Table Of ContentAdvances in Comparative and Environmental Physiology 8
Editor-in-Chiej
R. Gilles, Liege
Editorial Board
P. 1. Butler, Birmingham
R. Greger, Freiburg
Ch. P. Mangum, Williamsburg
G. N. Somero, La lolla
K. Takahashi, Tokyo
R. E. Weber, Aarhus
Volumes already published
Vol. 1: NaCI Transport in Epithelia
Edited by R. Greger (1988)
Vol. 2: From the Contents: Hibernation - Vapor Absorption
Nutrient Transport - Stable Pollutants (1988)
Vol. 3: Molecular and Cellular Basis of Social Behavior in Vertebrates
Edited by 1. Balthazart (1989)
Vol. 4: Animal Adaptation to Cold
Edited by L. C. H. Wang (1989)
Vol. 5: From the Contents: Osmoregulation - Chemoreception
Temperature - Spectroscopy - Metalloproteins
Maternal-Fetal Relationships (1989)
Vol. 6: Vertebrate Gas Exchange: From Environment to Cell
Edited by R. G. Boutilier (1990)
Vol. 7: From the Contents: Protein Turnover -
Xenobiotic Metabolism Lipoproteins (1991)
Vol. 8: From the Contents: Dormancy in Aquatic Invertebrates - Root Effect
Red Blood Cell Functions in Fish- Diving Mammals (1991)
Volumes in preparation
Vol. 9: Volume and Osmolality Control in Animal Cells
Edited by R. Gilles. E. K. Hoffman. and L. Bolis
Advances in
Comparative
and Environmental
Physiology 8
With Contributions by
M. A. Castellini . B. Fievet . s. C. Hand· R. Motais
B. Pelster· R. E. Weber
With 50 Figures
Springer-Verlag
Berlin Heidelberg New York
London Paris Tokyo
Hong Kong Barcelona
ISBN-13 :978-3-642-75902-4 e-ISBN-13 :978-3-642-75900-0
DOl: 10.1007/978-3-642-75900-0
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© Springer-Verlag Berlin Heidelberg 1991
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Foreword to the Series
The aim of the series is to provide comprehensive, integrated reviews giv
ing sound, critical, and provocative summaries of our present knowledge
in environmental and comparative physiology, from the molecular to the
organismic level.
Living organisms have evolved a widespread range of basic solutions
to cope with the different problems, both organismal and environmental,
with which they are faced. A clear understanding of these solutions is
of course of fundamental interest for all biologists, zoologically or med
ically oriented. They can be best comprehended in the framework of the
environmental and/or comparative approaches. These approaches de
mand either wide surveys of animal forms or a knowledge of the specific
adaptive features of the species considered. This diversity of require
ments, both at the conceptual and technological level, together with the
fact that physiology and biochemistry have long been mainly devoted to
the service of medicine, can account for the fact that these approaches
emerged only slowly amongst the other new, more rapidly growing disci
plines of the biological sciences.
The field has now gained the international status it deserves and the
organization of a series devoted to it appeared timely to me in view of
its actual rapid development and of the interest it arouses for a growing
number of biologists, physiologists, and biochemists, independently of
their basic, major orientation.
Liege, Belgium Raymond Gilles
List of Editors
Editor-in-Chief
R. Gilles
Laboratory of Animal Physiology
University of Liege
22, Quai Van Beneden
4020 Liege, Belgium
Editorial Board
·P. J. Butler G.N. Somera
School of Biological Sciences Scripps Institution
University of Birmingham of Oceanography
P.O. Box 363 University of California
Birmingham B 15 2TT, England La Jolla, CA 92093, USA
R. Greger K. Takahashi
Physiologisches Institut Zoological Institute
der Universitat Freiburg Faculty of Sciences
Lehrstuhl II University of Tokyo
Hermann-Herder-Strasse 7 Hongo, Tokyo 113, Japan
7800 Freiburg, FRG
R.E. Weber
Ch. P. Mangum Zoophysiology Laboratory
Department of Biology University of Aarhus
The College of William & Mary Building 131
Williamsburg, VA 23185, USA 8000 Aarhus C, Denmark
Those interested in contributing to this series should contact Professor
R. Gilles or one of the Series Editors. Review proposals should include
a short outline - and a Table of Contents - briefly defining the aims
and scopes of the review.
Contents
Chapter 1
Metabolic Dormancy in Aquatic Invertebrates
S. C. Hand
1 Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
2 Phylogenetic Survey of Dormancy
and Associated Environmental Cues ..................... 4
3 Metabolic Arrest During Anaerobic Dormancy. . . . . . . . . . .. 21
4 Coordinated Arrest of Development Under Anoxia ........ 28
5 Anhydrobiosis: Dehydration-Induced Quiescence .......... 30
6 Estivation in Gastropods ., . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 37
7 Directions for Future Study. . . . . . . . . . . . . . . . . . . . . . . . . . . .. 40
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 40
Chapter 2
The Physiology of the Root Effect
B. Pelster and R. E. Weber
1 Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 51
2 Characterization of the Root Effect . . . . . . . . . . . . . . . . . . . . .. 59
3 Root Effect and Swim bladder Function .................. 63
4 Root Effect and Ophthalmic Oxygen Secretion ............ 67
5 Adrenergic Effects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 70
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 72
Chapter 3
Na +/ H+ Exchanges and Red Blood Cell Functions in Fish
B. Fievet and R. Motais
1 Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 79
2 Evidence for Na +/ H+ Exchanges in the Erythrocytes
of Hypoxic Trout ..................................... 82
3 Effects of Na +/ H + Exchanges on the Acid Base Balance
of the Blood ........................................ " 86
VIII Contents
4 Effects of Na +/ H+ Exchanges on Erythrocyte pH ......... 91
5 Effects of Na +/ H + Exchanges on Respiratory Gas Transport 97
6 Other Physiological Situations ........................... 100
7 Concluding Remarks ................................... 101
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 102
Chapter 4
The Biology of Diving Mammals: Behavioral, Physiological,
and Biochemical Limits
M. A. Castellini
1 Introduction .......................................... 105
2 The Physiological and Biochemical Limits to Diving ....... 106
3 The Field as a Natural Laboratory ...................... 112
4 Diving Efficiency . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 118
5 "Diving" on Land-Sleep Apnea in Seals .................. 124
6 What is "Normal" for a Diving Mammal? ................ 129
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 131
Subject Index. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 135
Chapter I
Metabolic Dormancy in Aquatic Invertebrates
Steven C. Hand
Contents
Introduction 2
1.I Environmentally Induced Quiescence Versus Endogenous Diapause ................... . 2
1.2 Biological Rationale ........................................................... . 3
2 Phylogenetic Survey of Dormancy and Associated Environmental Cues ................ . 4
2.1 Unicellular Organisms ......................................................... . 4
2.2 Sponges ...................................................................... . 4
2.3 Cnidarians ................................................................... . 7
2.4 Turbellarians ................................................................. . 8
2.5 Aschelminths ................................................................. . 8
2.6 Molluscs ...................................................................... 12
2.7 Annelids ...................................................................... 15
2.8 Crustaceans ................................................................... 15
2.9 Bryozoans. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 19
3 Metabolic Arrest During Anaerobic Dormancy ..................................... 21
3.1 A Role for Intracellular pH ...................................................... 21
3.2 Suppression of Energy Flow Quantified with Microcalorimetry ........................ 22
3.3 Biochemical Coupling of Acidosis to the Arrest of Trehalose Catabolism ................ 24
4 Coordinated Arrest of Development Under Anoxia .................................. 28
4.1 Subcellular Differentiation During Preemergence Development in Artemia
and its Reversible Blockage ...................................................... 28
4.2 Disruption of Protein Synthesis: Cytochrome c Oxidase .............................. 29
5 Anhydrobiosis: Dehydration-Induced Quiescence ................................... 30
5.1 Patterns of Metabolic Suppression: Respirometric and Calorimetric Measurements ....... 30
5.2 Biochemical Correlates of Cellular Dehydration State ................................ 32
5.2.1 Nematodes and Tardigrades ..................................................... 32
5.2.2 Artemia Embryos ............................................................... 34
6 Estivation in Gastropods ........................................................ 37
6.1 Metabolic Patterns. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 37
6.2 Catabolism of Energy Reserves and Accumulation of Urea ............................ 38
6.3 Potential Mechanisms of Metabolic Arrest. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 39
7 Directions for Future Study ...................................................... 40
References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 40
Department of EPO Biology, University of Colorado, Boulder, Colorado 80309-0334, USA
Advances in Comparative and Environmental Physiology, Vol. 8
© Springer-Verlag Berlin Heidelberg 1991
2 Steven C. Hand
We sat beside the little pool and watched the tree-frogs and the horsehair worms and the
water-skaters, and had wondered how they got there, so far from water. It seemed to us that
life in every form is incipiently everywhere waiting for a chance to take root and start
reproducing; eggs, spores, seeds, bacilli ~ everywhere. Let a raindrop fall and it is crowded
with the waiting life .... And we, seeing the desert country, the hot waterless expanse, and
knowing how far away the nearest water must be, say with a kind ofd isbelief, "How did they
get clear here, these little animals?" And until we can attack with our poor blunt weapon
of reason that causal process and reduce it, we do not quite believe in the horsehair
worms .....
From Sea o[Cortez. John Steinbeck and Edward Ricketts, 1941
1 Introduction
One major approach used by invertebrates for coping with extreme environmental
conditions is to enter states of metabolic and developmental dormancy. The pos
session of a latent or resting stage is a common occurrence in the life cycle of
organisms inhabiting inconsistent or ephemeral environments, and this phen
omenon has been a source of long-standing speculation and fascination (cf. van
Leeuwenhoek 1702). Considering the remarkable habitat diversity that exists
among aquatic invertebrates, it is not surprising that the distribution of dormancy is
broadly scattered phylogenetically. Resting stages have now been reported in
virtually every major phylum of invertebrates, with the notable exception of
Echinodermata. In some taxa, mature adult forms have the ability to enter states of
rest, while in others, specialized resting forms are common only during earlier stages
oflife cycles.
Considerable effort on the part of numerous invertebrate zoologists has been
directed toward describing the environmental conditions that induce dormancy,
recording both the length and the seasonal timing of these bouts, and relating this
information to the life history strategy of the organism. Only more recently have
investigators begun tackling the physiological and biochemical mechanisms by
which metabolic processes of invertebrates are suppressed and then later reactivated
in response to environmental change. It is becoming clear that multiple solutions are
employed by different species, and even by different tissues within a species. The
purpose of this review is to relate the environmental and life history observations to
the growing body of information about the mechanisms governing reversible bouts
of dormancy. For the most part I will focus on aquatic invertebrates, the exception
being pulmonate snails, where information about regulatory mechanisms will come
from both aquatic and terrestrial forms. The voluminous data base on insect
dormancy has been reviewed thoroughly in recent volumes (e.g., Tauber et al. 1986;
Danks 1987) and will not be treated here.
1.1 Environmentally Induced Quiescence Versus Endogenous Diapause
As pointed out previously by other authors, the very term "dormancy" invites
controversy (Bushnell 1974). Undoubtedly, a portion of the confusion arises from
the fact that, in nature or in laboratory settings, the same organism may show a
