Cold hardiness classifications

The classification of insect cold hardiness strategies has essentially revolved around whether the temperature at which ice nucleation, or freezing of the body fluids, starts to take place in the extracellular spaces (the crystallization temperature, Tc, or SCP) represents the LLT for the insect. If it does not, then clearly the animal has some measure of freezing tolerance, whereas if the SCP and LLT are equivalent, the animal is freeze intolerant. In Section 5.2.3, we showed that in many species the LLT is much higher than the SCP, and thus there is considerable pre-freeze mortality. Likewise, in Section 5.1.2 we have pointed out that the period over which an insect is exposed to subzero temperatures also has an influence on its ability to survive these conditions. It has been shown that some species can only tolerate partial extracellular ice formation (i.e. they die if ice formation goes to equilibrium) (Sinclair et al. 1999), others can tolerate freezing even though they have very low SCPs (Ring 1982), and yet others can switch between a strategy of freezing tolerance and freeze intolerance (Kukal and Duman 1989). Bale (1993, 1996) first proposed that the dichotomous, freezing tolerant-freeze intolerant classification should be modified to encompass the complexity of the response of insects to subzero temperatures. Recognizing the importance of pre-freeze mortality and exposure time, Bale (1993, 1996) proposed that the following classes of cold hardiness should be recognized within the freeze intolerant category (Fig. 5.17):

1. Freeze avoiding species show little to no mortality at temperatures above their SCPs, even after exposure over a full winter season, and include species such as the goldenrod gall moth Epiblema scudderiana (Lepidoptera, Olethreutidae).

2. Highly chill tolerant species can survive prolonged exposure to low, subzero temperatures but there is some mortality above the SCP. In the Antarctic springtail, Cryptopygus antarcticus, the SCP is approximately —25°C in winter, but more than 20 per cent of the population does not survive winter cold.

3. Moderately chill tolerant species also have a relatively low SCP, but here survival at low temperatures above the SCP is low. As an example of this class Bale (1993) used Rhynchaenus fagi (Coleoptera, Curculionidae), which has an SCP of —25°C in winter, but which shows less than 30 per cent survival after 50 days at —15°C.

4. Chill susceptible species can survive temperatures below 0-5° C, but show considerable mortality after very brief exposures to relatively high subzero temperatures. For example, Myzus persicae (Hemiptera, Aphididae) has an SCP of c.—25°C, but mortality increases from 0 to 100 per cent after just a few minutes below 5°C.

Retain freezable water

Retain freezable water

Insect Cold Hardening

Killed by internal ice formation

Decreasing LLT

Figure 5.17 Schematic diagram illustrating the classes of cold hardiness characteristic of insects.

Remove freezable water

Partially

Remove freezable water

Partially

Wholly

Wholly

Anhydrobiosis

Cryoprotective dehydration

Killed by internal ice formation

Anhydrobiosis

Decreasing LLT

Figure 5.17 Schematic diagram illustrating the classes of cold hardiness characteristic of insects.

Note: CS chill susceptible, FA freeze avoiding, HCT highly chill tolerant, L freezing tolerant with low SCP, M moderate freezing tolerance, O opportunistic, P partial freezing tolerance, S strong freezing tolerance.

Source: Modified from Sinclair (1999).

5. Opportunistic species generally show considerable mortality at or just above 0oC when exposed to such temperatures for more than a few days. In environments with cold winters, these species usually avoid low temperatures by seeking thermal refugia.

Clearly, the species discussed in Section 5.2.3 that show rapid cold hardening, and an upregulation of polyhydric alcohols and heat shock proteins in response to cold, fall somewhere between the chill susceptible and moderately chill tolerant species. In addition, this classification illustrates the necessity of understanding the microenvironment within which an insect overwinters (Bale 1987; Sinclair 2001a).

Although there has been some debate regarding these new classes of cold hardiness, their utility has generally been widely recognized, especially with regard to better understanding the responses of insects to their natural environments. Indeed, in their investigation of a freezing tolerant caterpillar that dies at relatively high temperatures, Klok and Chown (1997) suggested that this freezing tolerant category could also usefully be broadened to recognize the variety of responses characterizing freezing tolerant species. Sinclair (1999) did just that. He recognized that some species survive only partial ice formation, others die only a few degrees below their SCP, while others can tolerate many degrees of freezing. Based on a quantitative investigation of the relationship between the SCP and LLT Sinclair (1999) recognized four classes of freezing tolerance:

1. Partial freezing tolerance. Here, individuals can survive some formation of ice in their bodies, but do not survive if ice formation goes to equilibrium at or above the SCP. This class is difficult to distinguish from freeze avoidance, because mortality may have a similar cause. A New Zealand lowland weta, Hemideina thoracica (Orthoptera, Anostostomati-dae), is one example of such a species.

2. Moderate freezing tolerance. These species freeze at a relatively high temperature and die less than 10o C below their SCP, in some instances can survive relatively long periods in a frozen condition, and generally occur in relatively mild climates. Pringleophaga marioni (Lepidoptera, Tineidae)

caterpillars from sub-Antarctic Marion Island have a mean SCP of —5°C and show 100 per cent mortality at —12.5°C (Klok and Chown 1997).

3. Strong freezing tolerance. In these species the LLT is substantially lower than the SCP. These include the 'classic' freezing tolerant species such as the goldenrod gall fly, Eurosta solidaginis (Diptera, Tephritidae), that freezes at —10° C, but dies below —50°C, and Arctic carabids that freeze at —10°C, but can survive temperatures lower than —80°C (Miller 1982).

4. Freezing tolerant with low SCP. These insects have extremely low SCPs, yet, can survive freezing a few degrees below their SCP. For example, Pytho deplanatus (Coleoptera, Pythidae) has a SCP of —54°C, but can survive freezing down to —55°C (Ring 1982).

The combination of Bale's (1993) and Sinclair's (1999) categories of programmed responses to cold (Fig. 5.17) provides a useful classification against which to assess the strategy of any given insect species. Although it might be argued that investigation of many more insect species might simply result in a cloud of points on Fig. 5.17, we are of the opinion that there are unlikely to be five million ways in which insects respond to cold (see Chapter 1).

Having recognized the continuum of classes of insect cold hardiness we now explore the characteristics of the two traditional categories, recognizing that there are likely to be characteristics that are unique to each of the nine classes identified above, and which are also shared between them. We limit our discussion of the third strategy, cryo-protective dehydration, to a small section owing to the fact that it has only been recorded, among insects, in the collembolan Onychiurus arcticus (Worland et al. 1998; Holmstrup et al. 2002).

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