Cold Tolerance Strategy Research Articles

Cold tolerance of mountain pine beetle among novel eastern pines: A potential for trade-offs in an invaded range?

Novel hosts may have unforeseen impacts on herbivore life history traits. The mountain pine beetle (Dendroctonus ponderosae Hopkins) is a tree-killing bark beetle native to western North America but constrained by cold temperatures in the northern limits of its distribution. In recent years, this insect has spread north and east of its historical range, and continued expansion, or accidental introduction, could result in the mountain pine beetle becoming invasive in eastern North America. The limiting effect of cold temperatures among novel host pines is unknown, yet crucial for understanding the risk posed to northeastern North American forests. We report the susceptibility of mountain pine beetle to cold temperatures while overwintering in six different pine species. Brood developed in two western pine hosts (Pinus contorta Dougl. var. latifolia Engelm. and P. ponderosa Dougl. ex. Laws. var. scopulorum Engelm.) as well as four eastern pines (P. banksiana Lamb., P. resinosa Ait., P. strobus L. and P. sylvestris L.) novel to this insect. The cold tolerance and cold tolerance strategy of the most common overwintering stage varied by host and year. Models describing lower lethal temperatures more accurately predicted observed field mortality of overwintering larvae than models based on temperatures at which larvae froze. Rapid development to less cold tolerant pupal and adult stages by brood in novel hosts prior to winter may constitute a trade-off between increased host suitability and winter mortality. We demonstrate that overwintering survival of mountain pine beetles in novel hosts depends on a match between the climate and ecophysiological effects of pine species. These results have implications for risk assessment models and management planning for eastern forests as mountain pine beetle continues to expand its range.

Cold Tolerance of Pityophthorus juglandis (Coleoptera: Scolytidae) From Northern California.

Winter survivorship of insects is determined by a combination of physiological, behavioral, and microhabitat characteristics. We characterized the cold tolerance of the walnut twig beetle, Pityophthorus juglandis Blackman, a domestic alien invasive bark beetle that vectors a phytopathogenic fungus. The beetle and fungus cause thousand cankers disease in species of Juglans and Pterocarya. The disease is spreading in the United States of America (USA) and Italy. Contact thermocouple thermometry was used to measure the supercooling points of adults and larvae and lower lethal temperatures of adults from a population from northern California. Supercooling points ranged from -12.2 °C to - 25.0 °C for adults and -13.6 °C to - 23.5 °C for larvae; lower lethal temperatures of adults ranged from -14 °C to - 23 °C. We found seasonal changes in adult supercooling points in fall, winter, and spring. The supercooling point for males was 0.5 °C colder than for females over all months and 1 °C colder in the winter than in other seasons. The cold-tolerance strategy shifted in P. juglandis adults from freeze intolerance (December 2013 and January 2014) to partial freeze tolerance (February 2014). An intermediate level of cold tolerance with a plastic response to cold partially explains survival of P. juglandis outside of its native range in the southwestern USA. In addition, we characterized the relationship between minimum air temperatures and minimum phloem temperatures in two Juglans spp. in northern California and Colorado and characterized portions of the native geographic range of eastern black walnut, J. nigra L., that may be too cold currently for this insect to persist.

Freeze tolerance ofCyphoderris monstrosa(Orthoptera: Prophalangopsidae)

AbstractThe great grig,Cyphoderris monstrosaUhler (Orthoptera: Prophalangopsidae), is a large (20–30 mm, >1 g), nocturnal ensiferan that inhabits montane coniferous forests in northwestern North America.Cyphoderris monstrosaoverwinters as a late instar nymphs, but its cold tolerance strategy has not previously been reported. We collected nymphs from near Kamloops, British Columbia, Canada in late spring to determine their cold tolerance strategy.Cyphoderris monstrosanymphs were active at low temperatures until they froze at −4.6±0.3 °C. The nymphs survived internal ice formation (i.e., are freeze tolerant), had a lethal temperature between −9 °C and −12 °C, and could survive for between five and 10 days at −6 °C. IsolatedC. monstrosagut, Malpighian tubules, and metafemur muscle tissues froze at temperatures similar to whole nymphs, and likely inoculate freezingin vivo. Hemolymph osmolality was 358±51 mOsm, with trehalose and proline comprising ~10% of that total. Glycerol was not detectable in hemolymph from field-fresh nymphs, but accumulated after freezing and thawing. The control of ice formation and presence of hemolymph cryoprotectants may contribute toC. monstrosafreeze tolerance and overwintering survival.

Population divergence in cold tolerance of the intertidal gastropod Littorina brevicula explained by habitat-specific lowest air temperature

Temperature is a fundamental element determining the distribution patterns of ectotherms, and it is generally recognized that physiological tolerances of ectotherms change according to thermal gradients in their habitats. However, little is known about the variation in cold tolerance of marine invertebrates among local populations of the same species. In this study, three experiments were conducted to demonstrate inter-population variation in the cold tolerance of the intertidal gastropod Littorina brevicula, and to explore factors driving the variation. First, seasonal changes in the freezing temperature (the supercooling point, SCP) and the median lower lethal temperature (LLT50) of snails collected from a single population were examined to identify the cold tolerance strategies of this species. Seasonal fluctuation was clear in only the LLT50 which was lower than the SCP in winter, indicating that cold tolerance strategy of this species was freeze tolerant. Second, the cold tolerance of snails from four populations was compared. These populations were distributed at latitudinally different locations, and the comparisons were performed before winter when their cold tolerance was not required and in winter when their cold tolerance increased. In this experiment, while the cold tolerance of snails collected in winter was higher than that of snails collected before winter in all four populations, there were differences in tolerance among the populations. Furthermore, to estimate their ability of acclimation to cold environments, snails that were collected from the northernmost and southernmost populations in the four populations before winter were acclimated to a constant low temperature in the laboratory for a long period (120–130days). This long period of acclimation led to an increase in the cold tolerance of both populations, but the latitudinal difference was maintained. Additionally, after imposing the long period of acclimation to snails that were collected at 12 locations before winter, factors that might cause local variation in their cold tolerance were explored. This experiment clearly showed that local variation in cold tolerance was explained by the lowest local air temperature. Our study demonstrated inter-population variation in the cold tolerance of an intertidal mollusc, and that the variation is explained by thermal gradients in winter.

Supercooling points of diapausing forest tent caterpillar (Lepidoptera: Lasiocampidae) eggs

AbstractForest tent caterpillar (Malacosoma disstriaHübner; Lepidoptera: Lasiocampidae) is a widely distributed defoliator that undergoes intermittent outbreaks. It overwinters as pharate larvae within egg bands, is univoltine, and experiences low winter temperatures in its northern range. Little is known about how low temperatures affect winter survival and cold tolerances, their cold tolerance strategy, or how cold tolerances may vary over time and among populations. We evaluated supercooling points (SCPs) from four populations ofM. disstriaeggs collected along a 552 km latitudinal gradient from southern Wisconsin to northern Minnesota, United States of America. To test for potential effects of winter environment, we also administered three overwintering regimes (Madison, Wisconsin; Cloquet, Minnesota; Ely, Minnesota). Supercooling points were recorded in November, February, and March of 2011–2012. Supercooling points varied with maternal source (egg band), time of winter season, population source, and overwintering treatment. Means ranged from −26.8 °C (±0.5 °C) to −40.3 °C (±0.3 °C), accordingly. In a separate laboratory experiment, 89% of pharate larvae held at −20 °C (18.3 °C above coolest mean SCP) survived, but none held at −45 °C (6.7 °C below lowest mean SCP) survived. This relatively high degree of cold tolerance in its overwintering stage, due to freeze avoidance, may partially explain survival patterns and limits of overwinteringM. disstriain northern populations.

Cold tolerance of the montane Sierra leaf beetle, Chrysomela aeneicollis

Small ectothermic animals living at high altitude in temperate latitudes are vulnerable to lethal cold throughout the year. Here we investigated the cold tolerance of the leaf beetle Chrysomela aeneicollis living at high elevation in California’s Sierra Nevada mountains. These insects spend over half their life cycle overwintering, and may therefore be vulnerable to winter cold, and prior studies have demonstrated that survival is reduced by exposure to summertime cold. We identify overwintering microhabitat of this insect, describe cold tolerance strategies in all life stages, and use microclimate data to determine the importance of snow cover and microhabitat buffering for overwinter survival. Cold tolerance varies among life history stages and is typically correlated with microhabitat temperature: cold hardiness is lowest in chill-susceptible larvae, and highest in freeze-tolerant adults. Hemolymph osmolality is higher in quiescent (overwintering) than summer adults, primarily, but not exclusively, due to elevated hemolymph glycerol. In nature, adult beetles overwinter primarily in leaf litter and suffer high mortality if early, unseasonable cold prevents them from entering this refuge. These data suggest that cold tolerance is tightly linked to life stage. Thus, population persistence of montane insects may become problematic as climate becomes more unpredictable and climate change uncouples the phenology of cold tolerance and development from the timing of extreme cold events.

Adult plasticity of cold tolerance in a continental-temperate population of Drosophila suzukii

Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) is a worldwide emerging pest of soft fruits, but its cold tolerance has not been thoroughly explored. We determined the cold tolerance strategy, low temperature thermal limits, and plasticity of cold tolerance in both male and female adult D. suzukii. We reared flies under common conditions (long days, 21°C; control) and induced plasticity by rapid cold-hardening (RCH, 1h at 0°C followed by 1h recovery), cold acclimation (CA, 5days at 6°C) or acclimation under fluctuating temperatures (FA). D. suzukii had supercooling points (SCPs) between −16 and −23°C, and were chill-susceptible. 80% of control flies were killed after 1h at −7.2°C (males) or −7.5°C (females); CA and FA improved survival of this temperature in both sexes, but RCH did not. 80% of control flies were killed after 70h (male) or 92h (female) at 0°C, and FA shifted this to 112h (males) and 165h (females). FA flies entered chill coma (CTmin) at approximately −1.7°C, which was ca. 0.5°C colder than control flies; RCH and CA increased the CTmin compared to controls. Control and RCH flies exposed to 0°C for 8h took 30–40min to recover movement, but this was reduced to <10min in CA and FA. Flies placed outside in a field cage in London, Ontario, were all killed by a transient cold snap in December. We conclude that adult phenotypic plasticity is not sufficient to allow D. suzukii to overwinter in temperate habitats, and suggest that flies could overwinter in association with built structures, or that there may be additional cold tolerance imparted by developmental plasticity.

The overwintering biology of the acorn weevil, Curculio glandium in southwestern Ontario

The acorn weevil, Curculio glandium, is a widespread predator of acorns in eastern North America that overwinters in the soil as a larva. It is possible that low temperatures limit its northern geographic range, so we determined the cold tolerance strategy, seasonal variation in cold tolerance, and explored the physiological plasticity of overwintering larvae. Weevil larvae were collected from acorns of red and bur oak from Pelee Island, southwestern Ontario in fall 2010 and 2011. C. glandium larvae are freeze avoidant and larvae collected from bur oak acorns had lower supercooling points (SCPs: −7.6±0.36°C, LT50: −7.2°C) than those collected from red oak acorns (SCPs: −6.1±0.40°C, LT50: −6.1°C). In the winter of 2010–2011, SCPs and water content decreased, however these changes did not occur in 2011–2012, when winter soil temperatures fluctuated greatly in the absence of the buffering effect of snow. To examine whether larvae utilize cryoprotective dehydration, larvae from red oak acorns were exposed to −5°C in the presence of ice for seven days. These conditions decreased the SCP without affecting water content, suggesting that SCP and water content are not directly coupled. Finally, long-term acclimation at 0°C for six weeks slightly increased cold tolerance but also did not affect water content. Thus, although larval diet affects cold tolerance, there is limited plasticity after other treatments. The soil temperatures we observed were not close to lethal limits, although we speculate that soil temperatures in northerly habitats, or in years of reduced snow cover, has the potential to cause mortality in the field.

Parallel ionoregulatory adjustments underlie phenotypic plasticity and evolution of Drosophila cold tolerance.

Low temperature tolerance is the main predictor of variation in the global distribution and performance of insects, yet the molecular mechanisms underlying cold tolerance variation are poorly known, and it is unclear whether the mechanisms that improve cold tolerance within the lifetime of an individual insect are similar to those that underlie evolved differences among species. The accumulation of cold-induced injuries by hemimetabolous insects is associated with loss of Na(+) and K(+) homeostasis. Here we show that this model holds true for Drosophila; cold exposure increases haemolymph [K(+)] in D. melanogaster, and cold-acclimated flies maintain low haemolymph [Na(+)] and [K(+)], both at rest and during a cold exposure. This pattern holds across 24 species of the Drosophila phylogeny, where improvements in cold tolerance have been consistently paired with reductions in haemolymph [Na(+)] and [K(+)]. Cold-acclimated D. melanogaster have low activity of Na(+)/K(+)-ATPase, which may contribute to the maintenance of low haemolymph [Na(+)] and underlie improvements in cold tolerance. Modifications to ion balance are associated with both phenotypic plasticity within D. melanogaster and evolutionary differences in cold tolerance across the Drosophila phylogeny, which suggests that adaptation and acclimation of cold tolerance in insects may occur through similar mechanisms. Cold-tolerant flies maintain haemolymph osmolality despite low haemolymph [Na(+)] and [K(+)], possibly through modest accumulations of organic osmolytes. We propose that this could have served as an evolutionary route by which chill-susceptible insects developed more extreme cold tolerance strategies.

Protective Effect of Exogenous PGRs on Chlorophyll Fluorescence and Membrane Integrity of Rice Seedlings under Chilling Stress

The effects of chilling stress on chlorophyll content, chlorophyll fluorescence and Malondialdehyde (MDA; a biomarker for lipid peroxidation in membrane) were evaluated in rice (Oryza sativa) seedlings during chilling stress and subsequent recovery phase using a phytotron. The effects of Indole-3-Acetic Acid (IAA), Abscisic Acid (ABA) and Kinetin (CK) exogenously foliar applied to three rice genotypes differing in cold tolerance were probed. Under chilling stress reduced levels of photo inhibition and MDA due to hormone application in relation to no hormone treatment demonstrated the significant effect of applied hormones to induce chilling tolerance in the genotypes. There were different effects of hormones on genotypes and even on organs (root and shoot) in the case of MDA content, moreover the strategy for cold tolerance differed among the genotypes.

Cryoprotective dehydration is widespread in Arctic springtails

Cryoprotective dehydration (CPD) is a cold tolerance strategy employed by small invertebrates that readily lose water by evaporation when subjected to sub-zero temperatures in the presence of ice. Until now, relatively few species have been investigated using methods by which CPD can be shown. In the present study we investigated the cold tolerance strategy of seven soil arthropod species from the high Arctic Spitzbergen, and compared water content and water loss, body fluid melting points (MP) and survival under cold and desiccating conditions. We tested the hypothesis that CPD is a commonly occurring cold hardiness strategy among soil arthropods. We found that four springtail species ( Hypogastrura viatica, Folsomia quadrioculata, Oligaphorura groenlandica and Megaphorura arctica; Collembola) went through severe dehydration and MP equilibration with ambient temperature, and thus overwinter by employing CPD, whereas a beetle ( Atheta graminicola) and one of the springtails ( Isotoma anglicana) were typical freeze avoiding species over-wintering by supercooling. Desiccation tolerance of the red velvet mite ( Neomolgus littoralis) was also investigated; very low water loss rates of this species indicated that it does not survive winter by use of CPD. All in all, the results of the present study confirm the hypothesis that CPD is an effective over-wintering strategy which is widespread within soil arthropods.

Response to photoxidative stress induced by cold in japonica rice is genotype dependent

Two japonica rice genotypes, INIA Tacuarí and L2825CA, were analyzed for tolerance to low temperature during early vegetative growth. Effect on photosynthesis, energy dissipation, pigment content, xanthophyll-cycle pool conversion, hydrogen peroxide accumulation, oxidative damage and antioxidant enzyme activities were determined to better understand potential mechanisms for cold tolerance. Photoinhibition was measured using chlorophyll fluorescence and oxidative damage by lipid peroxidation and electrolyte leakage. Both genotypes were demonstrated to be cold tolerant which was consistent with their reduced levels of photoinhibition and oxidative damage compared with a cold-sensitive genotype during chilling stress. The strategy for cold tolerance differed between the two genotypes, and involved different mechanisms for disposal of excess energy. The presence of high lutein concentrations and the existence of active non-harmful energy dissipation processes through the xanthophyll cycle appeared to be responsible for chilling tolerance in INIA Tacuarí. On the other hand, increased cold tolerance of L2825CA relative to INIA Tacuarí was related to the higher constitutive superoxide dismutase (SOD, EC 1.15.1.1), ascorbate peroxidase (APX, EC 1.11.1.11) and catalase (CAT, EC 1.11.1.6).

The Evolution of Cold Tolerance inDrosophilaLarvae

Temperature is a primary determinant of insect and other ectotherm distribution and activity. Physiological and behavioral adaptations allow many insects to survive at subzero temperatures, yet the evolutionary influences on insect cold tolerance are unclear. Supercooling points, basal cold tolerance, cold-tolerance strategy, and inducible cold tolerance from rapid cold-hardening or acclimation were measured in a phylogenetically independent context in larvae of 27 phylogenetically diverse Drosophila species acquired from stock collections. Supercooling capacity is attributed primarily to physical factors, such as dry mass and water mass. Species of the obscura group were more resistant to acute cold tolerance than species of other groups within the genus, and plasticity in cold tolerance is constrained by phylogeny rather than by basal cold tolerance. The more cold-tolerant freeze-avoiding species appear to have arisen multiple times in Drosophila and are distinct from chill-susceptible species, which likely indicate the ancestral state. A phylogenetic influence is apparent on several measures of cold tolerance, which show considerable interspecific variation and indicate varying physiological mechanisms among Drosophila species when temperature limits are met.

The overwintering physiology of the emerald ash borer, Agrilus planipennis Fairmaire (Coleoptera: Buprestidae)

Ability to survive cold is an important factor in determining northern range limits of insects. The emerald ash borer ( Agrilus planipennis) is an invasive beetle introduced from Asia that is causing extensive damage to ash trees in North America, but little is known about its cold tolerance. Herein, the cold tolerance strategy and mechanisms involved in the cold tolerance of the emerald ash borer were investigated, and seasonal changes in these mechanisms monitored. The majority of emerald ash borers survive winter as freeze-intolerant prepupae. In winter, A. planipennis prepupae have low supercooling points (∼−30 °C), which they achieve by accumulating high concentrations of glycerol (∼4 M) in their body fluids and by the synthesis of antifreeze agents. Cuticular waxes reduce inoculation from external ice. This is the first comprehensive study of seasonal changes in cold tolerance in a buprestid beetle.

Temporal gene expression profiles in a palaearctic springtail as induced by desiccation, cold exposure and during recovery

Summary 1. Cryoprotective dehydration is a cold tolerance strategy used by small permeable invertebrates overwintering in frozen habitats. Even though an increasing number of species using this strategy have been described, little is known of the functional genomics of cryoprotective dehydration. 2. Megaphorura arctica is a northern palaearctic springtail (Collembola) which survives extreme low temperatures by cryoprotective dehydration. The massive loss of body water associated with this strategy requires a fine tuned physiological adaptation to both desiccation and cold exposure. 3. We investigated the temporal gene expression profile of six candidate genes, and compared gene expression responses to desiccation and cold separately, as well as both factors combined. 4. The major responses were found in Heat shock protein 70 (HSP70) and Trehalose‐6‐Phosphate‐Synthase (TPS). TPS expression followed water loss closely, while HSP70 was induced after considerable water loss. HSP70 transcript response in M. arctica was induced by desiccation and rehydration, but not by exposure to cold. 5. The data suggest that cold and water loss induce partly different responses and that temporal sampling is important for uncovering the dynamics of gene responses to cryoprotective dehydration.

Overwintering of terrestrial Arctic arthropods: the fauna of Svalbard now and in the future

There are over 500 species of arthropods recorded from Svalbard. These animals overwinter either within the soil or on the ground surface, and have to tolerate an environment where the ground is frozen for over 9 months each year. Three cold-tolerance strategies have been described from Svalbard invertebrates: freeze avoidance, freeze tolerance and desiccation. Once in a coldtolerant state the animals can be extremely cold tolerant in terms of both minimum exposure temperature and period of exposure. How the overwintering capabilities of these animals will be affected by climate changes during the next 100 years, as predicted by climate models, is not yet known. Four principle factors with an impact on overwintering of the terrestrial arthropod fauna are outlined here: (1) warmer winter temperatures, with an increased frequency of extreme events such as freeze–thaw cycles and surface icing; (2) changes in snow fall and snow lie; (3) pollutant load; and (4) dispersal of invertebrates to Svalbard. Finally, areas where further research is required are highlighted: including the development of controlled multi-season field experiments; effect of freeze–thaw cycles; changes in thickness and distribution of snow lie, with the subsequent effects on duration of the summer period; chill susceptibility of soil arthropods; assessing potential colonizing species and the likelihood of these species becoming established; assessing the effect of gene flow from surrounding populations; interactions between pollution and cold tolerance; anoxia stress; and the genetics of cold tolerance.

Climatic variability and hemispheric differences in insect cold tolerance: support from southern Africa

SummaryInsects generally survive subzero temperatures by utilizing either freeze tolerance or freeze avoidance. Comparative analyses from a limited data set have indicated that freeze tolerance may be predominant among species at temperate latitudes in the southern hemisphere, while freeze avoidance dominates in the north.We investigated the cold tolerance strategies of cockroaches and beetles from cold regions in southern Africa, including the Cederberg mountains, the Karoo desert and the Drakensberg mountains.We found that 8 of 11 species are freeze tolerant.Overall, 77% of species investigated in the southern hemisphere (n = 27) were freeze tolerant, which is significantly different from the 29% (n = 258) in the north (P &lt; 0·001).There are regular, unpredictable subzero temperature events in the southern African habitats; such variability appears to be a general feature of many cold habitats in the southern hemisphere, which may lead to the observed interhemispheric discrepancies in cold‐tolerance strategies.

Implication of pupal cold tolerance for the northern over-wintering range limit of the leafminer Liriomyza sativae (Diptera: Agromyzidae) in China

This study investigated the cold tolerance of a laboratory-reared population and latitude-separated populations of the leafminer Liriomyza sativae in China in terms of low-temperature survival rate and supercooling capacity. Pupae of the laboratory-reared population are susceptible to freezing temperatures. The supercooling point of the pupae varied at a maximum of up to 10°C among the geographic populations. Both acclimation of the pupae at 5 and 10°C significantly increased the cold survival rate of laboratory-reared and field-collected populations. But the field population had a more active response to the same acclimation regime. Combining the experimental data with previous field investigations, the −2°C isotherm of the minimum mean temperature of January was proposed as the leafminer's over-wintering range limit. Meanwhile, with the widespread availability of greenhouses as a source of re-infestation in northern China, the leafminer's natural border of distribution should be determined by the minimum temperature in warm seasons. Our results suggest that biologically similar Liriomyza species may cope with the intensifying cold stress along the latitude by adopting a mixed cold-tolerance strategy, which is closely associated with the greenhouse microhabitats. The physiologically based modeling of the over-wintering limit provides a tool for guiding the management for greenhouse pests and predicting the source of pest infestation.

Cold tolerance of Littorinidae from southern Africa: intertidal snails are not constrained to freeze tolerance

All intertidal gastropods for which cold tolerance strategies have been assessed have been shown to be freeze tolerant. Thus, freeze tolerance is considered an adaptation to the intertidal environment. We investigated the cold tolerance strategies of three species of subtropical and temperate snails (Gastropoda: Littorinidae) to determine whether this group is phylogenetically constrained to freeze tolerance. We exposed 'dry' acclimated and 'wet' rehydrated snails to low temperatures to determine temperature of crystallisation (Tc), lower lethal temperature and LT(50) and to examine the relationship between ice formation and mortality. Tc was lowest in dry Afrolittorina knysnaensis (-13.6+/-0.4 degrees C), followed by dry Echinolittorina natalensis (-10.9+/-0.2 degrees C) and wet A. knysnaensis (-10.2+/-0.2 degrees C) . The Tc of both A. knysnaensis and E. natalensis increased with rehydration, whereas Tc of dry and wet Afrolittorina africana did not differ (-9.6+/-0.2 and -9.0+/-0.2 degrees C respectively). Wet snails of all species exhibited no or low survival of inoculative freezing, whereas dry individuals of A. knysnaensis could survive subzero temperatures above -8 degrees C when freezing was inoculated with ice . In the absence of external ice, Afrolittorina knysnaensis employs a freeze-avoidance strategy of cold tolerance, the first time this has been reported for an intertidal snail, indicating that there is no family-level phylogenetic constraint to freeze tolerance. Echinolittorina natalensis and A. africana both showed pre-freeze mortality and survival of some internal ice formation, but were not cold hardy in any strict sense.

The environmental physiology of Antarctic terrestrial nematodes: a review.

The environmental physiology of terrestrial Antarctic nematodes is reviewed with an emphasis on their cold-tolerance strategies. These nematodes are living in one of the most extreme environments on Earth and face a variety of stresses, including low temperatures and desiccation. Their diversity is low and declines with latitude. They show resistance adaptation, surviving freezing and desiccation in a dormant state but reproducing when conditions are favourable. At high freezing rates in the surrounding medium the Antarctic nematode Panagrolaimus davidi freezes by inoculative freezing but can survive intracellular freezing. At slow freezing rates this nematode does not freeze but undergoes cryoprotective dehydration. Cold tolerance may be aided by rapid freezing, the production of trehalose and by an ice-active protein that inhibits recrystallisation. P. davidi relies on slow rates of water loss from its habitat, and can survive in a state of anhydrobiosis, perhaps aided by the ability to synthesise trehalose. Teratocephalus tilbrooki and Ditylenchus parcevivens are fast-dehydration strategists. Little is known of the osmoregulatory mechanisms of Antarctic nematodes. Freezing rates are likely to vary with water content in Antarctic soils. Saturated soils may produce slow freezing rates and favour cryoprotective dehydration. As the soil dries freezing rates may become faster, favouring freezing tolerance. When the soil dries completely the nematodes survive anhydrobiotically. Terrestrial Antarctic nematodes thus have a variety of strategies that ensure their survival in a harsh and variable environment. We need to more fully understand the conditions to which they are exposed in Antarctic soils and to apply more natural rates of freezing and desiccation to our studies.