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Freeze Tolerance vs Freeze Avoidance

Updated on March 10, 2011

To freeze or not to freeze? A discussion of freeze tolerance and freeze avoidance as coping strategies in animals at subzero temperature

A large proportion of the earth’s species live in regions which experience subzero temperatures. Extremely cold temperatures damage cellular structures and interfere with biological processes. Ectotherms are especially vulnerable to cold, as they are unable to regulate body temperature. Therefore, many species have evolved physiological coping strategies to minimise the effects of ice formation – specifically, Freeze Avoidance (FA) and Freeze Tolerance (FT).

The FA strategy maintains internal fluids in a supercooled state, and aims to remove all possible ice nucleating agents. It is common to stable, more extreme climates, has high initial and ongoing stress and energy costs, and a high risk of death should flash freezing occur. By depressing the freezing point of internal fluids, this strategy attempts to avoid ice formation entirely. FT promotes premature, controlled ice formation in extracellular spaces, carries high risk of freeze and thaw damage and incurs long terms debt from accumulated waste and stress. However, it requires very low initial investment or ongoing maintenance and allows individuals to survive at 5-40°C lower than with FA. Both share mechanisms common to anoxia and dehydration survival.

Survival of subzero temperatures is a complex and diverse topic, and alternate survival strategies, and applications of FA and FT, exist – cryoprotective dehydration, ‘mixed’ FA and FT, and the ‘bet hedging’ switch from FT to FA. This area is complex and not fully understood, with most research focussing on the physiological aspects, not the evolutionary history.

Introduction: Freezing Ecology and Strategies


A large number of the Earth’s biota are temperate and polar dwelling species, that will experience temperatures nearing and below the freezing point of water (Sømme, 1995). These cold periods can be variable or constant and extend down to -70°C.

Subzero temperatures are a significant risk to the survival of animals. Cold slows reactions and negatively affects metabolic processes, and ice formation physically damages internal membranes and causes osmotic stress (Storey & Storey, 1992a). This leads to cell dehydration and the disruption of chemical gradients (Franks et al, 1990; Mazur, 1984; Voituron et al., 2009) which is eventually fatal.


As ectotherms are dependent on internal energy sources, and cannot regulate their own body temperature, they need to find other ways of coping with the cold (Voituron et al., 2009). Many ectotherms have developed coping strategies to reduce the impact of cold temperatures. These range from behavioural (hibernation under mud, migration to warmer areas, annual lifespans) to physiological. Physiological strategies include Freeze Tolerance (FT) and Freeze Avoidance (FA) (Warren et al., 2001; Lee, 1991; Salt, 1961). FT species actively encourage early ice formation in extracellular spaces, while FA species prevent ice formation by supercooling their body liquids to well below freezing point and removing potential ice nucleators.

However, the physiological mechanisms and evolutionary history of these strategies are still a source of much speculation. The majority of research in has been done on insects, anurans and hatchling turtles (Sinclair et al., 2003; Voituron et al., 2009). It is now known that FA and FT are not exclusive, nor are they the only mechanisms for coping with freezing temperatures in animals.

More recently, ‘mixed’ strategies have been discovered (Voituron et al., 2009), and species that switch from FT to FA after freezing attempts (Salt, 1961; Voituron et al., 2009; Zachariassen, 1985). Finally, cryoprotective dehydration has been discovered in a recent study on the arctic springtail Ohychiurses arcticus (Holmstrup et al., 2002; Voituron et al., 2009).

Freeze Avoidance

Freeze Avoidance occurs more frequently in the benthos, subterranean regions (Costanzo et al., 1992; Storey & Storey, 1986; 1988; Swanson & Graves, 1995), and the northern hemisphere – areas which experience more predictable (e.g. seasonal) and longer lasting cold periods for more species, due to the greater landmass in the temperate and polar regions (Sinclair & Chown, 2005). For example, the hatchling painted turtle (Chysemys picta) can survive in a supercooled state for weeks, at a temperature of 12°C (Packard & Packard, 2004).

FA species use more than one method to supercool internal fluids and prevent ice formation. The first method is the induction of passive dehydration, as water possesses a higher water vapour pressure than ice, at the same temperature (Voituron et al., 2009). High sugar or sugar alcohol carbohydrates - usually glycerol, which can reach up to 20% of body mass, distributed evenly throughout the body, intra- and extracellular spaces – is used to depress the freezing point (Pfister & Storey, 2006). FA insects exhibit a breakdown rate of glycogen to glycerol that us about five times higher than that of FT insects (Chapman, 1998). Secondly, FA species accumulate low molecular weight cryoprotectants, and/or the produce antifreeze proteins, which bind to the ice crystals (Pfister & Storey, 2006; Voituran et al., 2009).

FA species attempt to avoid ice nucleators – any particle which can trigger a flash freezing event – through various physiological and behavioural strategies. For example: waterproofing (e.g. a wax cuticle (Duman, 2001); movement to a dry site (Marchand, 1996); cessation of feeding, and emptying the gut, and seasonal proteins to remove potential ice nucleating structures (Olsen & Duman, 1997).

The physiological consequences of supercooling fluids include the effects of higher vapour pressure (when compared to ice) (Zachariassen, 1991). Water loss through evaporation, negative effects on behaviour once thawed and an increased risk of freezing via inoculation (Packard & Packard, 1993b) which seeds ice into extracellular spaces. This fatal reaction can be due to escaping vapour freezing nearby and spreading back to the animal (Salt, 1963). Supercooling leads to a high risk of flash freezing, should ice be introduced to the system. Due to the extreme low temperature, freezing is instantaneous, more physical damage is caused, and a higher percentage of body fluid frozen, with consequences for internal osmotic processes (Claussen et al., 1990; Storey & Storey, 1992b; Swanson et al., 1996). The larger proportion of frozen fluids and smaller proportion of liquid, increases dehydration and causes rapid post-nucleation cooling rates, swiftly decreasing survival (Costanzo et al., 1991).

Freeze Tolerance

FT differs from FA in that ice nucleating agents (INAs) are inactive or absent (Duman, 2001), with ice prevention restricted to the intracellular spaces. Both strategies use polyols and antifreeze proteins, but use these for different functions (Duman, 2001). FT is more common in shallow waters, terrestrial regions (Costanzo et al., 1992; Storey & Storey, 1986; 1988; Swanson & Graves, 1995) and the southern hemisphere, due to the less extreme and more variable cold periods (Sinclair & Chown, 2005).

Insects exhibiting FT freeze at below -10°C, and can survive in this frozen state at temperatures of -30°C to -70°C. This gives them a buffer of 5-40°C past the initial freezing temperature, or supercooling point (SCP) before the cold becomes fatal (Bale, 2002; Brown et al., 2004). Freeze tolerant species can survive long periods of time with a large percentage of their body water frozen. For example, the wood frog, Rana sylvitica, can survive at least two weeks, with 65% of its body water frozen (Storey & Storey, 2004).

In anurans, ice formation in the extremities triggers liver glycolgenolysis. This increase blood glucose levels throughout the animal within a few hours (Voituron et al. 2009). Concentration jumps from -5mM to 150-300mM (Storey & Storey, 1984). Most species exhibit extreme hyperglycaemia, large liver glycogen reserves and high hepatic activity of glycogen phosphorylase (Edwards et al., 2000).

The accumulation of low molecular weight cryoprotectants (usually glycerol or glucose) (Storey & Storey, 1984) is significant enough in the freeze tolerance process that tissue carbohydrate levels are a critical determinant of FT (Costanzo et al., 1993; Swanson et al., 1996).

Risks include the damage from the freeze-thaw cycle, to cellular membrane structures and processes (Mazur, 1984; Sinclair & Chown, 2005) and damage from secondary ice formation. Once frozen, reliance shifts to anaerobic metabolism, as the temperature inhibits, and then shuts off, the circulatory system. Lactic acid and other end products accumulate and affect end behaviour after thawing (Packard & Packard, 2004).

Evolutionary and Physiological Aspects of Freezing Coping Strategies

The recent study by Voituron et al. (2002) proposed a formal model for the evolution of FA, FT and mixed strategies [Figure 1]. Many studies have focussed on the physiological responses to freezing (Voituron et al., 2009), especially the link between dehydration and freezing (Costanzo et al., 1993; Edwards et al., 2004; Swanson et al., 1986). The possible evolutionary role of FT mechanisms in water conservation is supported by the importance of urea as a cryoprotectant, by balancing osmolytes, in R. sylvitica (Costanzo & Lee, 2005). Glucose accumulation is also triggered by dehydration (Storey & Storey, 2004). However, most of these studies are greatly weakened by the lack of genetic relatedness among the study species (Garland et al., 2005) – with the exception of Irwin & Lee (2003). This study on closely related species of gray tree frog was also the first to raise the issue of frequency of FT or FA appearance over time (Irwin & Lee, 2003; Voituron et al, 2009). But what is known is that FT has evolved separately, at different times, among anurans (Voituron et al, 2009) and therefore is almost certainly not a genetic quirk, but a genuine and repeated response to unknown evolutionary pressures.

Knowledge of the mechanisms of freezing is still insufficient. While even closely related species demonstrate very different physiological responses, the actual steps are unknown (Anderson et al., 1983; Voituron et al., 2005; Voituron et al, 2009). Ability to withstand temperature decreases may not even be a result of freezing method, but simply how great a degree of frozen body fluid a species can survive – for example, mandarin leaves can tolerate a higher degree of frozen tissues than lemon leaves (Anderson et al., 1983).

Figure 1: An Optimisation Model For Cold Hardiness

An Optimisation Model For Cold Hardiness
An Optimisation Model For Cold Hardiness

Acclimation and Other Factors

While Anderson et al. (1983) looked at citrus leaves, rather than animals, the factors of freeze tolerance are applicable across all species: specifically: freezing initiation; minimal temperature experienced (and variability of temperature), and the degree of acclimation of the organism. Acclimated individuals consistently freeze at a lower temperature than their unacclimated counterparts (Anderson et al., 1983) and Swanson et al. (1996) found that phosphorylase activity increased with cold acclimation in frogs.

Links to Anoxia

Reese et al. (2004) raised the possible connection between anoxia tolerance in hibernation and in a supercooled state, in hatchling turtles. Hatchling painted turtles (Chrysemys picta) were allegedly a case of ‘unique natural freeze tolerance in amniotic vertebrates’ (Churchill & Storey, 1992) that could survive with 50% frozen fluids without antifreeze proteins, by removing IMAs from internal fluids and using the integument as a barrier against ice penetration (Storey, 1992; Storey et al., 1988; Storey & Storey, 1992b; 1999). However, later studies could not duplicate hatchling survival lower -3°C, and concluded that the original result was an artefact of laboratory based study, in which the hatchlings were not consistently frozen, and the natural ecology of the species was not taken into account, and they in fact exhibited FA (Churchill & Storey, 1992; Claussen et al., 1990; Costanzo et al., 1995b; Packard & Packard, 2004).

Mixed strategy responses

True mixed strategy species are rare (Voituron et al., 2002), but have been previously studied (Ring, 1982; Horwath & Duman, 1984b). However, Voituron (2004) concluded that a mixed FA/FT response was the most energetically advantageous option in variable environments.

Repeated Freeze-Thaw Events: ‘bet hedging’

It was assumed that FT species remain FT through successive freeze-thaw cycles during winter. However, Brown et al. (2004) found that, in a study of the freeze-tolerant larva of the hoverfly Syrphus ribesii, the first freezing event triggered freeze avoidance in the majority of the larva. A smaller number remained FT, but displayed a depressed SCP 15-20°C lower. A second freezing event proved fatal to the now FA larva, and repeated freezing severely reduced survival/emergence rates. Again, insufficient data regarding the mechanisms involved exists to explain this result - this reaction does not match a ‘mixed’ response, as described in Voituron et al. (2004).

It is possible that the first freezing destroyed or distorted the ice nucleation surface (Brown et al., 2004; Duman, 2001; Duman et al., 1992). However this does not account for the split in the initial group of larva, with no later events. The switch from FT to FA would reduce the negative effects of the freeze-thaw cycle, such as secondary recrystallisation (Bale, 2002; Knight et al., 2004) by suppressing the freezing point to – hopefully – below the lowest occurring temperature. Any subsequent freezing would prove fatal, but the magnitude of SCP depression was so great in some individuals, that the risk of reaching the flash freezing point was very low (Brown et al., 2004). It was hypothesised that the FT-FA switch would act as a failsafe in variable climates, and would not occur in harsher, more predictable, climes. This is borne out by the repeated freezing of New Zealand alpine insects (Sinclair, 2001) and the occurrence of this ‘bet hedging’ strategy in the beetle Hydromediom sarsatum (Bale, 2001). Insects can rapidly alter freezing point or freezing response (Worland & Convey, 2001).

Cryoprotective Dehydration

Discovered in the Arctic springtail Onychiurus articus cryoprotective dehydration is another response to low temperatures (Holmstrup et al, 2002). Cryoprotective dehydration uses wholly different processes to FA and FT. Rather than preventing body fluids from freezing; these species proactively remove water from the body [Figure 2] (Holmstrup et al, 2002; Sinclair et al., 2003; Voituron et al, 2009).

Figure 2: Cryoprotective dehydration - a third strategy

Cryoprotective dehydration - a third strategy
Cryoprotective dehydration - a third strategy


Freeze Tolerance and Freeze Avoidance are markedly different strategies that share common mechanisms and chemicals. Both are effective under specific energetic and climatic conditions. While FT is known to have evolved several times from FA species, little more is known about the evolutionary history of these coping strategies. Conjecture can be made using the formal model of energy and fitness, and this, along with the rarer, more diverse and less well understood stratagems (i.e. cryoprotective dehydration, mixed, ‘bet hedging’) are likely to be highly rewarding topics for further research.


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      2 years ago

      I remarked 5stars to this I think it should be 8..thank u.. :) :)

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      well written article!


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