The biology, life cycle and ecophysiology of the Antarctic mite Alaskozetes antarcticus

This paper is dedicated to the late Nigel Bonner, who as Head of the Life Sciences Division at British Antarctic Survey, encouraged and supported this research with his characteristic enthusiasm.
The cryptostigmatid mite Alaskozetes antarcticus (Michael) is a dominant member of many terrestrial communities in the maritime Antarctic, where it survives extreme temperatures, short cold summers, numerous freeze-thaw cycles, desiccating conditions and a limited season for growth and reproduction. However, examination of features of its biology, from morphology, through life-history strategy to physiology, indicate very little specialization to the Antarctic environment. Alaskozetes antarcticus is a herbivore/detritivore, typical of the Cryptostigmata in general, with low feeding and growth rates, long life span and low reproductive output. Physiological specializations exist in the form of low enzyme activation energies and elevated metabolic rates at low temperatures when compared with temperate species, and associated low optimum temperatures for activity, feeding and growth. Growth rates comparable with temperate species are achieved in the field, with an extended life cycle of five years or more as a result of the short growing season, and the ability of all life stages to overwinter equally successfully. Overwintering survival, involving supercooling enhanced by the use of antifreezes such as glycerol, although initially described in Antarctic species, is now known to be characteristic of many temperate relatives, so it is not a specific adaptation to the polar environment. The obvious success of A. antarcticus in maritime Antarctic terrestrial environments must be attributed to a combination of several features characteristic of the Cryptostigmata in general, rather than to specific polar adaptations.     

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.     

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.     

Responses to desiccation in four Coleopterans from sub-Antarctic South Georgia

RATES OF WATER LOSS WERE DETERMINED FOR FOUR COLEOPTERA SPECIES: the herbivores Hydromedion sparsutum, Perimylops antarcticus (Family Perimylopidae) and the carnivores Trechisibus antarcticus, Oopterus soledadinus (Family Carabidae) collected during summer from a range of terrestrial habitats at South Georgia. A recording microbalance enabled measurement of individual weight loss with time in <5% r.h. at 10, 20, 30 and 35 degrees C. Adults of T. antarcticus had significantly higher rates of water loss than any other species over all temperatures. Individuals of both herbivores exhibited the slowest water loss rates under the experimental conditions. Within species, rates at 10 or 20 degrees C were slower than at the higher temperatures. Adult P. antarcticus had significantly greater amounts of body water than adult H. sparsutum for each of the four temperatures. Within species and life-stages of both herbivores, body water contents after drying at 10 degrees C were significantly lower than individuals dried at 30-35 degrees C, but no such differences were observed for the carnivores. At each temperature, rates of water loss were negatively correlated with initial live weight in all four species, but this was not the case within species or between adults and larvae. Maximum survival times during desiccation declined as temperature increased, but did not differ between species at 10 degrees C. Over 30-35 degrees C, survival times of both herbivores were significantly longer than either of the carnivores. Smaller insects (e.g. the carabids) had faster rates of water loss than the larger perimylopids under the same environmental conditions. The latter had greater resistance to desiccation than the former. It is suggested that the larger body water content of P. antarcticus enables it to resist desiccation more than the other three species, which correlates with its ecological distribution. Differences in water contents after drying individuals at low and high temperatures may be caused either by the water binding properties of cells and tissues or by reduction in energy stores in order to maintain metabolism at lower environmental temperatures causing a body weight loss. Whilst both herbivores show some physiological adaptations to drying conditions, it is suggested that the two carnivorous beetles may have adapted behaviourally to the South Georgia environment.     

<Emphasis Type="Italic">Planococcus antarcticus</Emphasis> and<Emphasis Type="Italic"> Planococcus psychrophilus</Emphasis> spp. nov. isolated from cyanobacterial mat samples collected from ponds in Antarctica

Thirteen orange-pigmented bacteria associated with cyanobacterial mat samples collected from four different lakes in McMurdo, Antarctica, were isolated. Twelve of the isolates, which were coccoid in shape, were very similar and possessed all the characteristics of the genus Planococcus and represented a new species, which was assigned the name Planococcus antarcticus sp. nov. (CMS 26or(T)). Apart from the phenotypic differences, P. antarcticus differed from all reported species of Planococcus by more than 2.5% at the 16S rRNA gene sequence level. In addition, at the DNA-DNA hybridization level, it exhibited very little similarity either with P. mcmeekinii (30%-35%), P. okeanokoites (26%-29%), or CMS 53or(T) (15%-25%), the three species with which it is closely related at the rRNA gene sequence level (2.5%-2.9%). P. antarcticus also showed only 2.5% difference in its 16S rRNA gene sequence compared with the P. alkanoclasticus sequence. But it was distinctly different from P. alkanoclasticus, which exists only as rods, is mesophilic and phosphatase positive, can hydrolyze starch, cannot utilize succinate, glutamate, or glucose, and cannot acidify glucose. Most important, P. antarcticus and P. alkanoclasticus varied distinctly in their fatty acid composition in that C(15:0), C(15:1), C(16:0), iso-C(16:1), and C(17:0) were present only in P. antarcticus but absent in P. alkanoclasticus. CMS 53or(T), the thirteenth isolate, was also identified as a new species of Planococcus and was assigned the name Planococcus psychrophilus sp. nov. This species was distinctly different from all the reported species, including the new species P. antarcticus, with respect to a number of phenotypic characteristics. At the 16S rRNA gene sequence level, it was closely related to P. okeanokoites (98.1%) and P. mcmeekinii (98%), but with respect to the DNA-DNA hybridization, the similarity was only 35%-36%. The type strain of P. antarcticus is CMS 26or(T) (MTCC 3854; DSM 14505), and that of P. psychrophilus is CMS 530r(T) (MTCC 3812; DSM 14507).     

Position-independent and tissue-specific expression of porcine whey acidic protein gene from a bacterial artificial chromosome in transgenic mice

Silencing of transgenes is a frequent event after the random integration of foreign DNA in the host genome following microinjection. Long genomic fragments are expected to contain all the regulatory elements necessary to induce an appropriate expression of transgenes. A bacterial artificial chromosome containing the porcine wap gene with approximately 145 and 5 kb of 5'- and 3'-flanking sequences, respectively, was microinjected into fertilized mouse ovocytes. In the six transgenic lines studied, expression was strictly specific to the mammary gland of lactating animals and was position-independent. Levels of exogenous porcine wap mRNA per copy compared favorably with the porcine wap mRNA yield in the mammary gland of a 9-day lactating pig. These findings suggest that this insert contained most if not all of the cis-acting elements involved in the full specific expression of the porcine wap gene. These elements constitute good candidates for directing the optimized expression of protein recombinant-encoding genes in the mammary gland of lactating animals.     

Genome Sequence of the Antarctic Psychrophile Bacterium Planococcus antarcticus DSM 14505

Planococcus antarcticus DSM 14505 is a psychrophile bacterium that was isolated from cyanobacterial mat samples, originally collected from ponds in McMurdo, Antarctica. This orange-pigmented bacterium grows at 4°C and may possess interesting enzymatic activities at low temperatures. Here we report the first genomic sequence of P. antarcticus DSM 14505.     

Transcription profiling of acute temperature stress in the Antarctic plunderfish Harpagifer antarcticus

Harpagifer antarcticus (the Antarctic plunderfish), a shallow-water benthic fish distributed around the Antarctic Peninsula, is a member of the notothenioid family, one of whose adaptations to the cold waters of Antarctica has been the loss of the classic heat shock response. In order to gain a more comprehensive understanding of the effects of temperature stress on H. antarcticus, we constructed a liver cDNA library and a 10,371 feature microarray. This was hybridized with material from a time course series of animals held at 6°C for 48h. The resulting expression profiles show that this fish displays the classical vertebrate acute inflammatory response. There was also a pronounced signal for increased energy requirements via up-regulation of genes involved in the β oxidation of fatty acids and also a strong signature of response to oxidative stress. Genes in the latter category did not include the "classic" antioxidants such as glutathione S-transferase, but genes involved in the production of reducing potential in the form of NADPH, peroxisome proliferation via peroxisomal acyl co-enzyme A oxidase 1 and genes known to be up-regulated by hypoxia-inducible factor 1 (HIF1). These identifications provide clear support for oxygen being the whole animal limiting factor at least in acute short-term temperature challenges. The classical heat shock proteins were not up-regulated during this trial, although numerous clones for each were present on the gene chip, confirming the lack of this response in this species. These data significantly increase our knowledge of the cellular stress response from animals in this unique environment.     

shape Ogmogaster antarcticus Johnston, 1931 (Digenea: Notocotylidae) in shape Balaenoptera physalus (L.): first record in the Mediterranean Sea

Detailed parasitological investigations were carried out on the stomach and the intestine of a young male Balaenoptera physalus found stranded along the east coast of the northern Tyrrhenian Sea. Thousands of digeneans were found in both the caecum and the colon. Morphological and morphometric studies were carried out on these parasites, which were identified as Ogmogaster antarcticus Johnston, 1931. In contrast to the other species of the genus, O. antarcticus has a large geographical distribution and it is not specific to its definitive hosts. This is the first record of O. antarcticus from B. physalus in the Mediterranean Sea, a finding which helps confirm the world-wide distribution of this parasite.     

Rapid metabolic adaptation in European sea bass (Dicentrarchus labrax) juveniles fed different carbohydrate sources after heat shock stress

A study was conducted to evaluate the effect of two dietary carbohydrate sources (waxy maize starch and glucose) on the metabolic adaptation of sea bass juveniles (initial weight: 24 g) to a heat shock treatment (temperature rise from 18 degrees C to 25 degrees C within 24 h). Two isonitrogenous and isolipidic diets were formulated to contain 20% waxy maize starch (WS diet) or 20% glucose (GLU diet). Triplicate groups of fish were fed to near satiation for 4 weeks at both temperatures (18 degrees C and 25 degrees C). Then, fish previously maintained at 18 degrees C were submitted to a heat shock (18 degrees C to 25 degrees C) and continued to be fed with the same diets during 1 more week. The higher water temperature significantly improved growth performance, feed efficiency, as well as protein efficiency ratio, independently of diet. At 25 degrees C, but not at 18 degrees C, growth of fish fed the WS diet was higher than that of fish fed the GLU diet. Plasma glucose levels were higher in sea bass fed the GLU diet and not influenced by water temperature. Fish fed a glucose diet or reared at high temperatures (25 degrees C) showed enhanced liver glycolytic, lipogenic and gluconeogenic capacities compared to fish fed a starch diet or reared at low temperatures (18 degrees C). For the majority of the enzymes studied, 1 week seemed to be enough time for metabolic adaptation in sea bass submitted to an acute heat shock. Irrespective of carbohydrate source, HSP70 gene expression was similar in both cold water (18 degrees C) and warm water (25 degrees C) acclimated sea bass. A weak down regulation was observed after heat shock only in fish fed the GLU diet. This suggests that HSP70 gene expression is not affected by the rearing temperature per se.     

Moulting reduces freeze susceptibility in the Antarctic mite Alaskozetes antarcticus (Michael)

Abstract.  The effect of moulting on the cold hardiness of the oribatid mite Alaskozetes antarcticus (Michael) is investigated. Non moulting animals show clear seasonal patterns of cold hardiness with high supercooling points (SCPs) at the peak of summer and an increasing proportion of low SCPs with declining environmental temperatures. By contrast, both field-fresh and laboratory acclimated (5 °C) mites in the moult state are consistently found to have low SCPs regardless of environmental temperature.     

Reconsideration of the longiceps species group of the feather louse genus Columbicola (Phthiraptera: Philopteridae) with descriptions of two new species

We reconsidered the composition of the longiceps species group within Columbicola. Based primarily on head shape, the group is divided into the longiceps and the cavifrons groups, with 7 species in the former and 5 in the latter. Two new species are described: Columbicola claytoni (type host: Ducula rufigaster [Quoy and Gaimard]) and Columbicola malenkeae (type host: D. pacifica [J. E. Gmelin]). Columbicola wolffhuegeli (Eichler) is removed from synonymy with Columbicola longiceps (Rudow) and is recognized as a valid species. The true host for Columbicola paradoxus Tendeiro has been determined as Lopholaimus antarcticus (Shaw).     

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.     

Survival of sub-zero temperatures by two South Georgian beetles (Coleoptera,Perimylopidae)

Summary The ability of adults and larvae of two species of perimylopid beetles (Hydromedion sparsutum, Perimylops antarcticus) to survive sub-zero temperatures was studied at Husvik, South Georgia in summer during October–December 1990. Experiments determined their survival at constant sub-zero temperatures, their lower lethal temperatures and individual supercooling points. The effects of cooling rates (0.015°, 0.5° and 2.0°C min^–1) and starvation on survival were also assessed. Mean supercooling points of field-collected individuals of both species were in the range -3.0° to -5.4°C with Perimylops having a deeper capacity (ca. 1.5°C) for supercooling relative to Hydromedion. The former species also survived freezing temperatures significantly better than the latter and its mean lower lethal temperature was 2.5°C lower. At a constant temperature of -8.5°C, the median survival times for Perimylops adults and larvae were 19 and 26 h respectively, whilst both stages of Hydromedion died within 3 h. The three cooling rates resulted in significantly different median survival temperatures for adult Hydromedion with 0.5°C min^–1 producing maximum survival. Prior starvation did not have a significant influence on the survival of either species at sub-zero temperatures although both adults survived less well. The results support field observations on the habitats and distribution of these insects, and suggest differing degrees of freezing tolerance.     

Contrasting phylogeographical patterns for springtails reflect different evolutionary histories between the Antarctic Peninsula and continental Antarctica

Aim  We examined the genetic structure among populations and regions for the springtails Cryptopygus antarcticus antarcticus and Gomphiocephalus hodgsoni (Collembola) to identify potential historical refugia and subsequent colonization routes, and to examine population growth/expansion and relative ages of population divergence.
Location  Antarctic Peninsula for C. a. antarcticus ; Antarctic continent (southern Victoria Land) for G. hodgsoni .
Methods  Samples were collected from 24 and 28 locations across the Antarctic Peninsula and southern Victoria Land regions for C. a. antarcticus and G. hodgsoni , respectively. We used population genetic, demographic and nested clade analyses based on mitochondrial DNA (cytochrome c oxidase subunit I and subunit II).
Results  Both species were found to have population structures compatible with the presence of historical glacial refugia on Pleistocene (2 Ma–present) time-scales, followed by post-glacial expansion generating contemporary geographically isolated populations. However, G. hodgsoni populations were characterized by a fragmented pattern with several 'phylogroups' (likely ancestral haplotypes present in high frequency) retaining strong ancestral linkages among present-day populations. Conversely, C. a. antarcticus had an excess of rare haplotypes with a much reduced volume of ancestral lineages, possibly indicating historical founder/bottleneck events and widespread expansion.
Main conclusions  We infer that these differences reflect distinct evolutionary histories in each locality despite the resident species having similar life-history characteristics. We suggest that this has predominantly been influenced by variation in the success of colonization events as a result of intrinsic historical glaciological differences between the Antarctic Peninsula and continental Antarctic environments.     

Seasonal change in a pollinator community and the maintenance of style length variation in Mertensia fusiformis (Boraginaceae)

Background and Aims

In sub-alpine habitats, patchiness in snowpack produces marked, small-scale variation in flowering phenology. Plants in early- and late-melting patches are therefore likely to experience very different conditions during their flowering periods. Mertensia fusiformis is an early-flowering perennial that varies conspicuously in style length within and among populations. The hypothesis that style length represents an adaptation to local flowering time was tested. Specifically, it was hypothesized that lower air temperatures and higher frost risk would favour short-styled plants (with stigmas more shielded by corollas) in early-flowering patches, but that the pollen-collecting behaviour of flower visitors in late-flowering patches would favour long-styled plants.

Methods

Floral morphology was measured, temperatures were monitored and pollinators were observed in several matched pairs of early and late populations. To evaluate effects of cold temperatures on plants of different style lengths, experimental pollinations were conducted during mornings (warm) and evenings (cool), and on flowers that either had or had not experienced a prior frost. The effectiveness of different pollinators was quantified as seed set following single visits to plants with relatively short or long styles.

Key Results

Late-flowering populations experienced warmer temperatures than early-flowering populations and a different suite of pollinators. Nectar-foraging bumble-bee queens and male solitary bees predominated in early populations, whereas pollen-collecting female solitary bees were more numerous in later sites. Pollinators differed significantly in their abilities to transfer pollen to stigmas at different heights, in accordance with our prediction. However, temperature and frost sensitivity did not differ between long- and short-styled plants. Although plants in late-flowering patches tended to have longer styles than those in early patches, this difference was not consistent.

Conclusions

Seasonal change in pollinator-mediated selection on style length may help maintain variation in this trait in M. fusiformis, but adaptation to local flowering time is not apparent. The prevalence of short styles in these populations requires further explanation.     

Coping with temperature at the warm edge--patterns of thermal adaptation in the microbial eukaryote Paramecium caudatum

Background

Ectothermic organisms are thought to be severely affected by global warming since their physiological performance is directly dependent on temperature. Latitudinal and temporal variations in mean temperatures force ectotherms to adapt to these complex environmental conditions. Studies investigating current patterns of thermal adaptation among populations of different latitudes allow a prediction of the potential impact of prospective increases in environmental temperatures on their fitness.

Methodology/Principal Findings

In this study, temperature reaction norms were ascertained among 18 genetically defined, natural clones of the microbial eukaryote Paramecium caudatum. These different clones have been isolated from 12 freshwater habitats along a latitudinal transect in Europe and from 3 tropical habitats (Indonesia). The sensitivity to increasing temperatures was estimated through the analysis of clone specific thermal tolerances and by relating those to current and predicted temperature data of their natural habitats.All investigated European clones seem to be thermal generalists with a broad thermal tolerance and similar optimum temperatures. The weak or missing co-variation of thermal tolerance with latitude does not imply local adaptation to thermal gradients; it rather suggests adaptive phenotypic plasticity among the whole European subpopulation. The tested Indonesian clones appear to be locally adapted to the less variable, tropical temperature regime and show higher tolerance limits, but lower tolerance breadths.

Conclusions/Significance

Due to the lack of local temperature adaptation within the European subpopulation, P. caudatum genotypes at the most southern edge of their geographic range seem to suffer from the predicted increase in magnitude and frequency of summer heat waves caused by climate change.     

Paeonocanthus antarcticensis (Hewitt, 1965): a rare copepod parasite of bathypelagic fish, Bathylagus antarcticus Günther, from the Antarctic Ocean

Paeonocanthus antarcticensis (Hewitt, 1965) is redescribed based on four specimens recovered from a deep-sea smelt, Bathylagus antarcticus Günther, collected in the Antarctic Ocean (65 degrees S, 139 degrees 59.6'E). Studies on the morphological variations of these four specimens plus comparison with the three documented specimens yielded that the sphyriid reported as P. antarcticensis from the goiter blacksmelt, Bathylagus euryops Goode & Bean, taken in the Northwest Atlantic Ocean is a different species. It is renamed Paeonocanthus hogansi n. sp.