M. R. Worland

Partial desiccation induced by sub-zero temperatures as a component of the survival strategy of the Arctic collembolan Onychiurus arcticus (Tullberg)

The mechanism by which the freeze susceptible Arctic collembolan Onychiurus arcticus survives winter temperatures of -25 degrees C in the field is not fully understood but exposure to sub-zero temperatures (e.g. -2.5 degrees C) is known to induce dehydration and lower the supercooling point (SCP). In this study, changes in the water status and certain biochemical parameters (measured in individual Collembola) during a 3-week exposure to decreasing temperatures from 0 to -5.5 degrees C were studied. Osmotically active and inactive body water contents were measured by differential scanning calorimetry (DSC), water soluble carbohydrates by high performances liquid chromatography (HPLC) and glycogen by enzymatic assays. The activity of trehalase and trehalose 6-phosphate synthase were also measured. During the experiment, total water content decreased from 70 to 40% of fresh weight, mostly by the loss of osmotically active water with only a small reduction in the osmotically inactive component. The SCP decreased from -7 to -17 degrees C. Analysis of the results shows that if O. arcticus is exposed to -7 degrees C in the presence of ice, all osmotically active water would be lost due to the vapour pressure gradient between the animals supercooled body fluids and the ice. Under these conditions the estimated SCP would reach a minimum of c. -27 degrees C, but the Collembola may never freeze as all the osmotically active water has been lost, the animal becoming almost anhydrobiotic. Trehalose concentration increased from 0.9 to 94.7&mgr;g mg(-1)fw while glycogen reserves declined from 160 to 7.7 nmol glucose equivalents mg(-1) protein. Trehalase activity declined as the temperature was reduced, while trehalose 6-phosphate activity peaked at 0 degrees C. By adopting a strategy of near anhydrobiosis induced by sub-zero temperatures, O. arcticus, which was previously thought to be poorly adapted to survive severe winter temperatures, is able to colonise high Arctic habitats.

Effects of experimental temperature elevation on high-arctic soil microarthropod populations

An experiment was conducted to measure the effects of summer warming on the total population densities of soil-dwelling microarthropods in the high Arctic and to compare these results with those from natural between-year and between-site variations. Small polythene tents were used to elevate summer temperatures over 3 years on polar semi-desert and tundra heath in West Spitsbergen, Svalbard, Norway. Soil cores were taken at regular intervals from tented and untented (control) plots and heat extracted for mites (Acarina: Oribatida) and springtails (Collembola). Species present were similar at both sites, but at the start of the experiment total springtail populations were greater at the polar semi-desert whilst oribatid mite densities were equal at both sites. No significant effect of temperature elevation on oribatid mite populations emerged, even after 3 years. By contrast, springtail numbers were significantly lower on tented versus control plots at the polar semi-desert at the end of year 3, but not so at the tundra heath. Collembola numbers declined at both sites during the warm dry midsummers of 1992/1993 and this was most marked at the better drained polar semi-desert site. Over the equivalent period total oribatid mite populations, while relatively more stable, increased significantly at the polar semi-desert as a result of an increase in the number of juveniles. Results are interpreted in the context of the ecophysiological adaptations of oribatid mites and springtails to soil temperature and moisture. The resulting survival characteristics are considered in relation to the temperature and moisture characteristics of the two sites. The experiment demonstrated that year to year variation in climate, interacting with physical differences between sites, produced an equal or greater effect on microarthropod numbers at any one site than the 8–10% increase in “heat availability” (day degrees above zero) resulting from the summer tent treatment. The limitations of the use of tents to elevate soil temperatures are discussed. Comparisons are made with microarthropod population data from other polar and alpine sites.

Survival and water loss in some Antarctic arthropods

Abstract Seven species of Antarctic micro-arthropods (4 mites and 3 collembolans) were examined to determine their resistance to dehydration and their survival under dry conditions. Water loss at r.h. 5% at temperatures in the range −10 to 45°C was measured gravimetrically using a recording micro-balance. Survival of samples of mites was monitored after exposure to r.h. 5% and temperatures in the range 0–20°C. Rates of water loss ranged from 0 to about 30% fresh weight h −1 depending on temperature and species. The 3 Collembola were least resistant and the 2 oribatid mites were most resistant to dehydration under the experimental conditions. The optimal survival temperature of the mite Alaskozetes antarcticus was around 10°C under 5% r.h.; there were no significant differences in rate of water loss between temperatures. The results are discussed in terms of possible control mechanisms and the type of habitat occupied by each species.

Thermal adaptation in the Arctic collembolan Onychiurus arcticus (Tullberg)

Ecophysiological characteristics, including survival at high and low temperatures, locomotory activity at sub-zero temperatures, supercooling ability and oxygen consumption rates, were investigated for the Arctic springtail Onychiurus arcticus (Tullberg) (Collembola, Onychiuridae). Individuals had a mean (± SE) fresh weight of 428.2±107.6 μg which contained 74.0±10.2% body water. Survival at high temperatures was humidity dependent. After 3h exposure at 100% relative humidity and 30°C, >80% of the animals survived, but at >32.5°C no individual survived. 70% of the animals survived a 1 h exposure at 32.5°C but at 35.0°C all animals died. At 0% relative humidity there were no survivors after 3 h at >25.0°C. At sub-zero temperatures, 60% of the springtails survived for 84 days at −3.0°C, but at −5.0°C survival was reduced to 35%. Individual collembolans showed locomotor activity down to −4°C. O. arcticus was freezing-intolerant and individuals supercooled to −6.1±0.1°C before freezing. This relatively high mean (±SE) supercooling point was stable throughout summer and was unaffected by acclimation temperature. A non-linear relationship existed between oxygen consumption and temperature. Between 0 and 10°C the Q10 was high at 7.0. It declined to 1.6 over the temperature range 10 to 30°C, increasing to 5.8 at higher temperatures. O. arcticus possesses ecophysiological characteristics suited to life in the upper layer of soil and surface vegetation, and beneath snow cover. However, it appears to be poorly adapted to survive severe winter temperatures being intolerant of freezing and with little supercooling ability. Such features may restrict its present distribution in the Arctic, but it seems likely that it would benefit by an increase in environmental temperature.

Ecophysiological strategies of Antarctic intertidal invertebrates faced with freezing stress

Recent studies have revealed a previously unanticipated level of biodiversity present in the Antarctic littoral. Here, we report research on the ecophysiological strategies adopted by intertidal species that permit them to survive in this environment, presenting cold-tolerance data for the widest range of invertebrates published to date from the Antarctic intertidal zone. We found significant differences in levels of cold tolerance between species within this zone. However, and contrary to expectations, intraspecific comparisons of subtidal and intertidal groups of eight species found significant differences between groups in only three species. One species, the nemertean Antarctonemertes validum, showed evidence of the presence of antifreeze proteins (thermal hysteresis proteins), with 1.4°C of thermal hysteresis measured in its haemolymph. We found a strong inverse relationship across species between mass and supercooling point, and fitted a power law model to describe the data. The scaling exponent (0.3) in this model suggests a relationship between an animal’s supercooling point and its linear dimensions.

Thermal tolerance and acclimation response of larvae of the sub-Antarctic beetle Hydromedion sparsutum (Coleoptera: Perimylopidae)

Hydromedion sparsutum is a locally abundant herbivorous beetle on the sub-Antarctic island of South Georgia, often living in close association with the tussock grass Parodiochloa flabellata. Over a 4-day period in mid-summer when the air temperature varied from 0 to 20°C, the temperature in the leaf litter 5–10 cm deep at the base of tussock plants (the microhabitat of H. sparsutum) was consistently within the range of 5–7.5°C. Experiments were carried out to assess the ability of H. sparsutum larvae collected from this thermally stable environment to acclimate when maintained at lower (0°C) and higher (15°C) temperatures. The mean supercooling points (freezing temperature) of larvae collected in January and acclimated at 0°C for 3 and 6 weeks and 15°C for 3 weeks were all within the range of −2.6 to −4.6°C. Larvae in all treatment groups were freeze tolerant. Acclimation at 0°C significantly increased survival in a 15-min exposure at −8°C (from 27 to 96%) and −10°C (from 0 to 63%) compared with the field-fresh and 15°C-treated larvae. Similarly, survival of 0°C-acclimated larvae in a 72-h exposure at −6°C increased from 20 to 83%. Extending the acclimation period at 0°C to 6 weeks did not produce any further increase in cold tolerance. The concentrations of glucose and trehalose in larval body fluids increased significantly with low temperature acclimation. Larvae maintained at 15°C for 3 weeks (none survived for 6 weeks) were less able to survive 1-h exposures between 30 and 35°C than the 0°C-treated samples. Whilst vegetation and snow cover are an effective buffer against low winter temperatures in many polar insects, the inability of H. sparsutum larvae to acclimate or survive at 15°C suggests that protection against high summer temperatures is equally important for this species.

Temperature preferences of the mite, Alaskozetes antarcticus, and the collembolan, Cryptopygus antarcticus from the maritime Antarctic

Abstract. The thermal preferences of Alaskozetes antarcticus (Acari, Cryptostigmata) and Cryptopygus antarcticus (Collembola, Isotomidae) were investigated over 6 h within a temperature gradient (−3 to +13 °C), under 100% relative humidity (RH) conditions. After 10 days of acclimation at −2 or +11 °C, individual supercooling points (SCP) and thermopreferences were assessed, and compared with animals maintained for 10 days under fluctuating field conditions (−6 to +7 °C). Acclimation at −2 °C lowered the mean SCP of both A. antarcticus (−24.2 ± 9.1) and C. antarcticus (−14.7 ± 7.7) compared to field samples (−19.0 ± 9.0 and −10.7 ± 5.2, respectively). Acclimation at +11 °C increased A. antarcticus mean SCP values (−13.0 ± 8.5) relative to field samples, whereas those of C. antarcticus again decreased (−16.7 ± 9.1). Mites acclimated under field conditions or at +11 °C selected temperatures between −3 and +1 °C. After acclimation at −2 °C, both species preferred +1 to +5 °C. Cryptopygus antarcticus maintained under field conditions preferred +5 to +9 °C, whereas individuals acclimated at +11 °C selected +9 to +13 °C. For A. antarcticus, thermopreference was not influenced by its cold hardened state. The distribution of field specimens was further assessed within two combined temperature and humidity gradient systems: (i) 0–3 °C/12% RH, 3–6 °C/33% RH, 6–9 °C/75% RH and 9–12 °C/100% RH and (ii) 0–3 °C/100% RH, 3–6 °C/75% RH, 6–9 °C/33% RH and 9–12 °C/12% RH. In gradient (i), C. antarcticus distributed homogeneously, but, in gradient (ii), C. antarcticus preferred 0–3 °C/100% RH. Alaskozetes antarcticus selected temperatures between 0 and +6 °C regardless of RH conditions. Cryptopygus antarcticus appears better able than A. antarcticus to opportunistically utilize developmentally favourable thermal microclimates, when moisture availability is not restricted. The distribution of A. antarcticus appears more influenced by temperature, especially during regular freeze‐thaw transitions, when this species may select low temperature microhabitats to maintain a cold‐hardened state.

Influence of temperature on the hygropreference of the Collembolan, Cryptopygus antarcticus, and the mite, Alaskozetes antarcticus from the maritime Antarctic.

The hygropreference of adult Cryptopygus antarcticus and Alaskozetes antarcticus was investigated over 2 h at 5, 10 and 20 degrees C, along humidity gradients (9-98% RH) established by means of different salt solutions. Two chamber arrangements were employed, linear and grid, to determine any influence of thigmotactic behaviour on distribution within the RH gradient. The humidity preference of both species varied with temperature. At 5 and 10 degrees C, C. antarcticus distributed homogeneously showing no clear RH preference. At 20 degrees C, this species preferred the highest humidity (98% RH). A. antarcticus demonstrated a preference for the lowest humidity (9% RH) at 5 degrees C, but at 10 degrees C its distribution differed between the two arena types. At 20 degrees C, A. antarcticus showed no clear humidity preference. Assays to control for experimental asymmetries along the gradient; thigmotactic behaviour; and aggregative behaviour exclude these factors as explanations for the observed results. The mean initial water content of samples did not differ significantly between temperature regimes (C. antarcticus: 68.6, 71.1 and 74.3%; A. antarcticus: 68.1, 70.1 and 68.6% at 5, 10 and 20 degrees C respectively), but the level of water loss increased significantly with temperature. The influence of desiccation tolerance and the ecological significance of the observed humidity preferences are discussed.

The significance of the moult cycle to cold tolerance in the Antarctic collembolan Cryptopygus antarcticus

Research into the ecophysiology of arthropod cold tolerance has largely focussed on those parts of the year and/or the life cycle in which cold stress is most likely to be experienced, resulting in an emphasis on studies of the preparation for and survival in the overwintering state. However, the non-feeding stage of the moult cycle also gives rise to a period of increased cold hardiness in some microarthropods and, as a consequence, a proportion of the field population is cold tolerant even during the summer active period. In the case of the common Antarctic springtail Cryptopygus antarcticus, the proportion of time spent in this non-feeding stage is extended disproportionately relative to the feeding stage as temperature is reduced. As a result, the proportion of the population in a cold tolerant state, with low supercooling points (SCPs), increases at lower temperatures. We found that, at 5 degrees C, about 37% of the population are involved in ecdysis and exhibit low SCPs. At 2 degrees C this figure increased to 50% and, at 0 degrees C, we estimate that 80% of the population will have increased cold hardiness as a result of a prolonged non-feeding, premoult period. Thus, as part of the suite of life history and ecophysiological features that enable this Antarctic springtail to survive in its hostile environment, it appears that it can take advantage of and extend the use of a pre-existing characteristic inherent within the moulting cycle.

Pre-adapted to the maritime Antarctic? – Rapid cold hardening of the midge, Eretmoptera murphyi

During the 1960s, the midge, Eretmoptera murphyi, was transferred from sub-Antarctic South Georgia (55°S 37°W) where it is endemic to a single location on maritime Antarctic Signy Island (60°S 45°W). Its distribution has since expanded considerably, suggesting that it is pre-adapted to the more severe conditions further south. To test one aspect of the level of its pre-adaptation, the rapid cold hardening (RCH) response in this species was investigated. When juvenile (L1-L2) and mature (L3-L4) larvae of E. murphyi were directly exposed to progressively lower temperatures for 8h, they exhibited Discriminating Temperatures (DTemp, temperature at which there is 10-20% survival of exposed individuals) of -11.5 and -12.5°C, respectively. The mean SCP was above -7.5°C in both larval groups, confirming the finding of previous studies that this species is freeze-tolerant. Following gradual cooling (0.2°Cmin(-1)), survival was significantly greater at the DTemp in both larval groups. The response was strong, lowering the lower lethal temperature (LLT) by up to 6.5°C and maintaining survival above 80% for at least 22h at the DTemp. RCH was also exhibited during the cooling phase of an ecologically relevant thermoperiodic cycle (+4°C to -3°C). Mechanistically, the response did not affect freezing, with no alteration in the supercooling point (SCP) found following gradual cooling, and was not induced while the organism was in a frozen state. These results are discussed in light of E. murphyis pre-adaptation to conditions on Signy Island and its potential to colonize regions further south in the maritime Antarctic.