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Comparative Biochemistry and Physiology Part A 132(2002) 739–761

1095-6433/02/$ - see front matter� 2002 Published by Elsevier Science Inc.PII: S1095-6433Ž02.00045-4

ReviewClimate variations and the physiological basis of temperature

dependent biogeography: systemic to molecular hierarchy of thermaltolerance in animals�

H.O. Portner*¨

Alfred-Wegener-Institut fur Polar- und Meeresforschung, Okophysiologie, Postfach 12 01 61, D-27515 Bremerhaven, Germany¨¨

Received 2 May 2001; received in revised form 17 September 2001; accepted 30 October 2001

Abstract

The physiological mechanisms limiting and adjusting cold and heat tolerance have regained interest in the light ofglobal warming and associated shifts in the geographical distribution of ectothermic animals. Recent comparative studies,largely carried out on marine ectotherms, indicate that the processes and limits of thermal tolerance are linked with theadjustment of aerobic scope and capacity of the whole animal as a crucial step in thermal adaptation on top of paralleladjustments at the molecular or membrane level. In accordance with Shelford’s law of tolerance decreasing whole animalaerobic scope characterises the onset of thermal limitation at low and high pejus thresholds(pejussgetting worse). Theaerobic scope of an animal indicated by falling oxygen levels in the body fluids and or the progressively limited capacityof circulatory and ventilatory mechanisms. At high temperatures, excessive oxygen demand causes insufficient oxygenlevels in the body fluids, whereas at low temperatures the aerobic capacity of mitochondria may become limiting forventilation and circulation. Further cooling or warming beyond these limits leads to low or high critical thresholdtemperatures(T ) where aerobic scope disappears and transition to an anaerobic mode of mitochondrial metabolism andc

progressive insufficiency of cellular energy levels occurs. The adjustments of mitochondrial densities and their functionalproperties appear as a critical process in defining and shifting thermal tolerance windows. The finding of an oxygenlimited thermal tolerance owing to loss of aerobic scope is in line with Taylor’s and Weibel’s concept of symmorphosis,which implies that excess capacity of any component of the oxygen delivery system is avoided. The present studysuggests that the capacity of oxygen delivery is set to a level just sufficient to meet maximum oxygen demand betweenthe average highs and lows of environmental temperatures. At more extreme temperatures only time limited passivesurvival is supported by anaerobic metabolism or the protection of molecular functions by heat shock proteins andantioxidative defence. As a corollary, the first line of thermal sensitivity is due to capacity limitations at a high level oforganisational complexity, i.e. the integrated function of the oxygen delivery system, before individual, molecular ormembrane functions become disturbed. These interpretations are in line with the more general consideration that, as aresult of the high level of complexity of metazoan organisms compared with simple eukaryotes and then prokaryotes,thermal tolerance is reduced in metazoans. A similar sequence of sensitivities prevails within the metazoan organism,with the highest sensitivity at the organismic level and wider tolerance windows at lower levels of complexity. However,the situation is different in that loss in aerobic scope and progressive hypoxia at the organismic level define the onsetof thermal limitation which then transfers to lower hierarchical levels and causes cellular and molecular disturbances.Oxygen limitation contributes to oxidative stress and, finally, denaturation or malfunction of molecular repair, e.g. duringsuspension of protein synthesis. The sequence of thermal tolerance limits turns into a hierarchy, ranging from systemicto cellular to molecular levels.� 2002 Published by Elsevier Science Inc.

Keywords: Air breather; Cold adaptation; Critical temperatures; Geographical distribution; Law of tolerance; Mitochondria; Pejustemperatures; Proton leakage; Standard metabolic rate; Water breather; Bird; Bivalve; Crab; Fish; Mammal; Reptile; Squid; Worm

� This paper was submitted as part of the SEB Canterbury 2001 Meetings, 2–6 April 2001.*Tel.: q49-471-4831-1307; fax:q49-471-4831-1149.E-mail address: [email protected](H.O. Portner).¨

740 H.O. Portner / Comparative Biochemistry and Physiology Part A 132 (2002) 739–761¨

Fig. 1. Schematic depiction of the ranges of thermal tolerancein marine ectotherms(invertebrates and fish) in a latitudinalcline (modified after Portner, 2001). The preliminary diagram¨ignores the difference between climate regimes in Northern andSouthern hemispheres. Seasonal shifts of tolerance windowsoccur in temperate zone species. Note the narrowing of thetolerance range in polar, esp. Antarctic species(see text).

1. Introduction

Oscillations in the earth‘s climate lead to asso-ciated fluctuations in the temperature regimes ofmany marine and terrestrial ecosystems. Conse-quences in many marine ecosystems includechanges in the timing of reproduction as well aschanges in reproductive success, recruitment,growth performance and mortality of species andfinally, changes in their geographical distribution.Accordingly, impacts of decadal-scale variationsby the coupled ocean–atmosphere system onmarine communities and populations have beenwell documented(Cushing, 1982; Beamish, 1995;Bakun, 1996). Examples can be found amonginvertebrates(Southward et al., 1995) but alsoamong fishes where temperature related trends instocks of fish, e.g. North Sea cod(Dippner, 1997;O’Brien et al., 2000) or Pacific salmon(Klyash-torin, 1997) reflect the general fact that ectotherm-ic animal species are adapted to and depend uponmaintenance of the characteristic temperature win-dow of their natural environment. Climate changeswill have opposite effects on populations at thenorthern and southern edges of their distribution.In contrast to marine mammals and birds, noectothermic species is known to occur over thewidest temperature ranges possible across latitudesbetween polar and tropical areas. Accordingly,thermal tolerance windows differ between speciesdepending on the range of environmental temper-ature. An overview of thermal tolerance ranges oftropical, temperate and polar bivalves and otherectotherms, compiled by Peck and Conway(2000), suggests that tolerance windows are widerin tropical and temperate species than in polarstenotherms. This leads to the question whethertrue stenothermality really exists except in thecold. Fig. 1 indicates that adaptation to tempera-tures below a threshold value of approximately 88C leads to a narrowing of the tolerance window.This strongly suggests that life in the cold is asevere challenge to the organism and forces it totruly specialise in living at low temperatures.Eurytherms tolerate wider temperature fluctuationand, in temperate zones, are able to dynamicallyshift tolerance windows between summer and win-ter temperature regimes. Nonetheless, they stillspecialise on a characteristic thermal environment.As life in warm waters is likely to reflect theoriginal evolutionary situation(Arntz et al., 1994),the capability of surviving seasonal or permanent

cold must be considered an evolutionary accom-plishment rather than a general characteristic of alllife forms. The contribution of temperature chang-es to climate dependent mass extinction and thedrop in biodiversity in a temperature cline towardshigher (Northern) latitudes would support thisconclusion(cf. Portner, 2001, for review).¨Physiological acclimatisation to wide tempera-

ture windows correlates with increasing geneticdifferentiation visible already between populationsof the same species throughout a latitudinal oraltitudinal cline (Hummel et al., 1997; Dahlhoffand Rank, 2000). The reasons for the thermalspecialisation of animals, i.e. the factors determin-ing and limiting temperature related geographicaldistribution need to be identified. The presentpaper summarises recent developments of a con-cept that may support an understanding of thephysiological basis of temperature dependent bio-geography, esp. in ectotherms. Previous data col-lected in various groups of predominantly marinewater breathing but also in air breathing ectotherms(annelids, sipunculids, molluscs like bivalves andcephalopods, crustaceans, fishes, terrestrial arthro-pods and reptiles) indicate that limited oxygenavailability and aerobic scope are crucial in limit-ing thermal tolerance. The relative stability of seawater compared with terrestrial and fresh watertemperatures makes animals from the marine envi-

741H.O. Portner / Comparative Biochemistry and Physiology Part A 132 (2002) 739–761¨

ronment an excellent group to study the relevanceof temperature on a large global scale and toelaborate the principles of thermal tolerance in amuch clearer way than would be possible incomparisons of eurythermal species on smallerlatitudinal scales. Accordingly, the present studyaims at the development of a unifying hypothesisof thermal limitation and adaptation, which mayexplain the thermal limits of geographical distri-bution. As a second step this concept also attemptsto explain the reasons for reproductive failure atthe borders of the temperature window as well asfor changes in energy allocation to growth andreproduction as a consequence of thermal accli-matisation(Portner et al., 2001).¨

Thermal sensitivity needs investigation at boththe high end and the low end of the temperaturespectrum. The crucial mechanism(s) of thermallimitation and adaptation should link low and hightolerance limits, since they shift unidirectionallyduring thermal acclimation. Also, changes occur-ring during acclimation to high temperaturesshould reverse the processes involved in low tem-perature acclimation. These patterns should besimilar for all groups of metazoans. Within anorganism the crucial mechanisms of temperatureadaptation should be visible in all tissues support-ing the functional co-ordination of the organismicentity. If failure of individual molecular mecha-nisms is involved whole animal limits and thelimits of these individual molecular mechanismsshould be identical. In consequence, sensitivitylevels of molecules, organelles, cells, tissues andthe intact organism need to be distinguished aswell as the difference between mechanisms respon-sible for long and short-term tolerance. Thisincludes the key question as to which physiologicalprocesses define the temperature window ofgrowth and reproduction as required for successfullong-term maintenance of a population in its nat-ural environment. Beyond this window, passivetolerance may ensure time-limited survival of theindividual animal, e.g. during unfavourable con-ditions like extreme seasonal cold or warm. How-ever, such limits likely do not reflect closeco-ordination between environmental temperaturesand the range of optimum physiological perform-ance and may, thus, not be closely correlated withgeographical distribution limits.

2. Thermal sensitivity and the level of organi-sational complexity

It is widely held that heat tolerance limits forall metazoa are found at approximately 478C.Even the ‘Pompeii worm’, which is believed to bethe ‘most thermotolerant eukaryote on earth’(Des-bruyeres et al., 1998) by being exposed to tem-peratures between 2 and, possibly, 1058C in itsWhite Smoker environment at hydrothermal deepsea vents, will likely not live long-term beyond 318C (Dahlhoff and Somero, 1991; for review seeDesbruyeres et al., 1998). The upper thermal limitof nematodes may reach somewhat higher andbeyond 45–478C, which is considered as theupper temperature limit of continuous inhabitation(Nicholas, 1984). Similarly, a desert ant tolerates53.6 8C but only during short-term periods of itsmidday feeding excursions(Wehner et al., 1992,see below). The average upper thermal limit forinsects was evaluated as 47.4"0.4 8C (Addo-Bediako et al., 2000). In general, temperaturesbeyond 478C are tolerated only temporarily bymetazoans(cf. Schmidt-Nielsen, 1997). This con-trasts the thermal limits of bacteria some of whichthrive continuously at temperatures over 908C andeven in boiling waters. Simple eukaryotes likefungi or algae still grow at temperatures of approx-imately 55–608C (Tansey and Brock, 1972).The question arises at which organisational lev-

el, molecular, cellular or organismic, the limits ofthermal tolerance are likely to be found. Accordingto an early hypothesis by Tansey and Brock(1972), there should be no difference in the ther-mal stability of aerobic heterotrophic metabolismbetween pro- and eukaryotes. Eukaryotes, how-ever, are characterised by the formation of intra-cellular organelles like nuclei and mitochondria, aprocess which might have reduced the capacity totolerate extreme temperatures. Selective transportof macromolecules across organellar membranesoccurs and, according to Tansey and Brock(1972),these large pore membranes may be leakier andless thermostable than plasma membranes. How-ever, the further reduction in heat tolerance fromsimple eukaryotes to metazoans(see above)remains unexplained by this interpretation. Thisproblem disappears when it is considered, that theformation of intracellular organelles reflects a gainin structural and functional complexity betweenpro- and eukaryotes. The limits of tolerance wouldbe set at the level of the organelles and their


Fig. 2. Heat sensitivity depending on cellular and organismic complexity. The rise in organisational complexity between prokaryotes,unicellular eukaryotes and metazoa is interpreted to cause a drop in thermal tolerance. For further explanations see text.

functional co-ordination with the rest of the cell,i.e. at a higher level of complexity(cellular com-partmentation) than in prokaryotes(Fig. 2).Even higher levels of organisational complexity

are added in metazoans, for example by the spe-cialisation of tissues, the establishment of centralcontrol and the requirement to circulate and movebody fluids and air or water for gas exchange andhomeostatic maintenance. Associated with thisgain in complexity is an increase in metabolic ratereflecting a performance increment between uni-cellular organisms and animals(Hemmingsen,1960, as depicted by Schmidt-Nielsen, 1997). It isintriguing to assume that the rise in performanceseen between pro- and unicellular eukaryotes aswell as between simple eukaryotes and metazoaoccurs at the expense of greater thermal sensitivity.The limits of tolerance would be set at the highestlevel of organisational complexity, i.e. the func-tional co-ordination of organismic componentstowards a larger unit. Within the metazoan organ-ism, lower thermal sensitivities would again beexpected at lower complexity levels, i.e. at cellularand molecular levels. A sequence of thermal sen-sitivities results which relates to the level oforganisational complexity of the system(Fig. 2).A concept that considers the combination of

functional elements towards higher levels of inte-gration is the concept of symmorphosis as devel-oped for the mammalian respiratory system(Taylorand Weibel, 1981). This concept states that animalsmaintain just enough structure to support oxygen

flux rates at their maximum oxygen uptake rates.The design of all components of a system matchfunctional demand in a way that excess capacityof any single component is avoided(Hoppeler andWeibel, 1998). This concept becomes important inthe context of temperature adaptation and limita-tion, since oxygen limitation at extreme tempera-tures(both low and high) is most likely a unifyingprinciple in animals, which defines the first linesof both heat and cold intolerance(Portner et al.,¨1998, 2000; Portner, 2001). More recent evidence¨discussed for an oxygen limitation of thermaltolerance supports earlier, more descriptive work,where improved survival of fish at high tempera-tures was found in normoxia compared withhypoxia in the case of trout and roach(Alabasterand Welcomme, 1962) or in hyperbaric hyperoxiacompared with normoxia in the case of goldfish(Weatherley, 1970).Evidence is discussed that the first line of

thermal sensitivity becomes apparent at the highestfunctional level possible, in this case the integratedfunction of ventilation and circulation. It is hypoth-esised that a shift of thermal tolerance windows ispredominantly caused by the observed changes intissue mitochondrial densities andyor functionalproperties and the respective consequences for celland tissue function as well as central functionslike nervous control, circulation and respiration.Molecular and membrane adjustments supportthose at the organellar, cellular and tissue levelleading to the maintenance and sensible adjustment


Fig. 3. Cold induced onset of anaerobic mitochondrial metabolism in the temperate zone intertidal wormSipunculus nudus is indicatedby the accumulation of succinate, propionate and acetate in the body wall musculature(left). Transition to cold induced anaerobiosisappears as the final result of a cold induced collapse of ventilatory peristalsis below 48C (right, after Zielinski and Portner, 1996).¨

of central functions. The changes in mitochondrialfunctions would not only explain a shift in thermaltolerance limits defined at high levels of organi-sational complexity, but also contribute to trade-offs within energy budgets with the respectiveconsequences for temperature dependent changesin growth, fecundity and recruitment, ecologicalkey processes which determine population struc-ture and dynamics.

3. Oxygen limitation of thermal tolerance: aunifying principle?

3.1. Water breathers

Recent evidence for oxygen limited thermaltolerance arose from the observation of low andhigh thermal tolerance thresholds in various marineinvertebrate species and, most recently, high tol-erance limits in fish, which were associated withthe transition to an anaerobic mode of mitochon-drial metabolism. These low and high temperaturethresholds had been defined as critical tempera-tures(T , for review see Portner et al., 1998, 2000;c ¨Portner, 2001). In all studies reported the onset of¨

mitochondrial anaerobiosis indicated transition topassive, time limited cold or warm tolerance.Cold or warm induced onset of mitochondrial

anaerobic metabolism in fully aerated water indi-cated a mismatch of oxygen supply and demandand critically low tissue oxygen levels. Investiga-tions of oxygen consumption during warming sug-gested that high critical temperatures wereassociated with the upper limit of a heat inducedrise in oxygen demand(cf. Portner, 2001). Cold¨exposure led to a progressive failure of ventilatoryperistalsis, as shown in a marine worm,Sipunculusnudus. Below a threshold temperature of 48C thisprocess led to progressive hypoxia in the bodyfluids and finally transition to anaerobic mitochon-drial metabolism(Fig. 3, Zielinski and Portner,¨1996). The picture became even more completefor the spider crab,Maja squinado, where contin-uous analysis of haemolymphPO during progres-2

sive warming or cooling (Fig. 4) revealedmaintenance of high oxygen levels and maximumoxygen supply only within an optimum tempera-ture window. Major changes in haemolymphPO2occurred outside of this window, until finally,oxygen partial pressure had fallen to extremely


Fig. 4. Correlation of haemolymph oxygen tensions and transition to anaerobic metabolism in the spider crab,Maja squinado (data byFrederich and Portner, 2000). The PO and metabolite profiles recorded during progressive cooling from 12 to 08C (at 1 8Cyh) or2¨warming from 12 to 408C (at 2 8Cyh, tissues were sampled after the final temperatures were reached) characterises aerobic scopeavailable to the animals and, finally, tissue hypoxia at extreme temperatures. The profiles match optimum, pejus and pessimum rangeswith respect to temperature, as adopted from the law of tolerance(Shelford, 1931; Schwerdtfeger, 1977; Frederich and Portner, 2000).¨

low levels and concentrations of lactate and suc-cinate rose in tissues and haemolymph(Frederichand Portner, 2000). The transition from a temper-¨ature range with maximum arterialPO to low or2

high ranges of temperature characterised by pro-gressive hypoxia in the body fluids identified asecond set of low and high threshold temperatureswell within the range encompassed by criticaltemperatures. Adopting Shelford’s law of tolerance(Shelford, 1931) these threshold temperatures were

called pejus temperatures,T I and T II (pejussp p

getting worse), since they indicate the limits ofoptimum haemolymph oxygenation and, thereby,onset of a worsening of oxygen supply to theorganism(Frederich and Portner, 2000; Fig. 4).¨In the spider crab the highPO betweenT I2 p

andT II was maintained by a temperature-depend-p

ent increase in heart and ventilation rates asrequired to compensate for the rise in oxygendemand(Fig. 5). However, beyond the high pejus


Fig. 5. Correlated changes in ventilation and heart rates in the spider crabMaja squinado between 0 and 408C. Threshold temperatures(Tc I, Tp I, Tp II and Tc II) are identified by breakpoints in ventilation rate and corresponding changes inPO and heart rate(cf. Fig.2

2, after Frederich and Portner, 2000).¨

temperature(T II) ventilation and heart ratesp

became more or less constant and independent oftemperature, indicating capacity limitation. Theonset of a decrease inPO then reflects a rise in2

oxygen demand which was no longer compensatedfor by an increase in ventilation and circulation.Beyond the upper critical temperature(T II)c

ventilatory and circulatory activity collapsed. Asin Maja squinado, collapse of circulatory activitywas seen during long term recordings in heatstressed Antarctic clams,Laternula ellipticaaccompanied by a decrease in oxygen uptake(Peck et al., 2001). In cold exposed spider crabs,a further decrease in ventilation and heart ratesbeyond the low pejus temperature(T I) was againp

followed by a decrease inPO , also indicating2

insufficient oxygen uptake and transport(Fig. 5;Frederich and Portner, 2000). Collapse of ventila-¨tory activity finally occurred, similar to the results

obtained earlier in sipunculids(Fig. 3; Zielinskiand Portner, 1996).¨A capacity limitation of ventilation at the upper

critical temperature threshold was also indicatedby a progressive deviation of ventilation frequencyfrom that dictated by the normalQ relationship10

in the notothenioid fish,Lepidonotothen nudifrons(Hardewig et al., 1999). Studies summarised byFarrell (1997) suggest that in temperate salmonidfish the limits of aerobic scope in the heart maylead to insufficient blood circulation at extremetemperatures. Accordingly, heat stress in cod wasshown to elicit a temperature-dependent decreasein venous, but not arterial oxygen tensions(Portner¨et al., 2001). Non-invasive magnetic resonanceimaging data obtained in polar and temperateeelpout support these conclusions by identifying ahigh pejus temperature where maximum bloodflow is reached well below the critical temperature.


Unchanged white muscle blood oxygen levelsduring an exponential rise in oxygen demandreflect a loss in aerobic scope and emphasise thatthe changing relationships between metabolic oxy-gen demand and maintained or changing tissuePO are important to indicate onset of changes in2

aerobic scope(F. Mark, C. Bock and H.O. Portner,¨unpublished). Finally, the fish heart may be unableto circulate blood at a sufficiently high rate tomaintain the arteriovenous difference in bloodPO and a venous reserve. Progressive hypoxia2

and, finally, anaerobic metabolism results at thetissue level, at first in tissues with a high oxygendemand such as liver(van Dijk et al., 1999). Thefish heart itself may be very resistant since itpumps venous blood and is specialised to operateat low venousPO . Myocardial oxygen consump-2

tion removes only a small fraction of venousoxygen content(Farrell, 1996; Block, 1990). Thisstatement is valid until venousPO reaches a low2

value or oxygen demand rises to a level in thewarm at which the oxygen partial pressure headrequired for diffusion is no longer sufficient(cf.Steffensen and Farrell, 1998). In terms of tissuedesign, stenothermal Antarctic notothenioid fishespossess type I heart ventricles, which are charac-terised by full trabeculation and the absence of acoronary circulation(Axelsson et al., 1998) andreflect a restricted dynamic range of the circulatorysystem as well as the narrow thermal tolerancewindows characteristic for this group(Somero andDeVries, 1967).Ventilatory organs actively and continuously

involved in oxygen uptake may also be among thefirst tissues to experience the drop in oxygensupply. In the body wall musculature of wormsand the mantle musculature of cephalopods, whichare responsible for ventilation, anaerobic glycolysiswas observed in addition to mitochondrial anaer-obic metabolism(cf. Portner, 2001). Finally, a¨drop in energy levels(Gibbs free energy of ATPhydrolysis) to critically low levels characterisedfunctional failure in cold exposed ventilating bodywall musculature ofS. nudus (Zielinski and Port-¨ner, 1996). The development of oxygen deficiencyand onset of functional insufficiency and finallyfailure of any tissue involved in homeostatic main-tenance obviously go hand in hand(Zielinski andPortner, 1996; Sommer et al., 1997; Sommer and¨Portner, 1999; cf. Figs. 3–5).¨Prior to anaerobiosis the progressive drop in

arterialPO in the cold and in the warm reflects a2

reduction of oxygen availability to mitochondria.At reduced PO mitochondria will no longer2

achieve maximum rates of oxygen consumption.This apparent reduction of mitochondrial aerobiccapacity indicates a reduced scope for aerobicactivity of the whole animal as defined by meas-urements of oxygen consumption in fish(Bennett,1978). The scope for aerobic activity extends fromthe whole animal to tissue to mitochondrial levels(Lindstedt et al., 1998), since it reflects the rangebetween minimum and maximum oxygen con-sumption by mitochondria and depends upon suf-ficient oxygen delivery by ventilation andcirculation. Evidently, the slowing of ventilationand circulation in the cold and the insufficientincrease in the warm cause a mismatch betweenoxygen delivery and demand which finally leadsto the collapse of physiological function(Portner¨et al., 1998, 2000; Portner, 2001). Limited func-¨tional capacity leading to oxygen limitation andfinally, functional failure are most likely interrelat-ed processes, since transition to anaerobiosisalways indicates time limited tolerance. In accor-dance with the argument developed above, oxygenuptake and distribution by ventilation and circula-tion are most likely those processes of a highorganisational complexity which were predicted toset the limits of thermal tolerance.As a corollary, the data indicate that the tem-

perature range characterised by maximum bodyfluid PO represents the temperature window of2

maximum scope for aerobic activity. It thereforeindicates the temperature range of optimum per-formance of the animal. Within this thermal rangethe animal is fully operative and availability ofaerobic energy is maximal for all physiologicalfunctions including growth and reproduction tosupport long-term survival in the natural environ-ment. Thermal limitation already sets in at thetransition from optimum to pejus range, character-ised by progressively insufficient oxygen supplyowing to temperature limited ventilatory and car-diac capacity(Figs. 3 and 5).

3.2. Air breathers

According to Section 3.1 evidence is strong forwater breathers that thermal tolerance limits areset by limited oxygen supply before disturbanceof molecular functions sets in. The question arisesas to whether the transition to air breathing may


Fig. 6. Development of alveolar criticalPO (P ) and maxi-2 c

mum alveolarPO in two species of fresh water turtles, data2

adopted from the indicated literature studies. Intersection of theextrapolated curves(dotted lines) quantifies the critical tem-perature(T ), where no aerobic scope for spontaneous activityc

is left (see text). Similar conclusions were drawn for alligators(Alligator mississipiensis) by Portner(2001).¨

have changed the sequence of thermal tolerancelimits (from loss of aerobic scope to onset ofanaerobic metabolism and then molecular denatur-ation). Transition to air breathing implies a reduc-tion by one order of magnitude in the energy costof ventilation at approximately 30 times higherlevels of ambient oxygen. This may have allowedair breathers to be more eurythermal at a reducedcost of ventilation. This advantage of breathing airrather than water is counterbalanced by the factthat thermal buffering is insignificant in the terres-trial compared to the aquatic environment.Nonetheless, specialisation of physiological

function to a thermal window is still observed inair breathers. Even endotherms, although they haveoptimised functions at constant high body temper-atures, are adapted to a given climate, either byinsulation from the environment or by mechanismsof improved heat transfer. However, the mecha-nisms limiting heat tolerance have not really beenestablished in air breathers. Nonetheless, somereports indicate that thermal tolerance may beoxygen limited and allow vague estimates of thecritical temperature, mostly in ectothermic speciesadapted to temperate or warmer climates. In thecold below 158C, malfunction of the circulatorysystem and acetate accumulation developing inwarm adapted air breathing arthropods, scorpionsand tarantulas(Bridges et al., 1997, R.J. Paul,unpublished) indicates oxygen limited cold toler-ance(cf. Portner, 2001). In the alligator,Alligator¨mississipiensis, the criticalPO as identified by the2

onset of anaerobic metabolism(Portner and¨Grieshaber, 1993), increases as temperature risesand reaches normoxic values at approximately 458C indicating elimination of aerobic scope inaccordance with the above definition of theTc

(Branco et al., 1993, cf. Portner, 2001). Tempera-¨ture dependent changes in the ratio of ventilatoryvolume and oxygen consumption in the fresh waterturtle, Pseudemys scripta elegans (Jackson, 1971)suggest that alveolar oxygen extraction inPseu-demys scripta elegans becomes insufficient at theT between 35 and 408C. Further studies in freshc

water turtles demonstrated that alveolar oxygenlevels in the lung decrease and alveolar, criticalPO increases exponentially at high temperatures2

(White and Somero, 1982; Fuster et al., 1997).Both curves would intersect between 40 and 458C, again indicating full elimination of the aerobicscope at the high critical temperature(Fig. 6).

If long-term heat tolerance limits in metazoa aregenerally found at approximately 458C, air breath-ers, for the reasons discussed above, seem toapproach that limit more closely than water breath-ers. A recent review of upper thermal limits ininsects(on average 47.48C) revealed that upperlethal limits are not correlated with ambientextremes or latitude(Addo-Bediako et al., 2000).It needs to be emphasised here that these limitshave been determined during experimental short-term temperature increments leading to limitsbeyond upper pejus and, most likely, critical tem-peratures. Evidently, short-term tolerance limits arenot significantly correlated with geographical dis-tribution, at least not in insects.In endotherms studies addressing the question

whether a mismatch of oxygen supply and demand


is involved in thermal tolerance limits are rare.For example, data provided by Jourdan et al.(1989) suggest that progressive circulatory failurebelow 208C body temperature in the rat leads toprogressive energy deficiency and elevated lactatelevels. Accordingly, functional failure(capacitylimitation) of circulation and tissue perfusion islikely to limit cold tolerance. The role of oxygendemand in heat tolerance is not clear. However,many events discussed for both cold and heatdamage are similar to those elicited by hypoxia orischemia including the formation of oxygen radi-cals (Rifkind et al., 1993, Ivanov 2000). In gen-eral, studies of thermal tolerance usually focus onlower complexity levels, the pathology of heatshock and cold injury, including the cellular mech-anisms of heat or cold hardening by heat shockproteins and related chaperones(e.g. Burdon,1987; Fujita, 1999) as well as temperature inducedinjuries by oxygen radical formation(Ando et al.,1994; Bhaumik et al., 1995), endotoxemia(Caputaet al., 2000) or elevated calcium levels(Ivanov,2000). As a corollary, further investigations at thelevel of aerobic scope and ventilatory and circu-latory capacity depending on body temperature arehighly needed in mammals and birds.

3.3. Synopsis

In both air and water breathers exposure toextreme heat or cold appears to involve eliminationof aerobic scope and finally oxygen deficiency.For a final judgement of whether oxygen limitationreally limits thermal tolerance the situationbecomes much clearer for air breathers if it isconsidered that the window delimited by pejustemperatures will be smaller than the one definedby critical temperatures and closer to environmen-tal temperature oscillations. Since pejus tempera-tures characterise the onset of a reduction inaerobic scope the conclusion arises that onset of aloss in aerobic scope sets the long-term limits ofthermal tolerance in air breathing ectotherms asmuch as it does in water breathers.Finally, if oxygen limitation characterises ther-

mal intolerance, it is no longer surprising thatlactate as an end product of anaerobic metabolismis able to elicit behavioural hypothermia in aquaticand terrestrial ectotherms. In vertebrates and someinvertebrates lactate indicates extreme oxygen lim-itation and, being formed at the highT , wouldc

stimulate the organism to move to cooler temper-

atures (Portner et al., 1994; De Wachter et al.,¨1997; Branco and Steiner, 1999). Optimised func-tions depending on temperature in the sense thatmaximum aerobic scope is maintained, are sup-ported by behavioural thermoregulation in bothecto- and endotherms. If different thermal nichesare accessible to an individual, they are choseneither to maximise activity and reactivity, e.g. bywarming up in the sun, or they are chosen toescape from daily or seasonal temperatureextremes by hiding in the shade or underground.Considering that the rise in the performance of

ventilatory and circulatory structures matches therise in whole organism performance throughoutthe animal kingdom(e.g. between amphibians andmammals) a limiting role of ventilation and cir-culation becomes understandable when the capac-ity of oxygen uptake and transport systems is setto a minimally required level in accordance withmetabolic requirements. These considerations arein line with the concept of symmorphosis(seeabove). In the context of thermal adaptation andlimitation this means that the functional capacitiesof oxygen delivery systems are set to be optimalbetween the average highs and lows of environ-mental temperatures. This immediately leads tothe conclusion that the specific design constraintsof a phylum together with the lifestyle dependentmetabolic rate of a species in relation to the oxygencontent of ambient media will determine the tol-erated temperature extremes. Accordingly, Fig. 7emphasises that limiting temperature maxima andconstraining factors shift between animal groupsbut all relate to oxygen provision. Owing to thevariability in lifestyles and designs relatively safecomparisons appear possible especially at the highend of metazoan body temperatures and betweengroups from similar environments. Comparing adesert pupfish and a warm water squid, which areboth water breathers, the higher metabolic rate andpoorer oxygen transport of the squid(cf. Portner,¨in press) may explain, why maximum heat toler-ance in this group is lower than in fish. Comparinga desert lizard and a desert ant the design of therespiratory system of the insect would support itsslightly higher heat tolerance, however, only at abody size several orders of magnitude smaller thanthe reptile. The assumption of an oxygen limiteddesign in insects is supported by the observation,that only the elevation of atmospheric oxygenlevels (35% atmospheric oxygen in the Phanero-zoic compared with 20.9% of today) allowed for


Fig. 7. Comparisons of maximum sustained body temperatures in warm adapted highly organised animal groups identifying metabolicrate, body size or the efficiency of ventilatory systems as the crucial differences(see lightly shaded areas) between paired species. Gasexchange systems are countercurrent gills in the water breathers, lungs in reptiles and trachea in insects, as well as lungs operatingeither as a pool exchange system in mammals or as a cross current system in birds. Low oxygen availability in water likely explainsthe lower heat tolerance of squid and fish compared with air breathers.

the evolution of large insects, namely giant dragonflies (Dudley, 1998; Berner et al., 2000). Finally,when comparing mammals and birds, the improvedventilatory efficiency of the bird lung with itscross-current gas exchange system would suggesta lesser degree of oxygen limitation in birdsallowing for higher defended body temperaturesthan in mammals and a more active lifestyle inhot terrestrial environments(Fig. 7).In general and as a corollary, the three-dimen-

sional interaction between oxygen limitation, envi-ronmental temperature and also performance levelsof the whole animal needs to be considered as animportant constraint in animal evolution. Recentstudies emphasised that high oxygen concentra-tions in ambient media supported the evolution oflarger species. This trend becomes visible(e.g.among amphipods; Chapelle and Peck, 1999) incold, polar and Lake Baikal waters characterisedby elevated oxygen solubilities compared withwarmer waters and also in earth history with thepresence of giant dragon flies at high atmosphericoxygen contents in the warm(see above). In atrade-off between maximum aerobic scope foractivity, ambient oxygen levels and temperature,maximum body size within a group is limited byeach of these factors, a suggestion which seemsmost unequivocal in aquatic invertebrate athleteswith a high oxygen demand, squid(Portner and¨Zielinski, 1998; Portner, in press). Since the max-¨imum levels of muscular activity appear generallylower in the permanent cold(Clarke, 1998), highoxygen levels in cold waters would then allow forgiant life forms to develop. Accordingly, giant andmore or less sluggish cephalopods are confined to

cold ocean environments, the deep sea in the caseof giant squid(supported by neutral buoyancy ofammoniacal tissues) or the cold Northern Pacificin the case of the giant octopus. In warm watersthe necessity to maximise aerobic scope at reducedambient oxygen levels would then limit maximumbody size in cephalopods. This comparison alreadyshows the principle difference between terrestrialand aquatic environments in that oxygen levels interrestrial environments are independent of tem-perature. The mitochondrial story told below sug-gests that cost efficiency, i.e. maximum output ofaerobic energy at minimum mitochondrial densityincreases with rising temperature, however, onlyas long as sufficient oxygen can be provided.Therefore, metabolic efficiencies rise at high bodytemperatures(see below). These relationshipsbecome effective, especially in air and support thedevelopment of larger forms of terrestrial ecto-therms in the warm.

4. Hierarchy and time windows of thermallimits

Oxygen limitation of thermal tolerance, visibleas limitation in aerobic scope, appears as a unify-ing principle at temperatures above freezing(cf.Portner, 2001). It is set as the first line of thermal¨sensitivity at the whole organism level, i.e. at ahigh level of organisational complexity, due tocapacity limitations of ventilation and circulation.The initial limiting effect of temperature is areduction in aerobic scope and oxygen supplybeyond pejus temperatures(T in Fig. 8). Ap

sequence of thermal limits results, where oxygen


Fig. 8. Modelled hierarchy of thermal tolerance thresholds in animals(modified after Portner, 2001) considering changes in metabolic¨

heat production according to patterns of oxygen consumption( O ), or anaerobic heat production(Q ). The model is predominantlyM 2 anae

based on data for water breathers(T critical, T , pejus,T denaturation temperatures) but likely extends to air breathers(see text).c p d

Mechanisms shifting the respective tolerance thresholds include overall mitochondrial functional capacity, which causes a shift in bothupper and lowerT andT , at the expense of significant metabolic cold adaptation in eurytherms(see text). Downward pointing linearc p

arrows qualify increased oxidative stress during progressive hypoxia. A drop in oxygen demand as well as anaerobic heat productionis expected from a decrease in mitochondrial densities and capacities during warming. The upper denaturation temperature likely shiftswith the presence of heat shock proteins(HSPs, cf. Tomanek and Somero, 2000) or antioxidants(Abele et al., 1998b). A lowerdenaturation temperature is not considered, but the same mechanisms may be effective. Antifreeze protection or supercooling as wellas reduced Mg levels in body fluids extend the tolerance range below the freezing point of body fluids(not shown).2q

Fig. 9. Mechanisms defining the time limits of thermal tolerance(see text).

limitation in the sense of a reduction in aerobicscope indicates the earliest limits reached, namelythe limits of long term tolerance. According to theearly work by J.R. Brett, activity and even moreso reproduction(which includes associated spon-taneous activity) of sockeye salmon(Oncorhyn-chus nerca) occurs within much narrower thermalwindows than metabolic maintenance(for review

see Cossins and Bowler, 1987). Once aerobicscope starts to be diminished beyond pejus thresh-olds growth and reproduction would be the firstprocesses to be suspended(Fig. 9). This causes adecline in population but has limited effects onindividual survival except for a temperature-dependent change in individual life span(rate ofliving).


As temperature rises further beyond pejus levels,individual tolerance but becomes progressivelytime limited (Fig. 9). Spontaneous activity isreduced as aerobic scope falls such that fooduptake is finally prevented towards the criticaltemperature(Fig. 8). Survival becomes a questionof hours, days or weeks, depending on individualresistance to starvation. Once critical temperaturesare surpassed, the transition to extreme hypoxiaand, finally, an anaerobic mode of mitochondrialmetabolism characterises passive tolerance limits(T ). Since maintenance of aerobic standard metab-c

olism is no longer possible, the capacity of anaer-obic metabolism and, thus, hypoxia tolerance ormetabolic depression strategies will determineindividual survival on a time scale reduced furthercompared with the pejus range of temperaturesbetweenT andT (Fig. 9).c p

Oxidative stress may already increase whenoxygen limitation sets in at pejus and even moreso during extreme hypoxia beyond critical temper-atures. Since mitochondria are considered as majorcellular sources of reactive oxygen species atbetween 1% and 3% of their rate of oxygenconsumption(Sohal and Weindruch, 1996) warm-ing will not only cause an increase in metabolicrate but also an associated increase in oxygenradical production possibly linked to enhancedoxidative stress. At the same time, hypoxia devel-ops during warming and cooling(see above).Hypoxia has been found to cause excess produc-tion of oxygen radicals owing to facilitated auto-oxidation of haem groups in mitochondria orhaemoglobin(Boveris and Chance, 1973; Rifkindet al., 1993). These processes are also found inmarine invertebrates(Abele et al., 1998a). Amoderate accumulation of malondialdehyde as aproduct of lipid peroxidation, was found in theAntarctic bivalve,Yoldia eightsi at 5 8C and above(Abele et al., 2001) and a progressive destabilisa-tion of membranes occurred in the Antarctic limpetNacella concinna (Abele et al., 1998b). SODforms the first line of defence against oxidativestress, as it catalyses the removal of oxygen radi-cals at the expense of generating H O , which is2 2

then removed by catalase. Increased availability ofSOD either by chemical modification or owing tooverexpression alleviates oxidative stress and min-imises hypoxia induced post-ischemic injury(Wang et al., 1998, Nakajima et al., 2000). Duringwarming above ambient temperature maxima,superoxide dismutase(SOD) levels decreased in

Yoldia eightsi and in N. concinna (Abele et al.,1998a,b, 2001). The reasons for the inactivationof SOD at elevated temperatures remain unclear,however, progressive hypoxia elicited by the dras-tic increase in oxygen demand at high temperaturesmay hamper protein synthesis(see below) andthereby, SOD expression. In similar ways as in theAntarctic molluscs, oxidative stress mechanismsappear to contribute to thermal stress in temperatezone invertebrates(Tremblay et al., 1998) and alsoto thermal stress and bleaching in tropical corals(Lesser et al., 1990; Lesser, 1997). In the seaanemoneAiptasia pulchella (Nii and Muscatine,1997) oxidative stress occurs during heatingregardless of the presence of endosymbiotic algae.As a corollary, the progressive development ofhypoxia and oxidative stress very likely go handin hand, at least during heat stress. Functionalconsequences of oxidative stress have not beeninvestigated, however, damage by oxygen radicalsmay support progressive loss of function alreadybeyond pejus and, even more so, critical tempera-tures. Short-term tolerance to oxidative stress willsupport tolerance to extreme thermal events(Fig.8) and is likely to be most expressed in theintertidal, a conclusion supported by the relativelyhigher stability of antioxidative enzymes in inter-tidal compared with subtidal invertebrates(Regoliet al., 1997).In the sequence of thermal limits, finally, loss

of protein function occurs at denaturation temper-atures (T in Fig. 8), possibly indicated by and

Arrhenius break temperatures of molecular, orga-nellar or cellular functions or by neuromuscularfailure in the heat. At lower levels of complexity,each individual molecular or membrane functionhas been optimised with respect to ambient tem-perature. Therefore, functional failure of thesemechanisms(T in Fig. 8) likely correlates withd

whole animal tolerance thresholds, however, attemperatures beyond pejus or even critical values.For example, the Arrhenius break temperature ofstate 3 respiration in isolated mitochondria corre-lates with habitat temperature but is usually situ-ated above experimental tolerance limits of thewhole organism(Weinstein and Somero, 1998;Somero et al., 1998), even above critical temper-atures(Portner et al., 2000).¨A cellular defence mechanism discussed to con-

tribute to thermal tolerance is the so-called heatshock response, which involves the increased syn-thesis of heat shock proteins(HSP) under condi-


tions of cold or warm stress(for review see Federand Hofmann, 1999). A role for heat shock pro-teins(HSPs) in thermal protection is suggested bya comparison of congeneric snail species fromdifferent tidal heights (Tomanek and Somero,1999, 2000). Rapid expression of HSPs to mod-erate levels is correlated with increased hardinessagainst extreme thermal events(shifting T in Fig.d

8). Expression is also correlated with the improvedcapability to recover from heat stress. Similarly, adesert ant(Cataglyphis) that regularly undergoestemperatures beyond 508C during feeding excur-sions, synthesises heat shock proteins as a protec-tive measure against these temperature extremeswhich nonetheless are lethal during exposure long-er than several minutes(Gehring and Wehner,1995). However, excess synthesis of heat shockproteins seems harmful since it occurs at theexpense of other protein synthesis(Tomanek andSomero, 2000).HSPs likely protect cellular molecules especially

in situations which require time-limited tolerance(hardening), e.g. in the intertidal zone, and beyondthe limits of long-term thermal tolerance as definedabove. This thinking is in line with the conclusionthat temperature ranges between pejus and criticaltemperatures and even more so beyond criticaltemperatures are accessible for the organism onlyduring limited time periods. It is also in line withthe observation that HSP expression is triggeredby hypoxia events(see Burdon, 1987; Feder andHofmann, 1999, for review). Extreme hypoxia atthe T associated with increased oxygen radicalc

production may thus contribute to elicit HSP geneexpression. At more extreme temperatures HSPsynthesis stops(cf. Tomanek and Somero, 1999).On the one hand, the frequency of extreme tem-perature events in the natural environment will beimportant in whether adequate use of this responseis crucial for wider distribution patterns in suchenvironments(cf. Tomanek and Somero, 1999).Such a correlation still needs to be established inthermal tolerance analyses. On the other hand, lifein thermally stable natural environments may elim-inate the necessity to use the heat shock response.This thinking is supported by the finding thatstenothermal Antarctic fish but also cod do notshow a temperature induced heat shock responsein vivo (Hofmann et al., 2000; Portner et al.,¨2001). Despite existence of the gene family somespecies may not use the response and have lost

tolerance to extreme temperatures beyond therange of long-term fluctuations. In those species,which express the heat shock response, the corre-lation of the threshold temperatures for HSP induc-tion with the thermal niche of a species or withseasonal acclimatisation(cf. Feder and Hofmann,1999) will likely be influenced by a shift inthermal tolerance windows defined by oxygenlimitation.According to the links outlined between oxygen

deficiency, protein synthesis, oxidative stress andheat shock protein expression, the picture arisesthat not only a sequence but a hierarchy of thermallimits exists in metazoa(Fig. 8). In the wholeorganism, disintegration of mechanisms at a lowerlevel of complexity may at least be favoured ifnot elicited by oxygen deficiency beyond pejus orcritical thresholds(T or T in Fig. 8) and may,p c

thus, not only result from direct thermal denatur-ation. Damage to membranes or proteins mayoccur as a consequence of rising oxidative stress.Protein synthesis may be reduced or completelycollapsed during temperature induced hypoxia,thereby preventing molecular repair such that lim-its become effective depending on the duration ofexposure to thermal stress. Whereas the conceptof symmorphosis is an approach to understandhow individual components match the design ofthe system the concept of a hierarchy of thermaltolerance emphasises that insufficient capacity ofthe overall system will affect the functional andstructural integrity of individual components,through insufficient oxygen supply.It is important to note in this context that thermal

tolerance is frequently investigated during short-term progressive heat increments and defined aslethal limits. However, these short-term protocolswill only provide information on the tolerance toshort-term extreme temperature events that verylikely go far beyond the thresholds defined by theonset of oxygen limitation(Fig. 8). The presenceof heat shock proteins and antioxidants will causemore or less efficient molecular protection(Fig.8) at extreme temperatures and, thereby, influencethe period of time-limited survival. These consid-erations explains why acute survival thresholdsidentified by the typical procedure of progressiveshort-term heating or cooling within minutes orhours (cf. Elliott and Elliott, 1995) are higher inthe warm (lower in the cold) than the limits oflonger term thermal tolerance for the resting indi-


vidual. This extends to Antarctic species(Lahdes1995; Urban, 1998). For example, the upper lethaltemperature(LT ) of the Antarctic bivalveLater-50

nula elliptica has been determined at 14.98C after24 h of acute temperature exposure(Urban, 1998).However, oxygen limitation sets in already at apejus temperature close to 48C (H.O. Portner,¨L.S. Peck, T. Hirse, unpublished). Interestingly,this is very close to the temperature(3.6 8C) atwhich 50% of the animals lost the ability to reburyin the sediment(Urban, 1998).Fig. 9 illustrates how the hierarchy of thermal

tolerance limits is reflected in an increasinglyreduced tolerance over time to extreme thermalevents. Limits are found at progressively lowerorganisational levels, and malfunction of the higherlevels would set the time limits(Fig. 8). Nonethe-less, even the short-term lethal limits may shiftwith long term acclimation to higher or lowertemperatures(e.g. Tomanek and Somero, 1999;Stillman and Somero, 2000). Upward shifts areobserved in temperate but no longer in tropicalspecies where further heat acclimation is no longerpossible. As a precondition for the shifts of short-term tolerance limits during long term acclimation,pejus and critical thresholds should shift as well,such that the full array of organismic to moleculartolerance limits moves more or less in parallel.Key mechanisms causing such long-term shifts inpejus and critical temperatures need to bediscussed.From an ecological perspective, pejus rather

than critical temperatures are likely to reflect theupper and lower temperature limits determininggeographical distribution. In the future, this con-clusion needs to be tested and quantified for bothair and water breathing species in a latitudinalcline, in a collaborative effort of physiologists andecologists. In this context, the hierarchy of pejus,critical and denaturation temperatures and the dis-tances between these thresholds await further quan-tification in water breathers and even more so inair breathers, where a limitation of thermal toler-ance by loss in aerobic scope still needs unequiv-ocal verification for many groups includingmammals and birds. These investigations shouldalso address the trade-offs involved in thermaladaptation and the consequences for the successof species in thermally stable vs. unstableenvironments.

5. Temperature adaptation: overcoming aerobicscope limitations in eurytherms andstenotherms

It became evident early on that critical temper-atures differ between species and populationsdepending on latitude or seasonal temperatureacclimatisation and are therefore related to geo-graphical distribution. For example, a within spe-cies comparison ofArenicola marina populationsin a latitudinal cline revealed that both low andhigh T values were lower in cold adapted, sub-c

Arctic animals from the Russian White Sea thanin boreal, North Sea specimens(Sommer et al.,1997). High critical temperatures close to 238Cwere found in eelpout from the North Sea andclose to 98C in eelpout from the Antarctic(vanDijk et al., 1999). Even lower ‘heat tolerance’limits of 2–3 8C were found in an Antarcticbivalve, Limopsis marionensis (Portner et al.,¨1999a).The width of the window between the two pejus

temperatures as well as between critical tempera-tures reflects the amplitude of temperature fluctu-ations in the habitat of a species. The tolerancewindow is large in tropical and temperate speciesand narrow especially in polar areas(Fig. 1) andmost notably in the Southern Ocean where thestenothermal marine fauna is constantly exposedto temperatures ranging betweeny1.9 andq18C. Nonetheless, this window is not the same forall Antarctic species(for review see Portner et al.,¨2000). A preliminary comparison of the lifestylesof these species suggests that sessile epifaunaspecies are characterised by lower critical temper-atures compared with those of mobile species. Thecapacity of ventilation and circulation is higher inactive fish or octopods than in sessile bivalves,and this may be related to the higher pejus andcritical temperatures in more mobile compared tosessile Antarctic species.The question arises which are the mechanisms

determining the position and width of thermaltolerance windows. This involves the question towhat extent the mechanisms used during coldadaptation are similar or different in stenothermsadapted to permanent cold and in eurythermsadapted to tolerate seasonal cold. EspeciallyNorthern hemisphere species possess the ability toacclimatise and shift both low and high tolerancethresholds(T and T ) between seasons and in ap c

latitudinal cline(cf. Portner, 2001). On evolution-¨


Fig. 10. Model depicting the ‘hub’ of seasonal and permanent cold adaptation(modified after Portner et al., 2000). Eurythermal cold¨adaptation causes standard metabolic rate to rise(cf. Fig. 8) in relation to the degree of ambient temperature fluctuations and the coldcompensation of mitochondrial aerobic capacity and proton leakage. Adaptation to the permanent cold of Antarctic and high Arcticareas does not show this phenomenon owing to a compensatory reduction in energy demand and a rise in kinetic barriers(Arrheniusactivation energies) which compensate for the energy demand elicited by cold induced mitochondrial proliferation(cf. Portner et al.,¨2000).

ary timescales baseline constraints and trade-offsin cold adaptation, with which animals had to copeon the way from permanently warm conditions viaeurythermal to stenothermal cold need to beidentified.Evidently, adaptation to changing temperatures

involves escaping the threat of temperature inducedhypoxia (Portner et al., 1998, 2000). Acclimation¨to seasonal cold is well known to cause a rise inmitochondrial density or mitochondrial aerobiccapacity in fish(e.g. St.-Pierre et al., 1998; Gud-erley, 1998). This process is reversed during sea-sonal warming. High mitochondrial densities havealso been observed in Antarctic ectotherms adaptedto permanent cold, however, at respiratory capaci-ties of individual mitochondria which were foundreduced in the cold, according to the effect ofQ . Only recently has cold-induced mitochondrial10

proliferation been confirmed for a marine inverte-brate,Arenicola marina, in a comparison of sub-Arctic and temperate populations(Sommer andPortner, submitted). In contrast to Antarctic spe-¨cies, cold-adapted Arctic eurytherms displayed arise in mitochondrial aerobic capacity, which com-pensates for the temperature dependent decrement(Tschischka et al., 2000; Sommer and Portner,¨

submitted). These findings are in accordance withhigh costs of eurythermal vs. stenothermal coldadaptation and significant metabolic cold adapta-tion in eurytherms(Portner et al., 2000, 2001; Fig.¨10).The interpretation that temperature-induced

changes in mitochondrial densities and functionalcapacities are crucial in causing a shift of oxygenlimited thermal tolerance windows casts new lighton the functional role of these processes. In thesense that a function of high organisational com-plexity defines the limits of thermal tolerance thekey role of mitochondria does not neglect theimportance of integrated modifications in lipidsaturation, kinetic properties of metabolicenzymes, contractile proteins and transmembranetransporters(cf. Johnston, 1990; Hazel, 1995; Tikuet al., 1996; Storelli et al., 1998; Portner et al.,¨1998), all of which will contribute to the optimi-sation of higher functions within the window ofthermal tolerance. Since each of these mechanismsis also found in unicellular pro- and eukaryotes,the larger tolerance windows of these groups com-pared with metazoa(see above) suggests that theindividual mechanism alone does not provide akey to understanding thermal limits in metazoa.


Only the combination of these mechanisms includ-ing the adjustment of mitochondria enables higherfunctions to take place. Mitochondrial changes areonly part of the overall picture but crucial tounderstand the aerobic capacity adjustments incold and warm adapted animals. In the context ofan oxygen limitation of thermal tolerance mito-chondrial adjustments are closest to setting thelevel of aerobic energy available to the organism,especially if it concerns mitochondrial contents oftissues involved in circulatory and ventilatory per-formance and its neural control.

5.1. Mitochondria in the cold providing insufficientaerobic energy

Mitochondrial density andyor capacity reflectthe level of aerobic scope of the whole animal.On the one hand, this capacity can only be madeavailable if PO is kept high in the body fluids2

which requires sufficient ventilation and circula-tion. On the other hand, limited capacity of mito-chondria to produce energy in the cold is likely tocontribute to the loss of function and scope, e.g.in circulation and ventilation. Limitations in theavailability of aerobic energy may therefore be thekey to understand why an increase in mitochon-drial aerobic capacity occurs during resistanceadaptation to cold(Portner et al., 1998, 2000), in¨parallel with a temperature-dependent adjustmentof contractile functions. These processes lead to adownward shift of the low temperature thresholds(critical and pejus). Cold adaptation of metabolicparameters as observed in water breathers alsooccurs in air breathers such as weevils and moun-tain beetles(Chown et al., 1997; Dahlhoff andRank, 2000, for review see Chown and Gaston,1999).

5.2. Limits to cold adaptation

The capacity to overcome the oxygen limitationof cold tolerance by mitochondrial adjustmentswill be limited by the freezing of body fluids or,as found in the case of marine reptant decapodcrustaceans, by high magnesium levels in the bodyfluids. The latter constraint is discussed to explainwhy this group is almost completely absent inareas of the Antarctic and the Arctic with perma-nent subzero water temperatures(Frederich et al.,2000a). Since magnesium acts as a natural calciumantagonist at neuromuscular junctions it exerts an

anaesthetising effect, especially in the cold, andthereby restricts ventilatory and circulatory capac-ities (Frederich et al., 2000b). In consequence,magnesium limits aerobic scope and thereby exac-erbates the oxygen limitation of cold tolerance.Obviously, reptant decapods could not overcomethis limitation by cold-induced mitochondrial pro-liferation. Only a reduction in haemolymph mag-nesium levels enabled other crustaceans likeamphipods, isopods and shrimp to occupy thoseniches in polar areas which in other oceans areusually dominated by benthic crabs(Frederich etal., 2001).At temperatures below freezing the presence of

antifreeze protection or passive freeze toleranceextends the range of cold tolerance. Polar fishesface the problem of sea water temperatures belowthe freezing point of their body fluids(y1.9 8Cvs. y0.9 8C). Elimination of the threat of coldinduced hypoxia by cold adaptation of the meta-bolic machinery(see above) could, therefore, onlybecome effective in combination with the devel-opment of antifreeze proteins, as an evolutionaryprecondition for fish life in the Antarctic and inthe Arctic (for review see DeVries, 1988; Fletcheret al., 1998; Wohrmann, 1998). Whereas antifreeze¨proteins in polar fish support an active mode oflife at permanently low water temperatures, anti-freeze protection or freeze tolerance in terrestrialenvironments also becomes important at tempera-tures well below the range of optimum physiolog-ical performance, e.g. during seasonal cold.Accordingly, supercooling points and lower lethallimits in insects were found to be correlated withgeographical distribution(Addo-Bediako et al.,2000) since such mechanisms guarantee passivesurvival during unfavourable seasonal conditions.

5.3. Mitochondria in the warm contributing tohigh oxygen demand

What are the consequences of a mitochondrialdensity adjusted high in the cold when the animalis exposed to high temperatures? As outlinedabove, the increase in oxygen demand duringwarming may become a problem at high temper-ature. It has only recently become clear that oxy-gen demand is not only related to cellular energyrequirements but some baseline oxygen demand isalready caused by the mitochondria present andtheir functional properties. Oxygen demand ofmitochondria is not only defined by the maximum


rate of coupled respiration in the presence ofsubstrate and ADP(state 3 respiration) but alsoby the rate of proton leakage across the innermitochondrial membrane. Mitochondrial protonleakage in the resting cell comprises a constantlylarge fraction of standard metabolic rate(Brand,1990; Brand et al., 1994). It accounts for 25% ofbaseline metabolism in rat hepatocytes, for 50%in skeletal muscle and for 20–30% in the wholeanimal (Brand et al., 1994; Rolfe and Brand,1996). Proton leakage reflects the baseline idlingof mitochondria, and on top of the cost of biosyn-thesis and degradation accounts for the cost ofmitochondrial maintenance(Portner et al., 1998).¨The relative contribution of proton leakage tostandard metabolic rate(SMR) is similar in ecto-therms and endotherms(Brookes et al., 1998).Moreover, SMR is related, by a more or lessconstant factor, to maximum aerobic capacity ofthe organism(Wieser, 1985; Brand, 1990; Lind-stedt et al., 1998). Proton leakage will thereforecontribute to the warm induced increase in SMR.Recently, the temperature dependence of Hq

leakage was investigated in mitochondria fromtissues of two Antarctic species, gills of thebivalve,Laternula elliptica (Portner et al., 1999b)¨and liver of the notothenioid fish,Lepidonotothennudifrons (Hardewig et al., 1999). The change inproton leakage with temperature was more or lesscontinuous, with constant but very high Arrheniusactivation energies. The thermal sensitivity of pro-ton leakage cannot be explained by a change inproton motive force(Dp), which scarcely varieswith temperature(investigated in mammals byDufour et al., 1996, and in Antarctic bivalves andfish by H.O. Portner and T. Hirse, unpublished).¨Whatever the mechanism of proton leakage, itshigh thermal sensitivity suggests that the futilecycling of protons may increase to a similar oreven larger extent than resting ATP turnover athigh temperatures. Thereby it likely contributes tothe exponential rise in oxygen demand duringwarming. Owing to the progressive limitation ofventilatory and circulatory capacity(Figs. 3 and5) this rise in oxygen demand would contribute tothe drop in haemolymphPO beyond T as2 p

observed inMaja squinado (Frederich and Portner,¨2000) and Laternula elliptica (H.O. Portner, L.S.¨Peck and T. Hirse, unpublished) or in venousblood of the cod(Gadus morhua, I. Serendero, G.Lannig, F.J. Sartoris, H.O. Portner, unpublished).¨Finally at T , ventilation and circulation fail toc

meet baseline oxygen requirements. Accordingly,mitochondrial baseline oxygen demand will con-tribute to the limited aerobic performance beyondthe upper pejus temperature(T II) and becomep

detrimental at the critical temperature(T II). Asc

a corollary, the reduction of mitochondrial densityobserved during warming leads to a reduction ofbaseline oxygen demand, thereby allowing theupperT to shift to higher values. These consid-c

erations have been considered in the model out-lined in Fig. 8. Some increase in oxygen demandwill also result from the exponential increase incell membrane and epithelial permeability uponwarming (Moseley et al., 1994), which requiresenergy for the compensation of dissipative ionmovements.

6. Perspectives: the hub of metabolic coldadaptation

According to the foregoing chapter the adjust-ment of mitochondrial densities and propertiesappears as one key mechanism contributing to theunidirectional shift in both low and high pejus andcritical temperatures. In accordance with the pre-diction mentioned earlier this mechanism linksupper and lower thermal tolerance thresholds.Enhancing mitochondrial capacity in the cold elim-inates the capacity limitations of ventilation andcirculation. Reduction of mitochondrial capacity inthe warm reduces the oxygen demand of mito-chondrial maintenance and leaves enough aerobicenergy for ventilation and circulation to maintainaerobic scope.These considerations lead to the conclusion that

a cold-induced rise in mitochondrial densitiesshould cause elevated costs of mitochondrial main-tenance and a rise in standard metabolic rate asseen in temperate ectotherms during winter coldor in eurythermal, esp. Northern hemisphere pop-ulations along a latitudinal cline. However, adap-tation to the permanent cold of polar areas and thedeep sea has led to life forms that do not displaya significant cold induced rise in metabolic rate(e.g. Clarke and Johnston, 1999). Using the base-line considerations of mitochondrial contributionsto standard metabolism outlined briefly above,Portner et al.(2000) elaborated a model(Fig. 10)¨that would explain the differences between coldstenotherms and eurytherms and that would alsoexplain why adaptation to permanent cold causedAntarctic species to become obligatory stenoth-


erms. Compared with eurythermal cold this maybe a secondary situation linked to reduced mito-chondrial capacities and increased Arrhenius acti-vation energies(E ) of mitochondrial oxygena

demand, especially proton leakage, and of fluxlimiting enzymes in metabolism like isocitratedehydrogenase(Portner et al., 2000). A high¨kinetic barrier may support low metabolic flux incold stenotherms despite mitochondrial prolifera-tion. In contrast, temperature dependence isreduced and flux is facilitated in other, e.g. equi-librium enzymes like lactic dehydrogenase(Hochachka and Somero, 1984). While E ofa

overall metabolism appears to be reduced in activewinter acclimated animals(cf. Portner, 2001), high¨E values in Antarctic species reflect a high tem-a

perature dependence of metabolism and, in con-sequence, a reduced heat tolerance of the wholeorganism. According to Fig. 10 cost of mainte-nance rises in cold adapted eurytherms to levelshigher than in cold stenothermal animals. As atrade-off growth and reproduction are reduced orsuspended in cold eurytherms, whereas in steno-thermal animals aerobic capacity and even moreso baseline energy expenditure are minimised tofree metabolic energy for growth and reproductionprocesses in the cold.Finally, recruitment failure of a species depend-

ing on climate change appears as a consequenceof the thermal limitations(loss in aerobic scope)discussed in the present review. The predictionalso arises that in those cases, where juvenilestages may prove more sensitive to temperaturechange than adults of the same species, the prin-ciples outlined in the current paper will still bevalid, i.e. thermal sensitivity likely results at thehighest level of complexity and relates to thecapacity of the oxygen supply system, which maybe more sensitive to environmental changes duringthe period of embryonic and larval developmentthan during the period of adult growth and repro-ductive activity. These relationships need to beaddressed in future efforts to extend our knowledgeon the role of aerobic scope in limiting thermaltolerance and geographic distribution in variousgroups of animals.

Acknowledgments

A contribution to the ELOISE project: Effectsof climate induced temperature change on marinecoastal fishes(CLICOFI), funded by the European

Union program ‘Climate and environment’, con-tract No. ENV4-CT97-0596. The author wishes tothank Dr Franz Riemann for providing informationon the thermal tolerance of nematodes.

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