William Block

COLD TOLERANCE OF MICROARTHROPODS

1. Microarthropods (Acari and Collembola) are dominant components of the terrestrial fauna in the Antarctic. Their cold tolerance, which forms the mainspring of their adaptational strategy, is reviewed against a background of their structure and function, and by comparison with other arthropods.

Experimental studies on the cold tolerance of Alaskozetes antarcticus

Abstract The cold tolerance mechanism of the Antarctic terrestrial mite Alaskozetes antarcticus (Michael) was investigated in cultured animals. Freezing is fatal in this species and winter survival occurs by means of supercooling, which is enhanced by the presence of glycerol in the body. There is an inverse, linear relationship between the concentration of glycerol and the supercooling point, which may be as low as −30°C. Feeding detracts from supercooling ability by providing ice nucleators in the gut which initiate freezing at relatively high sub-zero temperatures. Experiments on the effects of various environmental factors showed that low temperature acclimation gave rise to increased glycerol concentrations and suppressed feeding, while desiccation also stimulated glycerol production. Photoperiod had no effect on cold tolerance in this species. The juvenile instars of A. antarcticus were found to possess a greater degree of low temperature tolerance than adults.

Global Change and Arctic Ecosystems: Conclusions and Predictions from Experiments with Terrestrial Invertebrates on Spitsbergen

Extensive studies on invertebrates from Ny-Alesund, Spitsbergen, Svalbard and more limited data on aphids from Abisko, Sweden, produced the following main conclusions: (1) The population response to raised summer temperatures differed between the above and the below ground species, both in terms of speed and magnitude. (2) Similar animal communities responded differently to similar temperature manipulations on sites with different vegetation cover and composition. (3) For soil animals the between-year and between-site variations in population densities, were greater than the differences produced by the temperature manipulation experiments at any one site in any year. (4) Infrequent extreme climatic events strongly influence long-term trends in population density and community composition. (5) The population response of invertebrates to climate warming is greatest and most rapid at the coldest sites. (6) The spatial distribution of the above ground insect herbivores on their host plant is temperature limited. (7) The numerical abundance of flying predators/parasitoids of the above-ground herbivores is low. (8) The spatial distribution of some predators may be thermally restricted and less extensive than that of their prey. (9) Habitat temperature is the driving variable determining the flight activity patterns of insects. (10) Increased summer temperatures may alter or disrupt the seasonal patterns of insect emergence, particularly in species where the life cycle is cued into the seasonal rhythm. (11) The common species of arctic soil mites and Collembola are well adapted to survive enhanced summer temperatures, providing that moisture is not limited. (12) Water availability during the summer growing period is probably of greater significance than temperature in determining the survival and success of many arctic soil invertebrate groups. (13) Arctic soil microarthropod species are well adapted to survive and operate at subzero and low positive summer temperatures. (14) Freeze-thaw events represent critical points in the life history of the microarthropods. (15) Supercooling points are sometimes poor indicators of the capacity of arctic soil microarthopods to survive low temperatures. From these findings predictions are made as to how high arctic communities will respond to predicted changes in climate.

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.

Temperature variation and its biological significance in fellfield habitats on a maritime Antarctic island

Temperatures within soil and plant habitats on Signy Island in the maritime Antarctic were measured during 1987. Four sites were monitored using minithermistors attached to a data logging system. Three main periods within the annual temperature cycle were identified. In spring/summer (November–March) there was much inter-day variation in maximum temperatures, but minimum daily temperatures were always close to 0°C. However, there were very few freeze-thaw cycles extending below the −0.5°C threshold during this period, and those that occurred were not severe. It is considered that freeze-thaw cycling is unlikely to be a significant factor in organism survival during summer. All sites showed a long period of relatively mild subzero temperatures during autumn (March–May). This may be of importance in promoting cold-hardiness of organisms living in these ecosystems before the decline to lower winter temperatures. Minimum winter temperatures varied markedly between sites; lowest temperatures occurring in areas where there was little insulating snow cover. Within site temperature variation was generally small, confirming the validity of the use of small numbers of probes to monitor environmental temperatures in such habitats.

Effects of temperature elevation on a field population of Acyrthosiphon svalbardicum (Hemiptera: Aphididae) on Spitsbergen

A manipulation experiment was carried out on a field population of the aphid Acyrthosiphon svalbardicum near Ny Ålesund, on the high arctic island of Spitsbergen, using cloches to raise temperature. An average rise in temperature of 2.8 deg. C over the summer season markedly advanced the phenology of both the host plant Dryas octopetala and the aphid. Advanced aphid phenology, with concomitant increases in reproductive output and survival, and successful completion of the life-cycle led to an eleven-fold increase in the number of overwintering eggs. Thermal budget requirements in day degrees above 0°C were calculated for key life-cycle stages of the aphid. Temperature data from Ny Ålesund over the past 23 years were used to calculate thermal budgets for the field site over the same period and these were compared with the requirements of the aphid. Each estimated thermal budget was then adjusted to simulate the effect of a +2, +4, and −2deg. C change in average temperature on aphid performance. This retrospective analysis (i) confirms that the life-cycle of A. svalbardicum is well suited to exploit higher summer temperatures, (ii) indicates that the annual success of local populations are sensitive to small changes in temperature and (iii) suggests that the aphid is living at the limits of its thermal range at Ny Ålesund based on its summer thermal budget requirements.

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.

Cold hardiness of some Alpine Collembola

Abstract. 1 Individual supercooling points ranged from ‐2 to ‐44°C for six species of springtails, five species from the Swiss Alps and one from lowland Britain. Individuals of Isotomurus alticola (Carl) and Isotoma viridis Bourlet without gut contents had substantially lower supercooling points than those containing food material. 2 Juveniles were more cold resistant than adults in both I.alticola and Isotoma hiemalis Schött, both with respect to supercooling point and to their survival at prolonged subzero temperatures. 3 Temperature and acclimation time affected the degree of supercooling of four of the Alpine species especially I.hiemalis. 4 Duration of culture period had no consistent influence on the supercooling potential of all the species. 5 Tests for glycerol in the body fluids of the five Alpine springtails were negative, but the presence of a sugar, probably glucose, together with a five carbon polyhydric alcohol was indicated by chromatography.

Supercooling points of insects and mites on the Antarctic Peninsula

Abstract. 1. Mean supercooling points of eleven species of arthropods (three Collembola, seven Acari and one Diptera) ranged from ‐6.2 to ‐9.4°C (high group), and from ‐17.7 to ‐31.0°C (low group). The majority of individuals in the high group had food in their gut systems.

Desiccation stress at sub-zero temperatures in polar terrestrial arthropods

Cold tolerant polar terrestrial arthropods have evolved a range of survival strategies which enable them to survive the most extreme environmental conditions (cold and drought) they are likely to encounter. Some species are classified as being freeze tolerant but the majority of those found in the Antarctic survive sub-zero temperatures by avoiding freezing by supercooling. For many arthropods, not just polar species, survival of desiccating conditions is equally important to survival of low temperatures. At sub-zero temperatures freeze avoiding arthropods are susceptible to desiccation and may lose water due to a vapour diffusion gradient between their supercooled body fluids and ice in their surroundings. This process ceases once the body fluids are frozen and so is not a problem for freeze tolerant species. This paper compares five polar arthropods, which have evolved different low temperature survival strategies, and the effects of exposure to sub-zero temperatures on their supercooling points (SCP) and water contents. The Antarctic oribatid mite (Alaskozetes antarcticus) reduced its supercooling point temperature from -6 to -30 degrees C, when exposed to decreasing sub-zero temperatures (cooled from 5 to -10 degrees C over 42 days) with little loss of body water during that period. However, Cryptopygus antarcticus, a springtail which occupies similar habitats in the Antarctic, showed a decrease in both water content and supercooling ability when exposed to the same experimental protocol. Both these Antarctic arthropods have evolved a freeze avoiding survival strategy. The Arctic springtail (Onychiurus arcticus), which is also freeze avoiding, dehydrated (from 2.4 to 0.7 g water g(-1) dry weight) at sub-zero temperatures and its SCP was lowered from c. -3 to below -15 degrees C in direct response to temperature (5 to -5.5 degrees C). In contrast, the freeze tolerant larvae of an Arctic fly (Heleomyza borealis) froze at c. -7 degrees C with little change in water content or SCP during further cold exposure and survived frozen to -60 degrees C. The partially freeze tolerant sub-Antarctic beetle Hydromedion sparsutum froze at c. -2 degrees C and is known to survive frozen to -8 degrees C. During the sub-zero temperature treatment, its water content reduced until it froze and then remained constant. The survival strategies of such freeze tolerant and freeze avoiding arthropods are discussed in relation to desiccation at sub-zero temperatures and the evolution of strategies of cold tolerance.