Physiology of Polar Fishes

401 Pages·2005·6.98 MB·English

by  Anthony P. Farrell

CONTENTS
CONTRIBUTORS ix
PREFACE xi
1.
The Arcticand Antarctic Polar Marine Environments
Arthur L. DeVries andJohn F. SteVensen
I. Introduction 1
II. ThePolarMarineSystem 2
III. PhysicalandChemicalPropertiesofPolarSeawater 5
IV. PrimaryProductionandSeasonalLightAvailability 7
V. TheArcticMarineRegion 8
VI. TheAntarcticMarineRegion 12
VII. GlacialandGeologicalHistoryofthePolarRegionsanditsRelationto
PolarFishFaunas 19
References 22
2.
Systematics ofPolarFishes
Peter RaskMøller, Jørgen G. Nielsen, and M.EricAnderson
I. Introduction 25
II. Biogeography 30
III. AClassificationofFishesOccurringinArcticandAntarcticRegions,
withanAnnotatedListofFishFamiliesandNoteson
RevisionsandPhylogeneticHypotheses 33
References 69
3.
Metabolic Biochemistry: Its Role in Thermal Tolerance and in
the Capacities of Physiological andEcological Function
H. O. Po¨rtner,M.Lucassen, andD. Storch
I. Introduction 79
II. ColdAdaptation:PerformanceLevelsandModeofMetabolism 88
v
vi
CONTENTS
III. MembraneFunctionsandCapacities:ConstraintsinIonand
Acid–BaseRegulation 113
IV. MolecularPhysiologyofMetabolicFunctions 120
V. Trade‐OVsinEnergyBudgetsandFunctionalCapacities:
EcologicalImplications 128
VI. Summary 138
References 139
4.
AntifreezeProteinsandOrganismalFreezingAvoidanceinPolarFishes
ArthurL. DeVriesand C.‐H. Christina Cheng
I. Introduction 155
II. FreezingChallengetoHyposmoticTeleostFishinIce‐LadenFreezing
MarineEnvironments 157
III. FreezingAvoidanceStrategies 158
IV. OrganismalFreezingPoints 161
V. TypesofAntifreezeProteins 163
VI. NoncolligativeLoweringoftheFreezingPointbyAntifreezeProtein 168
VII. EnvironmentalIceandExogenous/EndogenousIceinPolarFish 174
VIII. TheIntegumentasaPhysicalBarriertoIcePropagation 179
IX. SynthesisandDistributionofAntifreezeProteinsinBodyFluids 181
X. StabilityofUndercooledFishFluidsLackingAntifreezeProteins 185
XI. SerumHysteresisLevelsandEnvironmentalSeverity 187
XII. MechanismofOrganismalFreezeAvoidance 191
References 193
5.
Respiratory Systemsand Metabolic Rates
JohnF. SteVensen
I. TheRespiratorySystem 203
II. MetabolicRates 214
III. Conclusion 231
References 233
6.
The Circulatory System and its Control
Michael Axelsson
I. TheCardiovascularSystemintheCold 239
II. AnatomyandControloftheFishHeart 251
III. TheBranchialandSystemicVasculature 262
IV. IntegratedCardiovascularResponses 268
V. Summary 272
References 273
vii
CONTENTS
7. Blood‐Gas Transport and Hemoglobin Function in Polar Fishes:
Does Low Temperature Explain Physiological Characters?
R. M.G. Wells
I. Introduction 281
II. MechanismofEvolutioninPhysiologicalSystems 283
III. ExpressionandSignificanceofMultipleHemoglobinComponents 284
IV. FunctionalPropertiesofHemoglobins 291
V. RespiratoryFunctionsofBlood:RoleofBloodinMaintainingHomeostasis 296
VI. ReflectionsandPerspectives 302
References 306
8.
Antarctic Fish Skeletal Muscle and Locomotion
William Davison
I. Introduction 317
II. BasicFishMuscleAnatomy 319
III. MechanicalandPhysiologicalPropertiesofIsolatedMuscle 327
IV. ProtectingtheCell 329
V. ExerciseandEnergySupply 330
VI. Swimming 334
VII. ExerciseandTemperature 337
Reference 341
9.
The NervousSystem
JohnMacDonaldand John Montgomery
I. Introduction 351
II. NervousSystem:StructureandFunction 353
III. SensoryPhysiologyofPolarFishes 366
IV. ConcludingRemarks 375
References 378
INDEX 385
OTHERVOLUMESINTHESERIES 395
CONTRIBUTORS
Thenumbersinparenthesesindicatethepagesonwhichtheauthors’contributionsbegin.
M. ERIC ANDERSON (25), The South African Institute for Aquatic
Biodiversity, J.L.B. Smith Institute of Ichthyology, South Africa
MICHAEL AXELSSON (239), Department of Zoology/Zoophysiology,
University of Go¨teborg, Go¨teborg, Sweden
C.‐H. CHRISTINA CHENG (155), Department of Animal Biology, University
of Illinois, Urbana-Champaign, Illinois
WILLIAM DAVISON (317), School of Biological Sciences, University of
Canterbury, Christchurch, New Zealand
ARTHURL.DEVRIES(1,155),DepartmentofAnimalBiology,Universityof
Illinois, Urbana‐Champaign, Illinois
M. LUCASSEN (79), Alfred‐Wegener‐Institut, fu¨r Polar‐ und Meeres-
forschung, Bremerhaven, Germany
JOHN MCDONALD (351), School of Biological Sciences, The University of
Auckland, Auckland, New Zealand
JOHN MONTGOMERY (351), Leigh Marine Laboratory, School of Biological
Sciences, The University of Auckland, Auckland, New Zealand
PETER RASK MØLLER (25), Zoological Museum, University of Copenhagen,
Copenhagen, Denmark
JØRGEN G. NEILSEN (25), Zoological Museum, University of Copenhagen,
Copenhagen, Denmark
H. O. PO¨RTNER (79), Alfred‐Wegener‐Institut, fu¨r Polar‐ und Meeres-
forschung, Bremerhaven, Germany
JOHN F. STEFFENSEN (1, 203), Marine Biological Laboratory, University of
Copenhagen, Helsingør, Denmark
ix
x
CONTRIBUTORS
D. STORCH (79), Alfred‐Wegener‐Institut, fu¨r Polar‐ und Meeresforschung,
Bremerhaven, Germany
R. M. G. WELLS (281), School of Biological Sciences, The University of
Auckland, Auckland, New Zealand
PREFACE
Comparedwiththetemperatureextremesthatprevailinterrestrialenvi-
ronmentsoftheArcticandAntarctic,thepolaraquaticenvironmentprovidesa
relatively stable temperature for animals. Nevertheless, the temperatures
experiencedbypolarfishesintheArcticandAntarcticenvironmentscanbe
sub‐zeroandthesetemperaturesarecertainlyfrigidintermsofphysiological
processes,especiallywhencomparedwithtropicalfishes(seevolume21ofthe
Fish Physiology series). Despite these frigid temperatures, polar aquatic
environments are remarkably productive and support large populations of
birds and mammals that feed extensively upon fish. This tells us that polar
fishes exploit these environments either seasonally through acclimatization
processesorareyearroundresidentswithspecialadaptationsforfrigidwater
temperatures,whichareespeciallychallengingduringthewinter:watertem-
peraturereachesanadir;gasexchangethroughtheiceislimited;andthelackof
sunlightlimitsphotosyntheticactivityatthebottomofthefoodchain.
Theoverarchingfocusofthisbookisonthephysiologicaladaptationsthat
evolvedtoallowcertainfishestoexploittheArcticandAntarctic.Therefore,the
primaryquestionansweredbyeachauthoris:Whatisspecialaboutthephysiol-
ogyoffishfromthestenothermalArcticandAntarcticenvironments?Itturns
outthatcertainaspectsofthephysiologyofpolarfishescanshowsomeremark-
ableanduniquefeatures.Forexample,somepolarfishhavenoredbloodcells;
thebloodisstraw‐coloredratherthantheusualredcolorofvertebrateblood.
Similarly, some polar fishes have pale‐colored heart muscle in which the red
intracellularrespiratorypigmentmyoglobinisnotexpressed.Inotherwaysthe
physiology of polar fishes is normal compared with temperate species. For
example,extensiveandsomewhatcontroversialearlierliteraturehadsuggested
thatpolarfisheshadanelevatedmetabolicrate–termedmetaboliccompensa-
tion.However,morecarefulmeasurementsofmetabolicrateinavarietyofpolar
fisheshaveshownthatthemetaboliccompensationtheoryshouldbeabandoned;
theearlierstudiesappeartohavereportedelevatedmetabolicratesfromstressed
fish.Anunwrittenmessagehereisthatresearchonthephysiologyofpolarfishes
presentsdiYculttechnicalchallenges.Indeed,someaspectsoftheirphysiology
aremorediYculttoworkonthanothers.Therefore,althoughanattemptwas
xi
xii
PREFACE
madetoprovidebroadcoverageofphysiologicalprocesses,certainaspectsof
physiologyaremoreamplyrepresentedthanothersinthechaptersthatfollow.
Thisunevencoverageisatruereflectionoftheknowledgebase.
AmorediYcultcentralquestionthattheauthorstriedtoanswerwas:are
therecommonthemestothephysiologyforthesefishesthatlivepolesapart
butinfrigidwater?Itisevidentthatthemajorityoftheknowledgebaseonthe
physiology of polar fishes is for a limited number of Antarctic species, in
particular the notothenioids. The physiology of Arctic species is woefully
under‐represented.Whileacomprehensiveanswertothepossibilityofacon-
vergentevolutionofpolarsurvivalstrategiesmustawaitfutureresearch,itis
clearthatthephysiogeographiesoftheArcticandAntarcticshowfundamen-
taldiVerences.Sinceitisthephysicalenvironmentthatshapesthephysiology
of animals, at least from the perspective of evolutionary adaptation, the
greater geographic isolation of Antarctic waters may possibly explain the
more extreme physiological adaptations seen for certain Antarctic fishes,
which are, asyet, undiscovered inArcticfishes.
We know that certain eurythermal fishes can acclimate to temperatures
experiencedinthepolarenvironments.Also,fishindeeplakesanddeepseas
(seevolume16oftheFishPhysiologyseries)facestenothermalenvironments
close to the upper temperature range of the polar environments. Therefore,
this observation raises a third question that each author addressed: how
do polar fishes diVer from those fishes that are more eurythermal and can
acclimatize to severe cold? To address this question, authors included brief
comparisons with theeurythermal fishes.
As this book reveals,our state of knowledge on the physiology of polar
fishesislimitedandfragmentary,andgreatlyfavoursoceanoverfreshwater
species despite the existence of numerous deep polar lakes. Also, human
nature(andoftenresearchfunding)issuchthatwetendtostudyfascinating
butextremeforms,andifinformationislimited,abiasmayappearinourview
ofthegeneralphysiologyofanimals,suchaspolarfishes,ifindeedcommon
groundcanbefound.Consequently,becausemuchremainstobediscovered,
many ofthe authors’ conclusionsare cautious ones.
Onethingiscertain,however.Polartemperaturesarewarming,aphenom-
enonthatisespeciallyevidentintheCanadianArctic.Towhatdegreethiswill
challengeandchangeArcticfishesisunknown,butthechangeshavealready
started.IrecentlyparticipatedinaresearchexpeditiontoGreenland,hoping
tostudyArcticcodatthesouthernendoftheirknowngeographicdistribu-
tion.However,wewereunabletocaptureevenoneArcticcodattheDanish
ArcticMarineStation.Apparently,theseawatertemperatureinthislocation
is now too warm for Arctic cod. Their southern distribution is now further
north. Clearly, we had arrived afew yearstoo late.
AnthonyP. Farrell
Vancouver, May2005
1
THE ARCTIC AND ANTARCTIC POLAR
MARINE ENVIRONMENTS
ARTHUR L. DEVRIES
JOHNF. STEFFENSEN
I. Introduction
II. ThePolarMarineSystem
III. PhysicalandChemicalPropertiesofPolarSeawater
A. EVectofTemperatureontheDensityandViscosityofSeawater
B. SalinityandFreezingofPolarWaters
C. OxygenSolubilityandTemperature
IV. PrimaryProductionandSeasonalLightAvailability
V. TheArcticMarineRegion
VI. TheAntarcticMarineRegion
A. TheAntarcticContinentalShelf
B. McMurdoSound
VII. GlacialandGeologicalHistoryofthePolarRegionsanditsRelationtoPolarFishFaunas
I. INTRODUCTION
Theoverarchingfocusofthisbookonpolarfishesisonthephysiological
adaptations that evolved to allow certain fishes to exploitthe frigid and yet
biologically productive Arctic and Antarctic marine regions. Although the
availableinformationmaylimitthescopeofanygivenchapter,theintentis
thatthreecentralthemesrunthrougheachchapterandthevolumeasawhole:
(cid:1) What is special about the physiology of fish from the stenothermal
Arctic and Antarctic environments?
(cid:1) Are there common themes to the physiology of these fishes that live
polesapartbutinfrigidwater?(Ifnot,whatmightbethebasisforthe
diVerences?)
1
ThePhysiologyofPolarFishes:Volume22 Copyright#2005ElsevierInc.Allrightsreserved
FISHPHYSIOLOGY DOI:10.1016/S1546-5098(04)22001-5
2
ARTHURL.DEVRIESANDJOHNF.STEFFENSEN
(cid:1) HowdothesefishesdiVerfromthosefishesthataremoreeurythermal
and can acclimatize to severe cold?
With respect to the second of these questions, and as will become
apparentineachchapter,considerationmustbegiventotheimportantfact
that the Arctic and Antarctic Oceans diVer in their physiogeographic char-
acteristics, despite that both share many features beyond being just frigid.
Considerationofphysiogeographic characteristicsisimportantfortworea-
sons.Foremost,itisthephysicalenvironmentthatshapesthephysiologyof
animals, from the perspectives of both evolutionary adaptation and accli-
matory responses to short‐term environmental changes. Second, the infor-
mation base available to authors is limited and fragmentary. Therefore,
comparisonsbothbetweentheArcticandAntarcticandwithineachofthese
environments cannot always be made evenly, so authors, out of necessity,
maycautionthereaderaboutsomeofthegeneralitiestheymake.Inviewof
this, we open this volume with a succinct comparison of the physiogeo-
graphic characteristics of the Arctic and Antarctic marine systems to
illustratesimilarities and diVerences.
II. THE POLAR MARINE SYSTEM
The northern and southern polar marine regions have some striking
physiogeographic diVerences but share a number of climatic and oceano-
graphicfeatures.TheArcticOceanismostlysurroundedbycontinentalland
massesandconnectstotheAtlanticandPacificOceansthroughanumberof
cold shallow seas and narrow passageways separating the continental land
massesandArcticislands(Figure1.1).TheArcticOceanisanoceanicbasin
with restricted circulation and a large input of Atlantic Ocean water that
lacksoceanicfronts.Theoutflowofcoldsalinewater islargely through the
Fram Strait into the shallow Greenland Sea where it flows southwards as a
distinct water mass. In contrast, Antarctica is an ice‐covered continent
surrounded by a vast Southern Ocean that is separated from the Atlantic,
Pacific, and Indian Oceans by a distinct oceanographic front but neverthe-
lessexchangeslargeamountsofheatandwaterwiththesurroundingoceans
(Smith and Sakshaug, 1990)(Figure 1.2).
Both marine regions mostly freeze during the winter and their surface
watersareattheirfreezingpoint((cid:2)1.8to(cid:2)1.9(cid:3)C);however,muchoftheice
melts during the summer. The freezing conditions of the marine waters are
largely an expression of the cold climates of the regions. Also, during their
respective winter season, both regions experience long periods of darkness.
In the high latitudes, the sun may be below the horizon for as much as