Survival strategies in polar terrestrial arthropods

Three components of the survival strategy of a terrestrial Antarctic mite, Alaskozetes antarcticus (Acari: Cryptostigmata) are considered: overwintering survival, energetics and life history. Supercooling is an important feature of its cold tolerance, whilst elevation of standard metabolism allows activity at low temperatures, both of which contribute tcTa long development and maximum survival of individuals in the population. These are facets of the overall survival strategy evolved by such a species in response to the Antarctic terrestrial environment, but which may be widespread in polar invertebrates.     

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.     

Growth and survival strategy of the Antarctic mite Alaskozetes antarcticus

Growth and mortality rates of three juvenile instars and adults of the oribatid mite Alaskozetes antarcticus were measured over a twelve month period using field enclosures m Its maritime Antarctic habitat A pattern was found of rapid growth during the short summer period (0 2-0 4 μg dry weight increment per day) followed by gradual weight loss overwinter Most individuals completed one instar per year, reaching a premoult resting phase by late summer, with the moult being delayed and relatively synchronised early the next summer A small proportion of proto- and deutonymphs completed two moults within one summer period After the final moult adults overwintered again before commencing oviposition, suggesting that the life cycle (egg-egg) will take at least five years Mortality was not biased towards any instar or time of year Highest individual growth rates were obtained at a constant temperature of 7°C in the laboratory However expenmentai increase of mean field temperature from 2 7 to 4 3°C by use of a plastic cloche led to decreased growth, although no change in moulting frequency or mortality rate Laboratory survival was greatest at 2°C and decreased with increasing temperature
Alaskozetes antarcticus may be descnbed as 'a' (adversity) selected, showing an exceptionally long life cycle of five to six years and extensive physiological investment in survival adaptations Moult synchronisation in early summer, involving entering winter in the inactive premoult phase, will increase overwinter survival by reducing the chance of inoculative freezing from gut contents, and may be advantageous in maximising the time available for feeding during the subsequent summer, or ensuring proximity of the sexes after the final moult     

Invited review: climate change impacts in polar regions: lessons from Antarctic moss bank archives

Mosses are the dominant plants in polar and boreal regions, areas which are experiencing rapid impacts of regional warming. Long‐term monitoring programmes provide some records of the rate of recent climate change, but moss peat banks contain an unrivalled temporal record of past climate change on terrestrial plant Antarctic systems. We summarise the current understanding of climatic proxies and determinants of moss growth for contrasting continental and maritime Antarctic regions, as informed by 13C and 18O signals in organic material. Rates of moss accumulation are more than three times higher in the maritime Antarctic than continental Antarctica with growing season length being a critical determinant of growth rate, and high carbon isotope discrimination values reflecting optimal hydration conditions. Correlation plots of 13C and 18O values show that species (Chorisodontium aciphyllum / Polytrichum strictum) and growth form (hummock / bank) are the major determinants of measured isotope ratios. The interplay between moss growth form, photosynthetic physiology, water status and isotope composition are compared with developments of secondary proxies, such as chlorophyll fluorescence. These approaches provide a framework to consider the potential impact of climate change on terrestrial Antarctic habitats as well as having implications for future studies of temperate, boreal and Arctic peatlands. There are many urgent ecological and environmental problems in the Arctic related to mosses in a changing climate, but the geographical ranges of species and life‐forms are difficult to track individually. Our goal was to translate what we have learned from the more simple systems in Antarctica, for application to Arctic habitats.     

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.     

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     

An association between the Antarctic mite Alaskozetes antarcticus and an entomophthoralean fungus of the genus Neozygites

A fungal pathogen provisionally identified as Neozygites cf. acaridis has recently been isolated from the Antarctic oribatid mite Alaskozetes antarcticus. The identification of the fungus is discussed with reference to recent changes in the taxonomy of Neozygites. The potential role of the fungus in the Antarctic mite populations is considered in relation to the known mite life cycles, and the particular environmental conditions in the Antarctic.     

Protein synthesis and specific dynamic action in crustaceans: effects of temperature

Temperature influences the specific dynamic action (SDA), or rise in oxygen uptake rate after feeding, in eurythermal and stenothermal crustaceans by changing the timing and the magnitude of the response. Intra-specific studies on the eurythermal crab, Carcinus maenas, show that a reduction in acclimation temperature is associated with a decrease in SDA magnitude, resulting from an increase in SDA duration but a decrease in peak factorial scope (the factorial rise in peak SDA over prefeeding values). Inter-specific feeding studies on stenothermal polar isopods revealed marked differences in SDA response between the Antarctic species, Glyptonotus antarcticus and the Arctic species, Saduria entomon. Compared to S. entomon held at 4 and 13 degrees C, the SDA response in G. antarcticus held at 1 degrees C was characterised by a lower absolute oxygen uptake rate at peak SDA and an extended SDA duration. At peak SDA, whole animal rates of protein synthesis increased in proportion to the postprandial increase in oxygen uptake rate in the Antarctic and the Arctic species. Rates of oxygen uptake plotted against whole animal rates of protein synthesis gave similar relationships in both isopod species, indicating similar costs of protein synthesis after a meal, despite their differences in SDA response and thermal habitat.     

Can the Antarctic terrestrial midge,Eretmoptera murphyi,tolerate life in water?

1. Early‐season flooding and ice entrapment at sub‐zero temperatures pose significant challenges to any polar terrestrial invertebrate. 2. The chironomid midge, Eretmoptera murphyi, is native to the sub‐Antarctic island of South Georgia and has been introduced to the maritime Antarctic (Signy Island). While the majority of its 2‐year life cycle is spent as a terrestrial larva, it is found in habitats potentially exposed to prolonged flooding. 3. The current study explored the tolerance of the larvae to extended submergence, demonstrating survival for at least 28 days, underlain by their ability to respire (oxy‐regulate) whilst submerged. To date, this ability is not known to be shared by any other terrestrial midge. Larvae also demonstrated notable anoxia tolerance whilst encased in ice, surviving for up to 28 days. 4. These data indicate a capacity to survive ecologically relevant periods of submergence and/or ice entrapment, such as may be experienced in their natural habitats.     

Soil arthropods as indicators of water stress in Antarctic terrestrial habitats?

Abiotic features of Antarctic terrestrial habitats, particularly low temperatures and limited availability of liquid water, strongly influence the ecophysiology and life histories of resident biota. However, while temperature regimes of a range of land microhabitats are reasonably well characterized, much less is known of patterns of soil water stress, as current technology does not allow measurement at the required scale. An alternative approach is to use the water status of individual organisms as a proxy for habitat water status and to sample over several years from a population to identify seasonal or long‐term patterns. This broad generalization for terrestrial invertebrates was tested on arthropods in the maritime Antarctic. We present analyses of a long‐term data set of body water content generated by monthly sampling for 8–11 years of seven species of soil arthropods (four species of Acari, two Collembola and one Diptera) on maritime Antarctic Signy Island, South Orkney Islands. In all species, there was considerable within‐ and between‐sample variability. Despite this, clear seasonal patterns were present in five species, particularly the two collembolans and a prostigmatid mite. Analyses of monthly water content trends across the entire study period identified several statistically significant trends of either increase or decrease in body water content, which we interpret in the context of regional climate change. The data further support the separation of the species into two groups as follows: firstly, the soft‐bodied Collembola and Prostigmata, with limited cuticular sclerotization, which are sensitive to changes in soil moisture and are potentially rapid sensors of microhabitat water status, secondly, more heavily sclerotized forms such as Cryptostigmata (=Oribatida) and Mesostigmata mites, which are much less sensitive and responsive to short‐term fluctuations in soil water availability. The significance of these findings is discussed and it is concluded that annual cycles of water content were driven by temperature, mediated via radiation and precipitation, and constituted reliable indicators of habitat moisture regimes. However, detailed ecophysiological studies are required on particular species before such information can be used to predict over long timescales.     

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.     

Low temperature constrains growth rates but not short-term ingestion rates of Antarctic ciliates

Low environmental temperature is a major factor affecting the feeding activities, growth rates, and growth efficiencies of metazooplankton, but these features are poorly characterized for most protistan species. Laboratory experiments were conducted to examine the growth and ingestion rates of cultured herbivorous Antarctic ciliates. Three ciliates fed several algal species individually at 0 °C exhibited uniformly low growth rates (<0.26 day^?1), but the algae varied substantially in their ability to support ciliate growth. Specific ingestion rate (prey biomass consumed per unit ciliate biomass per unit time) was strongly affected by ciliate physiological state (starved vs. actively growing). Starved cells ingested many more prey than cells in balanced growth during short-term (minutes-to-hours) experiment but did not grow faster, indicating temperature compensation of ingestion rate but not growth rate. Field experiments were also conducted in the Ross Sea, Antarctica, to characterize the feeding rates of ciliates in natural plankton assemblages. Specific ingestion rates of two dominant ciliates were an order of magnitude lower than rates reported for temperate ciliates, but estimated rates were strongly affected by prey abundance. Our data indicate that short-term ingestion rates of Antarctic ciliates were not constrained by low environmental temperature although overall growth rates were, indicating the need for caution when designing experiments to measure the ingestion rates of these species at low environmental temperature. We present evidence that artifacts arising from estimating ingestion in short-term experiments may lead to errors in estimating feeding impact and growth efficiencies that are particularly large for polar protists.     

Cold adaptation in marine organisms

Animals from polar seas exhibit numerous so called resistance adaptations that serve to maintain homeostasis at low temperature and prevent lethal freezing injury. Specialization to temperatures at or below 0 degrees C is associated with an inability to survive at temperatures above 3-8 degrees C. Polar fish synthesize various types of glycoproteins or peptides to lower the freezing point of most extracellular fluid compartments in a non-colligative manner. Antifreeze production is seasonal in boreal species and is often initiated by environmental cues other than low temperature, particularly short day lengths. Most of the adaptations that enable intertidal invertebrates to survive freezing are associated with their ability to withstand ariel exposure. Unique adaptations for freezing avoidance include the synthesis of low molecular mass ice-nucleating proteins that control and induce extracellular ice-formation. Marine poikilotherms also exhibit a range of capacity adaptations that increase the rate of some physiological processes so as to partially compensate for the effects of low temperature. However, the rate of embryonic development in a diverse range of marine organisms shows no evidence of temperature compensation. This results in a significant lengthening of the time from fertilization to hatching in polar, relative to temperate, species. Some aspects of the physiology of polar marine species, such as low metabolic and slow growth rates, probably result from a combination of low temperature and other factors such as the highly seasonal nature of food supplies. Although neuromuscular function shows a partial capacity adaptation in Antarctic fish, maximum swimming speeds are lower than for temperate and tropical species, particularly for early stages in the life history.     

Profiles of soluble carbohydrates and their adaptive role in maritime Antarctic terrestrial arthropods

The existence of seasonal changes in concentrations of water-soluble carbohydrates in arthropods (both freezing-tolerant and intolerant species) from Signy Island was demonstrated. Seasonal patterns of variation, imposed by seasonality of the maritime Antarctic environment, in the production of soluble carbohydrates in response to low temperatures and/or dehydration for a range of terrestrial arthropods were confirmed. The freshwater copepod Pseudoboeckellapoppei exhibited much lower levels of soluble carbohydrates, with glycerol as the main component, and smaller seasonal fluctuations relative to the four terrestrial species. The two Antarctic mites (Alaskozetes antarcticus and Gamasellus racovitzai) accumulated glycerol (as a single-component cryoprotective system), in agreement with previous work reporting increased glycerol levels and lowering of the supercooling point in A. antarcticus. In the case of G. racovitzai, increased levels of glycerol may function in a different manner. The larval dipteran Eretmoptera murphyi and the collembolan Cryptopygus antarcticus have complex multi-component cryoprotective systems involving trehalose that may be related to low temperature acclimation and dehydration. These findings are discussed in relation to published work on single and multiple cryoprotective systems, supercooling points and the involvement of dehydration as a complementary stress in overwintering insects. Received: 28 February 1997 / Accepted: 20 October 1997     

Mite dispersal among the Southern Ocean Islands and Antarctica before the last glacial maximum

It has long been maintained that the majority of terrestrial Antarctic species are relatively recent, post last glacial maximum, arrivals with perhaps a few microbial or protozoan taxa being substantially older. Recent studies have questioned this 'recolonization hypothesis', though the range of taxa examined has been limited. Here, we present the first large-scale study for mites, one of two dominant terrestrial arthropod groups in the region. Specifically, we provide a broad-scale molecular phylogeny of a biologically significant group of ameronothroid mites from across the maritime and sub-Antarctic regions. Applying different dating approaches, we show that divergences among the ameronothroid mite genera Podacarus, Alaskozetes and Halozetes significantly predate the Pleistocene and provide evidence of independent dispersals across the Antarctic Polar Front. Our data add to a growing body of evidence demonstrating that many taxa have survived glaciation of the Antarctic continent and the sub-Antarctic islands. Moreover, they also provide evidence of a relatively uncommon trend of dispersals from islands to continental mainlands. Within the ameronothroid mites, two distinct clades with specific habitat preferences (marine intertidal versus terrestrial/supralittoral) exist, supporting a model of within-habitat speciation rather than colonization from marine refugia to terrestrial habitats. The present results provide additional impetus for a search for terrestrial refugia in an area previously thought to have lacked ice-free ground during glacial maxima.     

Temporal resolution of cold acclimation and de-acclimation in the Antarctic collembolan, Cryptopygus antarcticus

Abstract.  The Antarctic collembolan, Cryptopygus antarcticus (Willem), can switch its supercooling point (SCP) between 'winter' and 'summer' modes of cold hardiness over a matter of hours. High resolution temporal scaling of the acquisition and loss of cold hardiness is undertaken by assaying changes in the proportion of animals freezing below −15 °C in response to cooling rate, acclimation temperature, and access to food and moisture. Rapid de-acclimation to the 'summer' modal state is readily achieved after 1–6 h in response to warming and access to food; however, rapid acclimation to the 'winter' modal state is only evident in response to slow cooling and narrow ranges of temperature (0–5 °C). The rapid loss of cold tolerance at higher temperatures with access to food, in particular, emphasizes this species' opportunistic responses to resource availability in the short polar summers. Cold hardiness is apparently more readily traded off against nutrient acquisition than vice versa in this maritime Antarctic species.     

Desiccation tolerance and drought acclimation in the Antarctic collembolan Cryptopygus antarcticus

The availability of water is recognized as the most important determinant of the distribution and activity of terrestrial organisms within the maritime Antarctic. Within this environment, arthropods may be challenged by drought stress during both the austral summer, due to increased temperature, wind, insolation, and extended periods of reduced precipitation, and the winter, as a result of vapor pressure gradients between the surrounding icy environment and the body fluids. The purpose of the present study was to assess the desiccation tolerance of the Antarctic springtail, Cryptopygus antarcticus, under ecologically-relevant conditions characteristic of both summer and winter along the Antarctic Peninsula. In addition, this study examined the physiological changes and effects of mild drought acclimation on the subsequent desiccation tolerance of C. antarcticus. The collembolans possessed little resistance to water loss under dry air, as the rate of water loss was >20% h(-1) at 0% relative humidity (RH) and 4 degrees C. Even under ecologically-relevant desiccating conditions, the springtails lost water at all relative humidities below saturation (100% RH). However, slow dehydration at high RH dramatically increased the desiccation tolerance of C. antarcticus, as the springtails tolerated a greater loss of body water. Relative to animals maintained at 100% RH, a mild drought acclimation at 98.2% RH significantly increased subsequent desiccation tolerance. Drought acclimation was accompanied by the synthesis and accumulation of several sugars and polyols that could function to stabilize membranes and proteins during dehydration. Drought acclimation may permit C. antarcticus to maintain activity and thereby allow sufficient time to utilize behavioral strategies to reduce water loss during periods of reduced moisture availability. The springtails were also susceptible to desiccation at subzero temperatures in equilibrium with the vapor pressure of ice; they lost approximately 40% of their total body water over 28 d when cooled to -3.0 degrees C. The concentration of solutes in the remaining body fluids as a result of dehydration, together with the synthesis of several osmolytes, dramatically increased the body fluid osmotic pressure. This increase corresponded to a depression of the melting point to approximately -2.2 degrees C, and may therefore allow C. antarcticus to survive much of the Antarctic winter in a cryoprotectively dehydrated state.     

Living on the edge – plants and global change in continental and maritime Antarctica

Antarctic terrestrial ecosystems experience some of the most extreme growth conditions on Earth and are characterized by extreme aridity and subzero temperatures. Antarctic vegetation is therefore at the physiological limits of survival and, as a consequence, even slight changes to growth conditions are likely to have a large impact, rendering Antarctic terrestrial communities sensitive to climate change. Climate change is predicted to affect the high‐latitude regions first and most severely. In recent decades, the Antarctic has undergone significant environmental change, including the largest increases in ultraviolet‐B (UV‐B; 290–320 nm) radiation levels in the world and, in the maritime region at least, significant temperature increases. This review describes the current evidence for environmental change in Antarctica, and the impacts of this change on the terrestrial vegetation. This is largely restricted to cryptogams, such as bryophytes, lichens and algae; only two vascular plant species occur in the Antarctic, both restricted to the maritime region. We review the range of ecological and physiological consequences of increasing UV‐B radiation levels, and of changes in temperature, water relations and nutrient availability. It is clear that climate change is already affecting the Antarctic terrestrial vegetation, and significant impacts are likely to continue in the future. We conclude that, in order to gain a better understanding of the complex dynamics of this important system, there is a need for more manipulative, long‐term field experiments designed to address the impacts of changes in multiple abiotic factors on the Antarctic flora.     

Hybridization of Southern Hemisphere blue whale subspecies and a sympatric area off Antarctica: impacts of whaling or climate change?

Understanding the degree of genetic exchange between subspecies and populations is vital for the appropriate management of endangered species. Blue whales (Balaenoptera musculus) have two recognized Southern Hemisphere subspecies that show differences in geographic distribution, morphology, vocalizations and genetics. During the austral summer feeding season, the Antarctic blue whale (B. m. intermedia) is found in polar waters and the pygmy blue whale (B. m. brevicauda) in temperate waters. Here, we genetically analyzed samples collected during the feeding season to report on several cases of hybridization between the two recognized blue whale Southern Hemisphere subspecies in a previously unconfirmed sympatric area off Antarctica. This means the pygmy blue whales using waters off Antarctica may migrate and then breed during the austral winter with the Antarctic subspecies. Alternatively, the subspecies may interbreed off Antarctica outside the expected austral winter breeding season. The genetically estimated recent migration rates from the pygmy to Antarctic subspecies were greater than estimates of evolutionary migration rates and previous estimates based on morphology of whaling catches. This discrepancy may be due to differences in the methods or an increase in the proportion of pygmy blue whales off Antarctica within the last four decades. Potential causes for the latter are whaling, anthropogenic climate change or a combination of these and may have led to hybridization between the subspecies. Our findings challenge the current knowledge about the breeding behaviour of the world's largest animal and provide key information that can be incorporated into management and conservation practices for this endangered species.