Lechuguilla Cave (New Mexico)
• Limrock Cave (Alabama)
• Logan Cave (Arkansas)
• Lower Kane Cave (Wyoming)
• Lower Potomac (District of Columbia)
• Mammoth Cave (Kentucky)
• McClean’s Cave (California)
• Ogalalla Aquifer (Nebraska)
• Old Mill Cave (Virginia)
• Organ Cave (West Virginia)
• Parker Cave (Kentucky)
• Pless Cave (Indiana)
• Robber Baron Cave (Texas)
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