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Journal of Thermal Biology 31 (2006) 332–336

www.elsevier.com/locate/jtherbio

What is thermal acclimation?

Kari Y.H. Lagerspetz�

Department of Biology, University of Turku, FIN-20014 Turku, Finland

Received 4 October 2005; accepted 10 January 2006

Abstract

Several recent contributions to this Journal have reflected on the current usage and understanding of the term acclimation [Bowler,

2005. Acclimation, heat shock and hardening. J. Therm. Biol. 30, 125–130; Loeschcke and Sfrensen, 2005. Acclimation, heat shock and

hardening—a response from evolutionary biology. J Therm. Biol. 30, 255–257; Sinclair and Roberts, 2005. Acclimation, shock and

hardening in the cold. J. Therm. Biol. 30, 557–562]. As a contribution to this discourse I propose that a look back into the introduction of

this term may provide a useful additional insight.

r 2006 Elsevier Ltd. All rights reserved.

Keywords: Acclimation; Resistance; Capacity; Definitions

1. Thermal biology of 50 years ago

Fifty years have elapsed since the publication of threescientific works important in thermal biology: the bookTemperatur und Leben, by Precht, Christophersen andHensel (1955), and the reviews by Prosser (1955) andBullock (1955), both in the same issue of the Biological

Reviews.These publications were received enthusiastically in

those biological laboratories where thermal biology wasactively pursued. Ten years after the end of the secondWorld War, there was still a shortage of common utilitiesin many European laboratories. For instance at Helsinki, agalvanometer and a thermocouple had been borrowedfrom the Physics Department, until such equipmentadapted for use in biology became commercially availablein 1954. But these three remarkable papers mentionedabove showed the international extent of research inthermal biology and gave further guidelines for it.

Now, 50 years later, it may be appropriate to look howthe ideas of Herbert Precht (1911–1992), C. Ladd Prosser(1907–2002) and Theodore Holmes Bullock (1916–) havepersisted in thermal biology. One of these was the concept

e front matter r 2006 Elsevier Ltd. All rights reserved.

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esses: karlag@utu.fi, kari.lagerspetz@utu.fi.

of thermal acclimation (Bowler, 2005; Loeschcke andSfrensen, 2005; Sinclair and Roberts, 2005).

2. Three definitions of acclimation

‘‘The capacity for acclimatization is beyond doubt one ofthe most remarkable of all the many mysterious attributesof living material’’ (Heilbrunn, 1952, p. 547). As in theearlier (1937, 1943) editions of his book on generalphysiology, L.V. Heilbrunn also, in the third edition,devoted a chapter to the subject of acclimatization tophysical and chemical factors, however without explicitlydefining it. Another important textbook, Comparative

Animal Physiology, edited by Prosser (1950), also gavemuch attention to adaptation (‘‘acclimatization’’) phenom-ena of individual organisms. Prosser (1955) definedphysiological adaptation as ‘‘any functional property of anindividual which favours continuous successful living in analtered environment’’, and used the term acclimation forphenotypic adaptive alterations of individual organisms.Species and populations gain adaptations through

evolution by selection, operating on generations ofindividuals on their hereditary properties. Adaptationsmay occur also during the life-time of a single individualand then be non-hereditary.To call the former genotypic and the latter phenotypic is

somewhat misleading, since by definition, any adaptation

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Fig. 1. The dependence of a biological function F on an environmental

variable E in three genotypes G1, G2 and G3. F0 is the survival limit of F

for the organisms (explained in the text).

K.Y.H. Lagerspetz / Journal of Thermal Biology 31 (2006) 332–336 333

must be expressed in the phenotype of individual organisms.Otherwise it could not affect the survival or maintenance of abiological unit and would not be discovered. In addition, anyproperty of organisms, inherited or not, has some genetic aswell as some environmental influences as its necessaryconditions.

Acclimation is commonly considered to mean a non-hereditary, usually reversible adaptation of an individual to asingle environmental factor, whilst acclimatization is used todenote a non-hereditary, usually reversible adaptation of anindividual to several, simultaneously changing environmentalfactors (Prosser, 1958). The adaptiveness of acclimationphenomena was a condition evident in the definitions givenby Prosser in 1950s and later (Prosser, 1986).

The change of biological rate function within normaltemperature range during temperature acclimation wascalled capacity acclimation (‘‘Leistungsadaptation’’), andthe change in thermal resistance of a function at extremetemperatures was called (cold or heat) resistance acclima-

tion (‘‘Resistenzadaptation’’) by Precht (1955, 1958).Capacity acclimations may extend normal functioningover a wider environmental range, resistance acclimationsmay confer better tolerance of the extremes. Resistanceacclimation is not restricted only to changes of thermalresistance of the whole organism, but may concern also itsseparate functions.

Precht (1949) defined five thermal capacity acclimationtypes (four if not counting ‘‘no acclimation’’ as a type ofacclimation). Among them were the type called inverse orparadoxical acclimation, in which the acclimation at atemperature increases further the immediate effects of thistemperature, and the type called overcompensation, in whichthe acclimation at a temperature decreases the immediateeffects below the original values before acclimation. Precht’stypes 1–5 show, that he intended to cover all, not only thereasonable (‘‘sinnvoll’’) and thus possibly ‘‘beneficial’’phenomena in his concept of acclimation (‘‘Adaptation’’).

Precht (1955) states this explicitly in Temperatur und

Leben (pp. 27–28). The expression ‘‘adaptation’’ means inthe first place nothing more than that time is a parameter in

adaptation. For instance, the beneficiality for the organismof a change in the activity of an enzyme caused by aprolonged change of holding temperature is not alwaysclear. Precht warns also against the perhaps subjectivemeaning of beneficiality to the individual or the specieswhich the expressions ‘‘adaptation’’ and also ‘‘acclimatiza-tion’’ may carry. According to Precht (1955), the adap-tiveness of acclimation phenomena may be a common, butnot a general property and it should not be included in thedefinition of acclimation. Precht also expressed thisopinion later: ‘‘It is therefore advisable to exclude theproblem of usefulness completely from consideration ofnon-genetic adaptations and to regard them as occurringwhen a change in AT [adaptation temperature] has anyconsequences that cannot be considered as direct re-sponses, but also not as regulations’’ (Precht et al., 1973,pp. 325–326).

Precht’s and Prosser’s definitions of acclimation differ inthis point. The definition of acclimation given by Bullock(1955) is intermediate between these. He uses the termacclimation for demonstrable compensations of immediatethermal effects.Three different definitions of acclimation were thus

proposed in 1955: (1) acclimation is an adaptive change

(Prosser), (2) acclimation is a demonstrable compensatory

change (Bullock), (3) acclimation is any change (Precht),caused by a change in an environmental variable (orvariables) in an individual organism and (usually) rever-sible during its lifetime.

3. Why acclimation is so common?

Whatever the definition, at least assumed acclimationphenomena have been found in all types of organismsstudied, and in respect to many environmental variables.The capacity for acclimation has sometimes been calledacclimability and it is pertinent to ask why is it so commonin organisms? There are two mutually compatible answersto this question. The first of these comes from evolutionarybiology and the second from thermodynamics.

3.1. Acclimation preserves genetic diversity

Let us assume that in a population there are threedifferent genotypes, G1, G2 and G3. They differ fromeachother in possessing different genes which affectdifferently a function F, which depends on an environ-mental variable E. A necessary condition for the survival ofthese organisms is that the value of F is larger than a limitvalue F0 (Fig. 1). This assumption sets the tolerance limitsof individuals.In an organism having genotype G1, F4F0 at E1 and E2,

in those with genotype G2, F4F0 at E1, E2 and E3, and inthose with genotype G3, F4F0 at E2 and E3. In otherwords, although all organisms of the population willsurvive at E2, only those with genotype G2 will survive atall three values of the environmental variable E. If E

changes from E2 to E3, organisms with G1 will die, and if E

changes from E2 to E1, organisms with G3 will die. Aftersuch changes only organisms with genotype G2 willsurvive. The variability of the population has thusdecreased, and if E now changes to values beyond E1 or

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Fig. 2. Hypothetical rate—temperature curves showing the relation

between the acutely measured temperature effect on cold-acclimated and

on warm-acclimated individuals and the curve when temperature is

changed slowly or time for acclimation is available at every temperature.

From Bullock (1955).

K.Y.H. Lagerspetz / Journal of Thermal Biology 31 (2006) 332–336334

E3, at which organisms with genotypes G1 and G3,respectively, would have survived, the population withonly G2 will die out.

Acclimability is a way to cope with this problem. Inacclimation, the F/E relationship is altered by a prolongedchange in E. If the F/E relationships of individualorganisms with G1 and G3 genotypes can, by acclimationto E2, shift F to such levels as found for G2 at E2, all thethree genotypes would survive changes from E2 to E3 andfrom E2 to E1. The population will thus retain geneticvariability enough to survive even a change of E to somevalues beyond E1 and E3.

The F/E relationship in Fig. 1 was assumed to follow anormal distribution, but it may be different in form, e.g.like that in Fig. 2, or unknown. The above reasoningconsiders only the resistance acclimation.

This example shows that individual acclimability preserves

genetic variability in a changing environment. If the individualorganisms can adapt to environmental changes by non-hereditary means, this not only increases the possibilities ofthe individual to survive, but through it retains the geneticvariability of the population, and also increases the chancefor survival of the whole population. This means that theacclimability of individual organisms enhances the survivalof the species, and it explains why species with acclimabilityas one of their characteristics are common.

3.2. Acclimation is the attainment of an altered steady state

The other, thermodynamic explanation of the common-ness of acclimation phenomena is linked with Precht’sdefinition of acclimation. Precht’s concept was expressedclearly by Grainger (1956, 1958), who pointed out, thatthermal acclimation phenomena could be explained astransitions from one steady state to another in an opensystem, such as organisms are. At a meeting, Grainger gavethis definition of acclimation:

I consider acclimation as meaning the changes whichtake place in a process in an organism up to the time

that the steady level is reached, after the organism hasbeen transferred suddenly from one temperature toanother within viable limits, regardless whether over-shoot is found or not (Grainger, 1958, p. 90).

Active living organisms are thermodynamically open,irreversible systems. In such systems, the production ofentropy is at its minimum when the system is in a steadystate (Prigogine and Wiame, 1946). An open system insteady state is also relatively stable. The attainment ofsteady state minimizes the energetic ‘‘cost of living’’, andtherefore its relative stability has a positive survival value.This does not imply that the metabolic rate of organismswould be at a minimum at the acclimation temperature,not even at the ‘‘basal’’ rate, because many energyconsuming functions may be activated at that temperature.It is meaningless to ask whether the transition of an open

system or any of its variables from one steady state toanother is ‘‘beneficial’’ or not, and it is hard to conceivethat any temperature biologist would ever had seriouslyconsidered all acclimation phenomena to be ‘‘beneficial’’. If‘‘adaptationism’’ is ‘‘panglossian’’, both the assumeddefence and the critique of the ‘‘beneficial acclimationhypothesis’’ (Leroi et al., 1994; Huey and Berrigan, 1996)seem slightly quixotic.Leroi et al. (1994) state the beneficial acclimation

hypothesis (BAH) in the following words: ‘‘acclimation toa particular environment gives an organism a performanceadvantage in that environment over another organism thathas not had the opportunity to acclimate to that particularenvironment’’. They consider the presumption of benefit tobe an empirical issue that needs experimental verification:‘‘That acclimatory responses are beneficial is not axiomati-cally true.’’ (Leroi et al., 1994, p. 1917).However, I think a point can be made for the converse

statement: it is axiomatically true that all acclimatoryresponses are not beneficial. If BAH, as stated by Leroiet al. (1994) would be valid, then the temperature range ofeach species could be extended by acclimation indefinitelyto both directions. Such BAH is impossible to defend andeasy to attack. It has been tested empirically already about50 years ago.Earl Segal, a former student of T.H. Bullock, studied in

late 1950s the temperature dependence of oxygen con-sumption and the cold resistance of the slug Limax flavus

acclimated to five different temperatures from 2 to 30 1C.He concluded: ‘‘It appears as though L. flavus has anoptimal acclimation temperature; the animals acclimatedto the extremes are not necessarily the ones that do best atthose temperatures. Limax shows an optimal acclimationtemperature both in metabolic compensation and insurvival at low temperatures’’ (Segal, 1961, pp. 242–243).However, as Wilson and Franklin (2002) express it, the

recent tests of BAH have given some interesting results ondevelopmental phenotypic plasticity, also called ‘‘ontoge-netic adaptation’’. Some of it is irreversible during the lifeof the individual.

ARTICLE IN PRESSK.Y.H. Lagerspetz / Journal of Thermal Biology 31 (2006) 332–336 335

A possible case of beneficial acclimation (and ofdevelopmental plasticity) is the change of preferredtemperature and from relative eurythermy to stenothermycaused by cold acclimation in the water flea Daphnia magna

(Lagerspetz, 2000). Animals acclimated to 23 1C showslight preference for that temperature, but move freelybetween 11 and 28 1C, while animals acclimated to 14 1Cprefer this temperature and move freely only between 12and 20 1C. The transfer of Daphnia from 23 to 14 1C causesalso a change from parthenogenetic to sexual reproductionand thus a need of partners of the other sex to producefertilized resting eggs. The change of preferred temperatureand its more narrow range enhance female–male encoun-ters and sexual reproduction, which is necessary for theproduction of survivable resting eggs.

Convincing evidence for the concept of thermal acclima-tion as a transition between different steady states is givenby the recent study of Cossins and his group (Gracey et al.,2004), based on a cDNA microarray analysis of RNAisolated from seven tissues of the common carp (Cyprinus

carpio) acclimated to 30 1C, and then subjected to 23, 17, or10 1C for different time periods up to 3 weeks. Altogether3461 cDNAs were affected by cold acclimation, and ofthese 1949 had homology to previously described genes,but the rest were so far unknown. Among other changes,the activity of 252 genes common to all tissues wasincreased. This reveals the scale and complexity ofresponses caused by cold acclimation and supports thedefinition of thermal acclimation as a transition betweendifferent steady states of the organism.

If adaptiveness, especially in the sense of evolutionaryfitness is included as a condition in the definition ofacclimation, there are usually difficulties in finding how totest it, and in the testing. It is also clear that all changeswhich occur in a living organism after a temperaturechange cannot be towards the assumedly ‘‘beneficial’’direction, but there must be also some ‘‘costs’’.

4. Why are thermal resistance and capacity acclimations not

parallel?

This coupling of capacity and resistance adaptation doesnot necessarily always occur. Resistance adaptationappears to be more commonly present than capacityadaptation. But few papers exist in which bothadaptations are examined together in the same species(Precht, 1958, pp. 52–53).if different factors are involved in effecting ‘capacity’and ‘resistance’ acclimations then those factors maybe differently subject to selection in evolution. Thereis very little evidence to shed light on this (Bowler, 2005,p. 126).

These two quotations, taken from review paperspublished with an interval of nearly 50 years, show thatthe ideal case depicted in Fig. 5 in the review by Bullock(1955), and reproduced here as Fig. 2, is not very common.However, the figure defines the resistance and capacity

acclimations and their correlation in a clear way. Accord-ing to it, and to the other early papers, the same lifefunction of an organism (as oxygen consumption, heartrate, enzyme activity) may show both compensatorycapacity acclimation within the normal temperature rangeand meaningful resistance acclimation at the extremetemperatures, although this is not always the case.I will call resistance acclimation and capacity acclima-

tion of some function parallel if both the upper and thelower resistance values and the temperature dependenceof the function are shifted by a change of livingtemperature towards the same direction as the livingtemperature (as in Fig. 2).There are several difficulties in the attempt to find such

parallelity:

(1)

The function studied must be temperature-dependentand have a measurable changing point at each end ofthe approximate scale of living temperatures of theorganism.

(2)

Many easily measured biological variables are sums ofmany different and differently regulated functions.

(3)

Resistances to cold and heat must usually be deter-mined on different individuals.

For instance, the rate of oxygen consumption is avariable, which is actually a sum of the effects of numerousbiological functions. Locomotor activity, and the sponta-neous spike activity of the nerve cord are other examples ofsuch fuzzy functions, in which the different parts do notalways contribute to the total sum function similarly, ornot at all. For such variables, the correlation of theirresistance and capacity acclimations may be accidental,vary between different conditions, seasons etc., and there-fore be of less general significance.One of the first well studied cases of the effect of thermal

acclimation on enzyme activity is acetylcholinesterase (EC3.1.1.7) from trout brain (Baldwin and Hochachka, 1970).The specific activity of this enzyme in brain homogenates isnot affected by acclimation of fish to 2 or 17 1C, but theproduction of the two isoforms of the enzyme is different.As the temperature dependence of their substrate affinity(measured as Km) is different, the maximum enzyme-substrate affinity (minimum Km) shifts with the acclimationtemperature. Acclimation thus permits large changes inactivity in response to physiological changes in substrateconcentrations at the respective acclimation temperatures.Not enzyme activity, but its effective regulation is thebiologically important variable, and the mechanism of itsacclimation is the differential gene expression caused bychange in temperature.On systemic level, parallel resistance and capacity

acclimation may be found in well-defined functions witha relatively simple control mechanism, like the heartfunction in some insects, which is controlled by definitesmall neuron groups.

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The pulsation rate of the tubular heart of aquatic larvaeof the midge Corethra plumicornis (Chaoborus chrystallinus)shows for a change of holding temperature from 4 to 20 1Ca corresponding shift of about 2.5 1C upwards. The upperlimit of the heart function is shifted from 38.1 to 40.8 1C,i.e. by 2.7 1C and the lower limit by about 3–4 1C upwardsfrom 1.5 or 0.5 1C (Perttunen and Lagerspetz, 1956, 1957).The acclimation response ratio is approximately 0.2. This isa case of parallel resistance and capacity acclimations, andthe only such case in insects listed in the review by IngridPrecht (Precht, 1967). Even now it is hard to find reportson such parallelity in any animal.

It is difficult to know, which biological variables arethose really important for the organism. What are calledbiological functions are not always well defined. Thermalcapacity acclimation and heat and cold resistance acclima-tions of the same function are separate phenomena whichusually have different mechanisms.

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