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. 2. Two species, the isotomid collembolan Cryptopygus antarcticus Willem and the oribatid mite Alaskozetes antarcticus (Michael), are examined in detail, and afford a comparative approach to the mechanisms underlying cold tolerance in insect and arachnid types. 3. All microarthropods appear to be freezing-susceptible (unable to tolerate tissue ice), and they utilize varying levels of supercooling to avoid freezing. Gut contents are considered to be the prime nucleation site in most arthropods when supercooled, particularly for Antarctic species. Moulting also increases individual supercooling ability especially in Collembola, and the activity of ice-nucleating bacteria in cold-hardy arthropods may be important. 4. Sources of ice nucleators are many and varied, originating externally (motes) or internally (ice-nucleating agents). They act either extracellularly (mainly in the haemolymph) to promote freezing in ice-tolerant life stages, or intracellularly in freezing-susceptible forms. Thermal hysteresis proteins, acting colligatively, occur in many arthropods including Collembola; they depress both the freezing point of body fluids and the whole-body supercooling point of freezing- susceptible and freezing-tolerant species. 5. Bimodal supercooling point distributions are a feature of microarthropods and water droplets. Samples of field populations of Antarctic mites and springtails show significant seasonal changes in these distributions, which in some respects are analogous to purely physical systems of water droplets. Supercooling points are confirmed as accurate measures of cold-hardiness and survival for Antarctic species, but not necessarily for other arthropods. The effects of constant sub-zero temperatures approaching the limit of the supercooling ability of arthropods require study. 6. Desiccation and dehydration influence microarthropod physiology in several ways; in Alaskozetes it triggers glycerol synthesis. Glycerol may aid binding of water in severely dehydrated insects, but the relationship of such ‘bound’ water to cold-hardiness is unclear. 7. Sugar alcohols (polyols) and sugars are accumulated as potential cryoprotectants in many arthropods at low temperatures, and antifreeze systems may be single or multi-component in structure. Cryoprotectant synthesis and regulation have been studied principally in insects, and fresh weight concentrations of 0–3-5 M of polyols have been found. Trehalose accumulation may also influence cold-hardiness. 8. Microarthropods fall within the spectrum of cold tolerance observed for arthropods and other invertebrates. No special adaptations are found in Antarctic species, and similar strategies and mechanisms are present in both insects and arachnids. The colonization and maintenance of microarthropod populations of polar land habitats seem not to have required the evolution of any novel features with respect to cold tolerance.     

The effect of feeding on specific soil algae on the cold-hardiness of two Antarctic micro-arthropods (Alaskozetes antarcticus and Cryptopygus antarcticus)

The effect of consuming terrestrial algae on the cold tolerance of two Antarctic micro-arthropods was examined. From the results of preferential feeding experiments, seven species of Antarctic terrestrial micro-algae were chosen and fed to two common, freeze-avoiding Antarctic micro-arthropods: the springtail Cryptopygus antarcticus (Collembola: Isotomidae), and the mite Alaskozetes antarcticus (Acari: Oribatida). Mites were very selective in their choice of food whereas the springtails were less discriminating. The ice nucleating activity of each species of alga was measured using an ice nucleator spectrometer and a differential scanning calorimeter. Pure cultures of individual species of algae had characteristic supercooling points ranging from ca. −5 to −18 °C. The effect of eating a particular alga on the supercooling point of individual micro-arthropods cultured at two different temperatures (0 and 10 °C) was examined. Neither species showed a preference for algae with low ice-nucleating activity and there was no clear correlation between the supercooling point of food material and that of the whole animal. However, feeding on certain algae such as Prasiola crispa, which contained the most active ice nucleators, decreased the cold tolerance of both species of arthropods. Accepted: 6 May 2000     

Experimental studies on the cold tolerance of Alaskozetes antarcticus

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.     

Energy contents and organic constituents in Antarctic and south Chilean marine brown algae

The content of proteins, lipids and carbohydrates and the calorific contents in six Antarctic and three south Chilean brown algae were determined. These constitute the first reports of chemical composition in the endemic Antarctic species Cystosphaera jacquinotii, Phaeurus antarcticus and Desmarestia antarctica. There were no marked differences in total energy levels between Antarctic and cold-temperate species (values between 10.6 and 13 kJ g^–1 dry weight). However, species such as Adenocystis utricularis showed significantly higher ash-free energy (26.3 kJ), which is explained in terms of morpho-functional differentiation. Ascoseira mirabilis and Phaeurus antarcticus showed high total lipids (2.1–2.2% dry weight) and soluble carbohydrates (5.9 and 3.4% dry weight). In general, algae from Chile had similar energy levels and no obvious differences in organic content could be found.     

Cold tolerance of alpine,Arctic, and Antarctic Collembola and mites

Because of their dominant role in the fauna of alpine, Arctic and Antarctic locations Collembola and mites are of particular interest regarding adaptations to low temperatures. No freezing-tolerant species have been found in these groups of terrestrial arthropods, and it appears that all species depend entirely on supercooling to survive the lower temperatures of their habitats. While summer animals have high supercooling points, an increase in supercooling ability occurs during autumn and early winter, and can be explained as a two-step process. Initially gut content has to be eliminated to avoid heterogeneous nucleation at high subzero temperatures due to foreign nucleating agents. Second, supercooling is further enhanced through accumulation of glycerol or other lowmolecular cryoprotective substances. Further studies are needed on the ability of such animals to avoid inoculative freezing in their microhabitats.     

Multiple stress tolerance in an antarctic terrestrial arthropod: Belgica antarctica

Terrestrial arthropods of the maritime Antarctic experience a diverse range of environmental Stressors including extended periods of ice and snow cover, anoxia, immersion in water of variable pH and salinity, and extensive habitat drying. The collembolan Cryptopygus antarcticus and the mite Alaskozetes antarcticus seasonally depress whole body supercooling points to avoid the lethal effects of freezing. Alternatively, the wingless chironomid Belgica antarctica has a relatively limited supercooling capacity (between −6 and −8 °C) and tolerates extracellular freezing. The lower limit of freeze tolerance remains unchanged near −13 °C throughout the year in B. antarctica. Summer larvae tolerate dehydration to a limit of 35% of initial body weight as well as extended periods of anoxia and immersion in freshwater and saltwater. Two weeks of exposure to variable pH (3–12) induced no mortality.     

Food choice of Antarctic soil arthropods clarified by stable isotope signatures

Antarctic soil ecosystems are amongst the most simplified on Earth and include only few soil arthropod species, generally believed to be opportunistic omnivorous feeders. Using stable isotopic analyses, we investigated the food choice of two common and widely distributed Antarctic soil arthropod species using natural abundances of ¹³C and ¹⁵N and an isotope labelling study. In the laboratory we fed the isotomid springtail Cryptopygus antarcticus six potential food sources (one algal species, two lichens and three mosses). Our results showed a clear preference for algae and lichens rather than mosses. These results were corroborated by field data comparing stable isotope signatures from the most dominant cryptogams and soil arthropods (C. antarcticus and the oribatid mite Alaskozetes antarcticus). Thus, for the first time in an Antarctic study, we present clear evidence that these soil arthropods show selectivity in their choice of food and have a preference for algae and lichens above mosses.     

Terrestrial arthropods and low temperature

Cold environments impose several ecological and physiological constraints upon arthropods, including reduction of metabolic rate, locomotory activity, and feeding. These result in slow growth rates and extended life cycles. Additionally, the probability of freezing is accentuated at subzero temperatures. Using data for Antarctic mites, the interplay of such constraints is examined, and the resultant ecophysiological adaptations outlined for a common oribatid mite (Alaskozetes antarcticus) of the maritime Antarctic. The synthesis suggests that its survival strategy is comprised of two components. First, the utilization of above-zero temperatures during the short austral summer to maximize growth and production, and thereby reproduce. These processes are aided by an elevation of its standard metabolic rate, commonly termed cold adaptation. Second, the tolerance of freezing temperatures by supercooling of all its postovum life stages throughout the entire year. Its supercooling potential is enhanced by the presence of glycerol and other polyols in the body fluids, the production of which is mediated by environmental temperature and desiccation at low relative humidities. Thus this species, in common perhaps with many other freezing susceptible arthropods, has ensured its survival in southern polar habitats by the evolution of a bipartite adaptational strategy.     

Adaptations for the maintenance of water balance by three species of Antarctic mites

Three species of Antarctic mites, Alaskozetes antarcticus, Hydrogamasellus antarcticus and Rhagidia gerlachei, are abundant in the vicinity of Palmer Station, Antarctica. No single mechanism for reducing water stress was shared by all three species. A. antarcticus and R. gerlachei (both ca. 200 μg) are over twice as large as H. antarcticus (ca. 90 μg), but all had similar body water content (67%) and tolerated a loss of up to 35% of their body water before succumbing to dehydration. All imbibed free water and had the capacity to reduce water loss behaviorally by forming clusters. Alaskozetes antarcticus was distinct in that it relied heavily on water conservation (xerophilic classification) that was largely achieved by its thick cuticular armor, a feature shared by all members of this suborder (Oribatida), and abundant cuticular hydrocarbons. In comparison to the other two species, A. antarcticus was coated with 2–3× the amount of cuticular hydrocarbons, had a 20-fold reduction in net transpiration rate, and had a critical transition temperature (CTT) that indicates a pronounced suppression in activation energy (E _a) at temperatures below 25°C. In contrast, H. antarcticus and R. gerlachei lack a CTT, have lower amounts of cuticular hydrocarbons and have low E _as and high net transpiration rates, classifying them as hydrophilic. Only H. antarcticus was capable of utilizing water vapor to replenish its water stores, but it could do so only at relative humidities close to saturation (95–98 %RH). Thus, H. antarcticus and R. gerlachei require wet habitats and low temperature to counter water loss, and replace lost water behaviorally through predation. Compared to mites from the temperate zone, all three Antarctic species had a lower water content, a feature that commonly enhances cold tolerance.     

Antarctic Collembolans Use Chemical Signals to Promote Aggregation and Egg Laying

Terrestrial arthropods that reside in Antarctica are exposed to considerable periods of environmental stress, thus factors that promote identification of favorable microhabitats are extremely important. In this study, we report the presence of chemical cues that induce oviposition and aggregation in two species of Antarctic collembolans, Cryptopygus antarcticus and Friesea grisea. Responses of the Collembola were enhanced by low temperatures but were not altered by humidity. One of the major physiological benefits derived from an aggregation was a substantial reduction in water loss rates. Although F. grisea and C. antarcticus were commonly found in cross-species aggregations, we found no evidence to suggest cross-species attraction. When individuals were exposed to areas previously occupied by groups of Collembola, more eggs were laid. Thus, chemicals released by the collembolans appear to induce both aggregation and oviposition in these Antarctic species.     

Lipids of Antarctic salps and their commensal hyperiid amphipods

Antarctic salps (Salpa thompsoni and Ihlea racovitzai) and their commensal hyperiid amphipods (Vibilia antarctica, Cyllopus lucasii and C. magellanicus) were collected near Elephant Island, in the South Shetland Islands, during 1997 and the salp-rich year 1998. The sterol composition of aggregate S. thompsoni and I. racovitzai (mostly 24-methyl-5,22E-dien-3β-ol, 24-nordehydrocholesterol, cholesterol and trans-dehydrocholesterol) was reflected in the sterol composition of the commensal amphipods and was consistent with a herbivorous planktonic diet. This was not the case for solitary S. thompsoni, with 24-methylenecholesterol as the major sterol. There was a greater abundance of aggregate salp stanols in 1997 (11.7% total sterols) than 1998 (5.2%) and these different stanol levels were reflected in the commensal amphipods. Eicosapentaenoic acid [20:5(n-3)] and docosahexaenoic acid [22:6(n-3)] were the major polyunsaturated fatty acids (PUFA) in all organisms. Octadecapentaenoic acid [18:5(n-3)] comprised 0.4–5.8% (of total fatty acids) in all 1998 salps and amphipods, but was absent in 1997 samples. This suggests a greater presence of dinoflagellates or other species rich in 18:5(n-3) in the “salp year” 1998. Very long chain PUFA (C₂₄, C₂₆, C₂₈) were also only detected in 1998 samples (up to 5.3%), reflecting commensalism and greater presence of dinoflagellates or species containing very long chain PUFA. Examination of the biomarker lipids has provided an indication of trophic interactions for these Antarctic salps and their commensal hyperiid amphipods. Accepted: 8 November 1999     

The diet of the Antarctic fur seal Arctocephalus gazella at Harmony Point, Nelson Island, South Shetland Islands

The diet of non-breeding male Antarctic fur seals (Arctocephalus gazella) was investigated at Harmony Point, Nelson Island, South Shetland Islands, by the analysis of 18 and 33 scats collected during February 1996 and 1997 respectively. Overall, fish were the most frequent prey (74.5%) and predominated by mass (54.4%), whereas krill predominated by number (94.2%). This coincides well with the pattern observed in 1997, but in 1996 krill was the most important prey by number and mass (50.2%). The importance of the remaining taxa represented in the samples (octopods, hyperiids and bivalves) was negligible. Among fish, myctophids represented 85.2% of the fish mass, with Gymnoscopelus nicholsi and Electrona antarctica being the main prey. These two species predominated in 1997, whereas the channichthyid Cryodraco antarcticus and the nototheniid Gobionotothen gibberifrons were dominant in 1996. The importance of the myctophids as prey of the Antarctic fur seal is discussed. Received: 7 October 1997 / Accepted: 24 May 1998     

Trade-offs between microhabitat selection and physiological plasticity in the Antarctic springtail, <Emphasis Type="Italic">Cryptopygus antarcticus</Emphasis> (Willem)

In the maritime Antarctic, terrestrial arthropods have recourse to two strategies to mitigate low summer temperatures: (1) physiological plasticity and (2) avoidance via microhabitat insulation. This study investigated the interaction between these strategies in the springtail, Cryptopygus antarcticus, established in situ within contrasting microcosms (buffered vs. exposed) and within two sets of habitat simulations (wet vs. dry) over diurnal scales through the Antarctic summer. Significant differences were found in the cold hardiness of springtails sampled simultaneously from each microcosm. Exposed animals showed greater plasticity in the “true” austral summer, but as field temperatures declined preceding the onset of winter, buffered animals showed greater resilience. Overall, water was found to inhibit the buffering effect of moss and there was a significantly greater discrimination between buffered and exposed microcosms in the dry treatment. Analysis of microhabitat temperatures indicate that it is thermal variability not lower temperature that is responsible for the greater plasticity of exposed animals.     

Variation in summer cold-hardiness of the Antarctic oribatid mite Alaskozetes antarcticus from contrasting habitats on King George Island

Summary The Antarctic oribatid mite Alaskozetes antarcticus was collected from several field habitats near Great Wall Station (62°13S, 58°58W) on King George Island during January and February 1990. The tritonymphs and adults were examined for their supercooling ability and survival at subzero temperatures in relation to inoculative freezing. The active tritonymphs and adults showed a wide range of supercooling points probably due to their polyphagous feeding activity and humid habitat conditions, with means ranging from -3.8° to -22.4°C. Detrivores were inferior to algivores in their supercooling ability. The former seemed to be transiently exposed to the hazard of freezing during the cool Antarctic summer. The resting (premoulting) tritonymphs exhibited the lowest mean supercooling point of -28.3°C. Inoculative freezing reduced the survival of A. antarcticus. Its effect became conspicuous at temperatures below -20°C and was serious in the deeply supercooled individuals, such as resting tritonymphs and algivorous adults. During the active season, spontaneous freezing probably started from the gut contents seemed to be more fatal than inoculative freezing for this freeze intolerant species.     

The terrestrial arthropod fauna of the Byers Peninsula,Livingston Island,South Shetland Islands – Collembola

 As an addendum to a recent publication on the terrestrial arthropod fauna of the Byers Peninsula Site of Special Scientific Interest (SSSI), which included preliminary identification of four Collembola, we now present detailed information on Collembola occurring within the SSSI. Five species were recorded [Friesea grisea (Schaffer), Tullbergia mixta Wahlgren, Isotoma (Folsomotoma) octooculata (Willem), Cyptopygus antarcticus Willem, and Cryptopygus sp. nov.]. Species occurrence and abundance differed between samples collected from poorly vegetated stony ground and vegetation cores. F. grisea was both the commonest (58% of individuals) and the most widely distributed (18/19 samples) springtail in the former habitat. Cryptopygus sp. nov. was recorded only in the vegetation core samples. All five species were more evenly distributed in vegetation samples, although C. antarcticus and Cryptopygus sp. nov. were again the least abundant. A list of the terrestrial arthropods of the SSSI is presented. Received: 7 June 1995/Accepted: 25 July 1995     

The contrasting diet of Harpagifer antarcticus (Notothenioidei, Harpagiferidae) at two localities of the South Shetland Islands, Antarctica

The diet of Harpagifer antarcticus was studied at two localities of the South Shetland Islands, Antarctica. The analysis of the stomach contents of specimens collected in tide pools at Potter Cove, King George Island, indicated that gammarid amphipods (mainly Gondogeneia sp.) were the main prey of this fish, followed by polychaetes, gastropods and isopods. By contrast, the specimens from Harmony Point, Nelson Island, which were recovered from stomach contents of Antarctic shags Phalacrocorax bransfieldensis feeding at depths of 46–110 m, preyed almost exclusively on the Antarctic krill Euphausia superba. These results are discussed and compared with previous studies. Received: 27 August 1997 / Accepted: 17 November 1997     

Seasonal lipid contents of Antarctic microarthropods

A technique for the accurate determination of lipid content of very small quantities of biological tissue was applied to two Antarctic oribatid mites,Alaskozetes antarcticus andHalozetes belgicae, and a collembolan,Cryptopygus antarcticus. Analysis of monthly samples of the three species, collected between November 1989 and March 1991, revealed little evidence of any seasonal pattern of lipid deposition or use. MaleAlaskozetes were the only exception, showing very low lipid levels for a short period of the austral summer, followed by rapid deposition before the onset of winter. Mean lipid contents of the three species over the study period were 10–15% of mean dry weight. There was evidence of a seasonal pattern of egg formation and oviposition in bothAlaskozetes andHalozetes, but this was not reflected in the observed lipid levels. Feeding activity was mostly restricted to the summer months (November–March); a temporary resumption of feeding in winter (late August 1990) was followed by an increase in lipid content in both sexes ofAlaskozetes.     

Reproductive biology of caridean decapods from the Weddell Sea

Summary Data on reproductive biology are presented for five benthic caridean shrimps from the high Antarctic (Chorismus antarcticus, Notocrangon antarcticus, Nematocarcinus lanceopes, Lebbeus antarcticus and Eualus kinzeri). The first three species were very common on the Weddell Sea shelf and upper slope, whereas only a few individuals of the other two species were caught-but these did include some ovigerous females. Our measurements include size at first maturity, fecundity (total number and mass of eggs), individual egg mass, egg length, ovary indices, maximum size encountered and documentation of the reproductive cycle in spring and summer. Egg number generally increases with female size, and the largest species (N. lanceopes) also carries the highest number of eggs. The eggs of all high Antarctic species are large, the extreme being L. antarcticus with an egg length of up to 3.3 mm. For C. antarcticus and N. antarcticus, which have wide geographic distributions, a comparison is made with older published and unpublished data from the Subantarctic (South Georgia). High Antarctic representatives of these two species grow to a larger maximum size, attain sexual maturity later in their life cycle, and produce fewer and larger eggs in relation to both carapace length and female mass, than their Subantarctic counterparts.Data presented here were collected during the European Polarstern Study (EPOS) sponsored by the European Science Foundation     

Effects of Late-Cenozoic Glaciation on Habitat Availability in Antarctic Benthic Shrimps (Crustacea: Decapoda: Caridea)

Marine invertebrates inhabiting the high Antarctic continental shelves are challenged by disturbance of the seafloor by grounded ice, low but stable water temperatures and variable food availability in response to seasonal sea-ice cover. Though a high diversity of life has successfully adapted to such conditions, it is generally agreed that during the Last Glacial Maximum (LGM) the large-scale cover of the Southern Ocean by multi-annual sea ice and the advance of the continental ice sheets across the shelf faced life with conditions, exceeding those seen today by an order of magnitude. Conditions prevailing at the LGM may have therefore acted as a bottleneck event to both the ecology as well as genetic diversity of today''s fauna. Here, we use for the first time specific Species Distribution Models (SDMs) for marine arthropods of the Southern Ocean to assess effects of habitat contraction during the LGM on the three most common benthic caridean shrimp species that exhibit a strong depth zonation on the Antarctic continental shelf. While the shallow-water species Chorismus antarcticus and Notocrangon antarcticus were limited to a drastically reduced habitat during the LGM, the deep-water shrimp Nematocarcinus lanceopes found refuge in the Southern Ocean deep sea. The modeling results are in accordance with genetic diversity patterns available for C. antarcticus and N. lanceopes and support the hypothesis that habitat contraction at the LGM resulted in a loss of genetic diversity in shallow water benthos.