Cold shock

Cold shock, or direct chilling injury (Chen et al. 1987), is a form of injury that results from rapid cooling in the absence of extracellular ice formation. It increases in severity both with an increase in cooling rate and the absolute temperature of exposure, and is also thought to be a significant cause of injury during freezing. Direct chilling injury is usually distinguished from the consequences of a long-term exposure to low temperatures, which is known as indirect chilling injury. In both cases, the absence of extracellular ice formation distinguishes these kinds of injury from those associated with nucleation or freezing of an insect's body fluids. However, these two forms of injury are quite distinct, or at least in the way that insects respond to them.

Direct and indirect chilling injury In Frankliniella occidentalis (Thysanoptera, Thripidae), rearing of individuals at 15°C (with or without cold hardening) prolongs the duration of their survival at —5°C compared to those maintained at 20°C prior to the —5°C exposure (Fig. 5.13). In contrast, hardening, or induced tolerance to cold, provides no improvement in survival of a prolonged —5°C stress irrespective of the temperatures at which the thrips were kept, but substantially improves survival of a rapid transition to —11.5° C (Fig. 5.14). Thus, McDonald et al. (1997) argued that these two physiological responses to cold are very

100 120 140 160 180 200 Exposure time (h)

Figure 5.13 Increases in duration of survival (mean ± SE) of a —5°C treatment in Frankliniella occidentals following rearing at 15°C compared to 20°C.

Note: The upper lines are data for hardened and non-hardened thrips at 15°C, whereas the lower lines represent thrips reared at 20°C.

Source: Reprinted from Journal of Insect Physiology, 43, McDonald et al., 759-766, © 1997, with permission from Elsevier.

100 120 140 160 180 200 Exposure time (h)

Figure 5.13 Increases in duration of survival (mean ± SE) of a —5°C treatment in Frankliniella occidentals following rearing at 15°C compared to 20°C.

Note: The upper lines are data for hardened and non-hardened thrips at 15°C, whereas the lower lines represent thrips reared at 20°C.

Source: Reprinted from Journal of Insect Physiology, 43, McDonald et al., 759-766, © 1997, with permission from Elsevier.

Exposure temperature (°C)

Figure 5.14 The improvement of survival (mean ± SE) of an acute low temperature treatment after hardening in Frankliniella occidentals thrips reared at 15 and 20°C.

Note: The upper lines indicate thrips that were hardened and the lower lines thrips that were not pre-treated.

Source: Reprinted from Journal of Insect Physiology, 43, McDonald et al., 759-766, © 1997, with permission from Elsevier.

Exposure temperature (°C)

Figure 5.14 The improvement of survival (mean ± SE) of an acute low temperature treatment after hardening in Frankliniella occidentals thrips reared at 15 and 20°C.

Note: The upper lines indicate thrips that were hardened and the lower lines thrips that were not pre-treated.

Source: Reprinted from Journal of Insect Physiology, 43, McDonald et al., 759-766, © 1997, with permission from Elsevier.

different, suggesting that the injuries themselves may well be distinct. A reversal in the relative abilities of F. occidentalis and another thrip species (Thrips palmi) to tolerate acute vs. chronic cold provides further support for this idea (McDonald et al. 2000). Chen and Walker (1994) reached a similar conclusion based on their investigation of the responses of D. melanogaster selected for greater tolerance to indirect chilling injury and to cold shock, respectively. They found that in each case tolerance increased, but that selection for improved survival of the one form of shock did not improve tolerance of the other. They concluded that the two forms of cold tolerance are based on rather different mechanisms. Again, these results suggest that the injuries caused by indirect and direct chilling are different.

Unfortunately, it is still not clear what the mechanisms of long-term chilling injury are, although prolonged exposure to cold often results in developmental abnormality (Lee 1991). In contrast, the causes of direct chilling injury are better known (Denlinger and Lee 1998; Ramlov 2000). Chilling induces fluid-to-gel phase transitions in membranes, which result in separation of membrane proteins and lipids, change membrane permeability, and cause a decline in the activity of membrane bound enzymes. This damage to the plasma membrane is thought to have a considerable effect on neurons and on neuromuscular transmission (Hosler et al. 2000). Support for this idea comes from several sources, but in particular from demonstrations that muscle contraction patterns during eclosion are altered following cold shock in S. crassipalpis (Yocum et al. 1994), and that adult flies fail to behave in a normal way if they have been exposed to cold shock as pharate adults (Kelty et al. 1996). Direct chilling injury also results in a decrease in enzyme activity, in protein structural changes and denaturation (Ramlov 2000), and possibly also in an increase in oxidative stress. In house flies, cold resistance is associated with an increase in superoxide dismutase, an enzyme responsible for converting oxygen free radicals into hydrogen peroxide and hydroxyl radicals, which in turn are rendered less toxic by glutathione (Rojas and Leopold 1996). Glutathione levels decline during prolonged cold exposure, further supporting the idea that oxidative stress contributes to cold shock. At the whole organism level, chilling injury not only leads to an increase in mortality, but is also associated with a decline in reproductive output (Coulson and Bale 1992).

Basal and induced cold tolerance The relationship between basal and induced cold tolerance has yet to be fully explored. Misener et al. (2001) found that in the presence of cycloheximide, a protein synthesis inhibitor, basal tolerance, that is, survival time of a — 7°C cold shock following 25°C, is substantially reduced in D. melanogaster adults compared to untreated controls. By contrast, cycloheximide treatment has no effect on adult flies that were hardened at —4°C for 2 h prior to cold shock. These results suggest that basal and induced responses to cold are distinct.

In contrast, in both D. melanogaster and D. simulans, the response to artificial selection for cold tolerance is markedly reduced in flies hardened prior to cold shock compared to those that were not acclimated. On this basis Watson and Hoffmann (1996) argued that the selection and hardening responses are based on similar mechanisms. Similarly, a field-based study of D. melanogaster revealed that the magnitude of the acclimation response did not differ between populations from cold and warm areas, although flies from the colder area had both a greater basal tolerance to a —2°C cold exposure and a greater tolerance following hardening at 4°C (Hoffmann and Watson 1993). However, this response was not consistent, and differed when a cold stress of —5°C was applied. Thus, it is not entirely clear what the relationship is between basal and induced cold shock tolerance and how it varies under different conditions. What is certain is that short-term acclimation at a sublethal temperature can considerably enhance tolerance of cold shock.

Rapid cold hardening

Traditionally, the response of insects to cold has been considered in the context of winter cold hardening or the 'programmed response' to an extended period of cold. However, beginning with the demonstration of rapid cold hardening in S. crassipalpis and several other insects by Lee et al. (1987), it has now become clear that in a variety of insect species a short-term exposure to a sublethal cold temperature can substantially reduce cold shock mortality (Table 5.1).

In S. crassipalpis, chilling at 0oC for as little as 30 min can increase survival of a — 10o C cold shock, although maximal protection usually follows a 2 h pretreatment (Lee et al. 1987) (Fig. 5.15). This pretreatment protection lasts for several hours although it declines within 20 days if flies are held at 0oC (Chen and Denlinger 1992). Curiously, exposure to an intermittent pulse of 15oC renews low temperature tolerance after 10 days at 0oC, suggesting that naturally occurring temperature cycles might be important for the maintenance of cold tolerance (see also Kelty and Lee 1999, 2001). Tolerance is, nonetheless, lost rapidly if the flies are returned to 25oC (Chen et al. 1991). Similar kinds of responses have been found in most of the other insects in which rapid cold hardening has been examined (Table 5.1). However, the rapid cold hardening response tends to decline with adult age and, like induced tolerance to high temperatures, can vary substantially between developmental stages (Czajka and Lee 1990). Generally, an increase in the chilling temperature reduces the hardening effect, although in several species it has become

Table 5.1 Insect species in which rapid cold hardening has been demonstrated

Species

Order

Family

Investigators

Dacus tyroni

Diptera

Tephritidae

Meats 1973

Sarcophaga crassipalpis

Diptera

Sarcophagidae

Lee et al. 1987

Xanthogaleruca luteola

Coleoptera

Chrysomelidae

Lee et al. 1987

Oncopeltus fasciatus

Hemiptera

Pyrrhocoridae

Lee et al. 1987

Drosophila melanogaster

Diptera

Drosophilidae

Czajka and Lee 1990

Musca domestica

Diptera

Muscidae

Coulson and Bale 1990

Sarcophaga bullata

Diptera

Sarcophagidae

Chen et al. 1990

Blaesoxipha plinthopyga

Diptera

Sarcophagidae

Chen et al. 1990

Drosophila simulans

Diptera

Drosophilidae

Hoffmann and Watson 1993

Culicoides variipennis

Diptera

Ceratopogonidae

Nunamaker 1993

Danaus plexippus

Lepidoptera

Danaeidae

Larsen and Lee 1994

Musca autumnalis

Diptera

Muscidae

Rosales et al. 1994

Spodoptera exigua

Lepidoptera

Noctuidae

Kim and Kim 1997

Frankliniella occidentalis

Thysanoptera

Thripidae

McDonald et al. 1997

Rhyzopertha dominica

Coleoptera

Bostrichidae

Burks and Hagstrum 1999

Cryptolestes ferrugineus

Coleoptera

Cucujidae

Burks and Hagstrum 1999

Oryzaephilus surinamensis

Coleoptera

Cucujidae

Burks and Hagstrum 1999

Sitophilus oryzae

Coleoptera

Curculionidae

Burks and Hagstrum 1999

Tribolium castaneum

Coleoptera

Tenebrionidae

Burks and Hagstrum 1999

Phytomyza ilicis

Diptera

Agromyzidae

Klok et al. 2003

Note: None of these species is tolerant of freezing in their extracellular fluids.

Note: None of these species is tolerant of freezing in their extracellular fluids.

Was this article helpful?

0 0

Post a comment