|
| |
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
First published online January 31, 2007
Journal of Experimental Biology 210, 593-601 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.02691
Plasticity and superplasticity in the acclimation potential of the Antarctic mite Halozetes belgicae (Michael)
1 Department of Biosciences, University of Birmingham, Edgbaston, Birmingham
B15 2TT, UK
2 British Antarctic Survey, Natural Environment Research Council, High
Cross, Madingley Road, Cambridge CB3 OET, UK
* Author for correspondence (e-mail: tinstone12{at}hotmail.com)
Accepted 12 December 2006
 |
Summary |
|---|
 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Key words: phenotypic plasticity, rapid cold hardening, maritime Antarctic, Halozetes belgicae, acclimation
|
Introduction |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
). In variable environments, plasticity in
biological traits may have considerable adaptive value, optimising fitness
over widely ranging conditions. At high latitudes temperature is one of the
primary environmental variables and adaptation to low temperatures – in
particular, acclimation potential – is one of the primary derived
features of terrestrial arthropods. This study examines the relationship
between plasticity and acclimation potential in a common, but largely
unexamined, species of maritime Antarctic mite.
Plasticity in the cold tolerance of polar terrestrial arthropods is
expressed as the change from a non-cold-hardy to a cold-hardy phenotype. In
the mites (Acari) and springtails (Collembola) that dominate the Antarctic
terrestrial fauna, this switch is well known and described at seasonal
temporal scales. Accomplished primarily by the management of supercooling
capacity, it involves the evacuation of gut contents, accumulation of
colligative antifreezes and concentration of body fluids with the onset of
winter (Cannon and Block,
1988). In this sense, these animals all demonstrate a kind of
bimodal plasticity moving physiologically between the two states with
predictable seasonal thermal variation.
However, although these phenotypic changes are fixed components of their low temperature adaptation, to what extent do polar arthropods demonstrate plasticity at other scales of thermal variability? In other words, at what level of spatial or temporal resolution has plasticity been incorporated into their acclimation and acclimatisation responses?
Evidence accrued to date from a variety of polar contexts suggests that
there is no common level of `incorporation' (e.g.
Klok and Chown, 2005;
Worland and Convey, 2001;
Sinclair et al., 2003;
Sinclair and Chown, 2003;
Lee et al., 2006b;
Hawes et al., 2006a). Is this
evidence for species-specific or context-specific variability? The expression
of phenotype is a result of an interaction between genotype and environment
and although some of the documented variance (or lack of it) in plasticity may
be partitioned phylogenetically (e.g. Klok
and Chown, 2003; Klok and
Chown, 2005), there are nonetheless observable correlations
between levels of plasticity and exposure to thermal variability (e.g.
Hawes et al., 2006a). However,
the answer to the species-versus-context question can only be arrived
at accretively by accumulating data on a range of species in a variety of
environmental contexts. Here, we examine a species at one end of the
variability gradient – extreme exposure.
Halozetes belgicae (Michael) is distributed throughout the
sub-Antarctic and maritime Antarctic
(Minto et al., 1991;
Star
and Block, 1998).
Known in Antarctica as the `lichen-mite'
(Bryant, 1945), it is a small
oribatid (adult body length <700 µm) often found in association with the
more common and well-studied oribatid, Alaskozetes antarcticus
(Cannon and Schenker, 1985). On
Signy Island (South Orkney Islands) it is described as being relatively scarce
with a distribution restricted to coastal areas
(Cannon and Schenker, 1985).
Further south, on the Antarctic peninsula, at Marguerite Bay, it can be found
in dense aggregations feeding near gull middens (T.C.H., personal
observation), where it grazes the algal and fungal components of encrusting
lichens. The extension of its geographical range to higher latitudes (and
lower temperatures) is correlated with an expansion in niche from littoral to
terrestrial environments (Marshall and
Convey, 2004) that is associated with increased exposure to
thermal variability. In fact, its preference for gull middens –
characteristically on exposed rock surfaces with elevated aspects –
means that it occupies the most thermally exposed sites of any terrestrial
arthropod in maritime Antarctica. This study tests the hypothesis that the
combined environmental context of low temperatures and greater thermal
variability has led to a high degree of plasticity in the acclimation
potential of this species.
|
Materials and methods |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
).
|
Measurement of cold tolerance
Supercooling points
SCPs were measured using differential scanning calorimetry (DSC)
(Block, 1994). Standard SCP
determinations followed previously published protocols
(Worland and Convey, 2001).
For temperature exposure treatments involving acclimation prior to SCP
determination, warming and cooling was carried out in an alcohol bath (Thermo
Haake Phoenix P2 Circulator; Thermo Haake International, Karlsruhe, Germany)
containing 95% ethanol solution. Animals (N=30) were placed in five
replicate Eppendorf tubes, sat in boiling tubes within the bath, exposed to
the set temperature for the chosen duration, then removed, weighed and placed
directly into the DSC for SCP determination. The cooling and warming rate for
acclimation experiments was 0.5°C min–1. To ensure
animals reached the desired temperature, a digital thermometer with sensor
inserted into an Eppendorf tube, monitored the actual temperature of animals
in the bath. As the experiments were directly aimed at identifying changes in
the shape of SCP distributions, statistical comparisons of SCPs were carried
out using the Kolmogorov–Smirnov test (which makes no assumptions about
the shape of distributions). Common non-parametric statistics (e.g.
Kruskal–Wallis) were employed to compare SCP distributions of the same
shape.
Chill torpor
Torpor temperature of mites was measured by filming animals cooled on a
cold stage. Ethanol (95% solution) was circulated around a metal cold stage
using an alcohol bath (see above) to control temperature and cooling rate.
Mites (N=7–15) were released into a small arena (diameter=5 mm)
with metallic sides and an open bottom with a circle of filter paper sat in
between the cold stage surface and the mites. To maintain relative humidity,
moist filter paper covered the stage surface, but to prevent inoculation at
sub-zero temperatures, the filter paper in the arena was kept dry (the lip on
the open bottom of the arena prevented direct contact with the wet filter
paper). A microscope cold-light was placed over the observation area to
increase visibility. A JVC colour video camera (TK L148B) with macro lens
(MLH, 10x) sat upon a tripod was placed over the arena and used to film
the mites. Images were captured using Studio Capture (Version 1.5.3) software
(www.studio86designs.freeserve.co.uk)
with temperature overlap (simultaneously recording the temperature of a
digital thermometer with thermocouple placed at the base of the cold stage).
Video images were captured at a rate of 2 s frame–1, at a
resolution of 320x240 pixels. Films of cooled animals were saved and
played back to identify individual torpor and recovery temperature for mites
that survived cooling treatments. Torpor was defined as the complete cessation
of movement (occasional twitching was ignored). Recovery temperature was
identified as the temperature at which animals resumed locomotion. Individual
animals were used for statistical analysis of torpor temperature (after
Gibert and Huey, 2001;
Gaston and Chown, 1999). Each
experiment was repeated five times to provide a reliable sample size (not all
animals survived, and a small number of animals had to be used for each
treatment so that aggregational or clumping behaviour did not obscure response
observations). Medians for chill coma and recovery were compared using the
Mann–Whitney tests; mean survival with the t-test.
|
Effect of acclimation and acclimatisation
SCPs were determined for mites acclimated at 5 and 10°C for 1 week on
lichen-encrusted rocks. Season-scale acclimatisation in field-fresh animals
was measured by snapshot sampling of SCPs on 5, 12 and 28 February. For each
snapshot sample the mean weekly temperature (mean temperature of the sample
day and previous 6 days) was calculated from mean hourly temperatures recorded
at the nearby micro-met station on Anchorage Island (British Antarctic Survey,
Biological Sciences Division). Diurnal acclimatisation was measured by daily
sampling (1–3 per day) of mite aggregations maintained outside the
laboratory over 7–11 February.
Effect of endogenous and exogenous factors on SCPs
The SCPs of animals acclimated at each temperature were compared with the
SCPs of starved and externally ice-inoculated mites. Starved animals were
maintained at the acclimation temperature on moistened filter paper without
access to food for 1 week. Inoculated animals were daubed with a layer of
surface moisture using a paintbrush (size=00) immediately prior to SCP
measurements.
|
Acclimation at 0, –5 and –10°C
The effect of non-lethal low temperature exposure on the SCPs of animals
was determined by cooling mites from each acclimation treatment to 0°C and
holding them at this temperature for 2, 4, 6, 8 and 10 h, then determining
their SCPs. This experiment was repeated with animals from both acclimation
temperatures using sub-zero (–5, –10°C) temperatures for the
induction of RCH. To prevent acclimation adjustments, animals were transferred
directly to DSC sample pans after sub-zero temperature acclimation. Survival
at these temperatures was therefore not monitored directly. Median SCPs
therefore include animals that may have frozen during the acclimation process.
As there is a good correspondence between 1st and 2nd SCPs of refrozen
arthropods that are highly chill-tolerant (Hawes, 2007), these may be
identified as SCPs above the acclimation temperature. These SCPs were included
in the calculation of medians for each treatment: as (i) they reflect a
component of the sample not rapidly cold hardening; (ii) their exclusion would
artificially depress the calculated medians; and (iii) their inclusion ensures
that calculations of change are conservative.
Cooling to just below CTmin (–12°C)
To compare the effect of acclimation and RCH on low temperature activity
thresholds, mites were cooled and filmed (as described above) to
–12°C, which a pilot study indicated was just below their critical
thermal minimum (CTmin). Torpor and recovery temperatures
of all individuals that survived were determined by examination of the videos.
Survival of each trial was assessed at the end of each experiment.
|
|
Water contents
Water content was determined gravimetrically. Animals were weighed on a
Mettler-Toledo microbalance (UMXW d=0.1 µg) (Mettler-Toledo Ltd, Leicester,
UK) prior to SCP determination, oven dried for 24 h at 60°C and then
reweighed. Water content was calculated as the percentage difference between
fresh and dry mass. Forty eight samples were examined, representing the range
of SCPs in the experiments, and regression analysis used to identify any
relationship between water content and SCP.
|
|
Results |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
;
Bale, 1996).
|
Effect of acclimation and acclimatisation
The SCP distributions of mites were significantly different
(N=25,21; dmax =0.499; P=0.007) after
acclimation for 1 week at 5 and 10°C
(Fig. 3A).
Fig. 3B shows the changes in
cold hardiness of field-fresh H. belgicae from mid to late summer.
There were highly significant differences between the SCP distributions of
mites sampled on the 5 and 12 February (dmax=0.516;
P=0.002), 5 and 28 February (dmax=0.897;
P<0.001) and 12 and 28 February (dmax=0.662;
P<0.001). Mean (± s.e.m.) weekly temperatures for the week
preceding these snapshot samples were: 3.39±0.27°C for 5 February;
2.60±0.20°C for 12 February; and 2.29±0.17°C for 28
February. [For a complete picture of temperature variation over the summer,
see Hawes et al. (Hawes et al.,
2006b).] Over a 5-day period, when environmental temperatures
ranged between 0 and 5°C, field-fresh mites showed a significant
difference between SCPs (H=28.52; d.f.=10; P=0.001 (adjusted
for ties); Kruskall–Wallis test), but no direct relationship with
temperature (Fig. 3C).
Effects of starvation and ice inoculation
Fig. 4 shows the effect of
starvation and ice inoculation on mites from both acclimation temperatures.
Starvation reduced the SCPs of 10°C acclimated mites significantly
(dmax=0.611; P=0.001), but as untreated mites had
high SCPs, ice inoculation made no significant difference to SCPs. Mites from
the 5°C treatment showed significant increases
(dmax=0.593; P<0.001) and reductions
(dmax=0.442; P=0.021), respectively, in cold
hardiness, as a result of starvation and inoculation.
Rapid cold hardening
Slower cooling rates did not result in significantly different SCPs in
mites from either acclimation temperature
(Fig. 5).
Fig. 6 shows the effect of
rapid cold hardening on mites acclimated at 5°C. Untreated mites already
had low SCPs so little change was detected, except for significantly lower
SCPs in mites acclimated at 0°C for 4 and 8 h
(Table 2). Mites acclimated at
10°C showed evidence of significant rapid cold hardening at all three
induction temperatures (Fig. 7,
Table 2). Indeed, the only
sample that did not show significant changes were the mites acclimated at
–10°C for 6 h, and their change closely approached significance
(N=21, 30; dmax=0.386; P=0.051).
|
|
There was no significant difference in chill coma temperature in untreated and rapidly cold hardened mites from either acclimation temperature (Fig. 8A), nor was there a difference between acclimation temperatures. Rapidly cold hardened mites acclimated at 10°C were found to have significantly lower recovery temperatures than untreated mites (N=19.26; W=577.5; P=0.0013) (Fig. 8B). Survival of the treatment was significantly greater in mites that underwent RCH from both 5 (N=5,4; d.f.=5; T=–2.61; P=0.048) and 10°C (N=6,6; d.f.=9; T=–5.72; P=0.0003; T-test) acclimation treatments (Fig. 8C).
|
Mites cold hardened for 12 h at 0°C and then returned to their acclimation temperatures for 2–12 h showed no significant loss of cold hardiness (Fig. 9).
|
Gut contents
Overall, mites from all treatments had a high proportion of empty guts
(N=75; mean=84.9±1.8%). Even mites acclimated at 10°C with
high SCPs were found to have 61% empty guts. Nonetheless gut contents are
likely to be responsible for the significantly higher SCPs in untreated mites.
The adjusted median SCP of mites acclimated at 10°C (the control for RCH
treatments) was –19.4°C versus an unadjusted median of
–7.6°C. By contrast, for 10°C mites whose SCPs were affected
exogenously by ice inoculation there was little difference between median SCP
(–8.3°C) and adjusted median SCP (–8.9°C).
|
Discussion |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Comparisons with a sub-Antarctic phenotype (Table 3) add support to an adaptive interpretation of this physiological malleability: lower latitude mites demonstrate pre-freeze mortality and less pronounced acclimation potential compared to mites investigated in this study that occupy extremely exposed ecological niches.
|
Although survival at extended low temperature exposure was not examined
here, Cannon and Schenker found 96.4% survival in field-fresh mites collected
in April and held at –15°C for 14 days
(Cannon and Schenker, 1985),
suggesting that maritime Antarctic phenotypes also show little pre-freeze
mortality over extended durations.
Susceptibility to inoculative freezing might be expected to counteract some of the advantages of H. belgicae's plasticity in acclimation potential. However, the exposed and rocky habitats occupied by these mites are dry environments. Summer rain – in recent years a more frequent phenomenon in the maritime Antarctic – occurs only in tandem with warmer temperatures. Although snowfall during summer freeze–thaw cycles and winters offers a real risk of inoculation, contact with ice can be minimised behaviourally; when they are not grazing lichens, H. belgicae utilise the microtopography of the rock surface (grooves, micro-fissures) as a sheltering environment.
To date, the RCH response of polar soil arthropods is unique in its effect
on supercooling capacity. Although there are undoubtedly other mechanisms
involved in rapid cold hardening (e.g. Chen
et al., 1987; Overgaard et
al., 2005; Lee et al.,
2006a) – particularly, in the context of H.
belgicae, with regard to its effects on chill torpor – the
parsimonious explanation for its dramatic effect on the supercooling potential
of H. belgicae is gut-evacuation. By no means does this connote a
lack of sophistication in the cold adaptation of these animals. Gut evacuation
has long been known to play an important part in the management of
supercooling potential in Antarctic terrestrial arthropods (e.g.
Burn, 1981;
Cannon and Block, 1988; Block,
1990). Indeed, these results only emphasise the extent to which this behaviour
has been dynamically incorporated into their low temperature responses and the
extent to which evacuation is an efficient means of ice nucleator
management.
The existence of a `rapid gut emptying response' was first proposed in the
Antarctic collembolan, Cryptopygus antarcticus
(Burn, 1981). Notwithstanding
this, no significant evidence for manipulation of gut contents in this
springtail was found when it was rapidly cold hardened
(Worland and Convey, 2001).
However, that study employed comparisons of faecal pellet production rather
than gut contents, and comparisons using the former may be affected by the
thermal energetics of polar soil arthropods. For example, maximum consumption
rates (measured using faecal pellet production) of C. antarcticus
occur at 5–10°C (Burn,
1984). Indeed, maximum faecal pellet production was found in
springtails acclimated at 5°C rather than at lower temperatures
(Worland and Convey, 2001).
Recent experiments have shown that feeding is certainly involved to some
extent in the reverse phase of the process (short term cold de-acclimation) in
C. antarcticus (Worland et al.,
2007), which might explain why mites in this study that were
returned to their acclimation temperature in the absence of food did not lose
their cold hardiness.
It is not often acknowledged that the sub-lethal experimental temperature
(0°C) employed in laboratory inductions of RCH, for most species that have
been examined (i.e. temperate species), is below or close to their critical
thermal minimum for activity. Although experiments on Antarctic
microarthropods (Worland and Convey,
2001; Lee et al.,
2006b) (this study) and on the `fine-tuning' of RCH in
Drosophila melanogaster (Shreve
et al., 2004) have demonstrated the induction of the response in
animals not in coma; for many documented cases of RCH, it has been induced in
animals effectively under chill coma, i.e. when metabolic activity is
minimal.
In the present study, we found RCH was successfully induced above (0°C,
–5°C), and at or just below (–10°C) the
CTmin of H. belgicae. Results for the latter were
less significant, although not enough to definitively suggest a gradient in
acclimation response. Extensive metabolic regulation (at least in terms of a
system-level response) may not be necessary for improved performance in
rapidly cold hardened insects; for example, at least some of the improvements
can be attributed to responses at the cellular level
(Yi and Lee, 2004).
Nonetheless, one might anticipate a more comprehensive physiological response
above the chill coma temperature when metabolic pathways (e.g. for the
production of desaturase enzymes involved in membrane lipid modification) are
more readily mobilised. In the context of this study, given the apparent
importance of gut-evacuation to H. belgicae's response, it would seem
that the period of time these mites spend above their
CTmin would be particularly important.
In conclusion, H. belgicae would appear to exemplify the notion of adaptive plasticity in cold tolerance. Its seasonally scaled responses are adaptive and, indeed, fundamentally necessary for high latitude life. Its evidence of genotypic plasticity (latitudinal variation) and short-term `superplasticity' are in agreement with environmental gradients in low temperature stress and variability.
|
Acknowledgments |
|---|
|
References |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Bale, J. S. (1993). Classes of insect cold hardiness. Funct. Ecol. 7, 751-753.
Bale, J. S. (1996). Insect cold hardiness: a matter of life and death. Eur. J. Entomol. 93,369 -382.
Block, W. (1994). Differential scanning calorimetry in ecophysiological research. Acta Oecologea 15,13 -22.
Bryant, H. M. (1945). Biology at East Base, Palmer Peninsula, Antarctica. Proc. Am. Philos. Soc. 89,256 -269.
Burn, A. J. (1981). Effects of temperature on the feeding activity of Cryptopygus antarcticus. Comité National Français Des Recherches Antarctiques 51,209 -216.
Burn, A. J. (1984). Energy partitioning in the Antarctic collembolan Cryptopygus antarcticus. Ecol. Entomol. 9,11 -21.
Cannon, R. J. C. and Block, W. (1988). Cold tolerance of microarthropods. Biol. Rev. Camb. Philos. Soc. 63,23 -77.
Cannon, R. J. C. and Schenker, R. (1985). Cold tolerance of a cryptostigmatid mite at Signy Island, Maritime Antarctic. Brit. Antarct. Surv. Bull. 67, 1-5.
Chen, C. P., Denlinger, D. L. and Lee, R. E. (1987). Cold-shock injury and rapid cold hardening in the flesh fly Sarcophaga crassipalpis. Physiol. Zool. 60,297 -304.
Deere, J. A., Sinclair, B. J., Marshall, D. J. and Chown, S. L. (2006). Phenotypic plasticity of thermal tolerances in five oribatid mite species from sub-Antarctic Marion Island. J. Insect Physiol. 52,693 -700.[CrossRef][Medline]
DeWitt, T. J. and Scheiner, S. M. (2004). Phenotypic variation from single phenotypes: a primer. In Phenotypic Plasticity Functional and Conceptual Approaches (ed. T. J. DeWitt and S. M. Scheiner), pp.1 -9. Oxford: Oxford University Press.
Gaston, K. J. and Chown, S. L. (1999). Elevation and climatic tolerance: a test using dung beetles. Oikos 86,584 -590.
Gibert, P. and Huey, R. B. (2001). Chill-coma temperature in Drosophila: effects of developmental temperature, latitude, and phylogeny. Physiol. Biochem. Zool. 74,429 -434.[CrossRef][Medline]
Hawes, T. C. (2006). Re-crystallisation temperature in an Antarctic springtail. CryoLetters In Press.
Hawes, T. C., Couldridge, C. E., Bale, J. S., Worland, M. R. and Convey, P. (2006a). Habitat temperature and the temporal scaling of cold hardening in the High Arctic collembolan, Hypograstrura tullbergi (Schäffer). Ecol. Entomol. 31,450 -459.[CrossRef]
Hawes, T. C., Bale, J. S., Convey, P. and Worland, M. R. (2006b). Ecologically realistic modalities in arthropod supercooling point distributions. Eur. J. Entomol. 103,717 -723.
Klok, C. J. and Chown, S. L. (2003). Resistance to temperature extremes in sub-Antarctic weevils: interspecific variation, population differentiation and acclimation. Biol. J. Linn. Soc. Lond. 78,401 -414.[CrossRef]
Klok, C. J. and Chown, S. L. (2005). Inertia in physiological traits: Embryonopsis halitcella caterpillars (Yponomeutidae) across the Antarctic Polar Frontal Zone. J. Insect Physiol. 51,85 -97.[Medline]
Lee, R. E., Damodaran, K., Yi, S.-X. and Lorigan, G. A. (2006a). Rapid cold hardening increases membrane fluidity and cold tolerance of insect cells. Cryobiology 52,459 -463.[CrossRef][Medline]
Lee, R. E., Elnitsky, M. A., Rinehart, J. P., Hayward, S. A.,
Sandro, L. H. and Denlinger, D. L. (2006b). Rapid
cold-hardening increases the freezing tolerance of the Antarctic midge
Belgica antarctica. J. Exp. Biol.
209,399
-406.
Marshall, D. J. and Convey, P. (2004). Latitudinal variation in habitat specificity of ameronothrid mites (Oribatida). Exp. Appl. Acarol. 34, 21-34.[CrossRef][Medline]
Minto, L. B., Shepherd, G. J. and Usher, M. B. (1991). The cryptostigmatid mite Halozetes belgicae (Michael) in the maritime Antarctic. Antarct. Sci. 3, 53-59.
Overgaard, J., Sorensen, J. G., Petersen, S. O., Loeschecke, V. and Holmstrup, M. (2005). Changes in membrane lipid composition following rapid cold hardening in Drosophila melanogaster.J. Insect Physiol. 51,1173 -1182.[CrossRef][Medline]
Shreve, S. M., Kelty, J. D. and Lee, R. E.
(2004). Preservation of reproductive behaviours during modest
cooling: rapid cold-hardening fine-tunes organismal response. J.
Exp. Biol. 207,1797
-1802.
Sinclair, B. J. and Chown, S. L. (2003). Rapid responses to high temperature and dessication but not to low temperature in the freeze tolerant sub-Antarctic caterpillar Pringleophaga marioni (Lepidoptera, Tineidae). J. Insect Physiol. 49, 45-52.[CrossRef][Medline]
Sinclair, B. J., Klok, C. J., Scott, M. B., Terblanche, J. S. and Chown, S. L. (2003). Diurnal variation in supercooling points of three species of Collembola from Cape Hallet, Antarctica. J. Insect Physiol. 49,1049 -1061.[CrossRef][Medline]
Star, J. and Block, W. (1998).
Distribution and biogeography of oribatid mites (Acari: Oribatida) in
Antarctica, the sub-Antarctic islands and nearby land areas. J.
Nat. Hist. 32,861
-894.
Wallwork, J. A. (1967). Cryptostigmata (Oribatid Mites). Antarct. Res. Ser. 10,105 -122.
Worland, M. R. and Convey, P. (2001). Rapid cold hardening in Antarctic microarthropods. Funct. Ecol. 15,515 -524.[CrossRef]
Worland, M. R., Hawes, T. C. and Bale, J. S. (2007). Temporal resolution of cold acclimation and de-acclimation in the Antarctic collembolan, Cryptopygus antarcticus (Willem). Physiol. Entomol. In Press.
Yi, S.-X. and Lee, R. E. (2004). In vivo and in vitro rapid cold-hardening protects cells from cold shock injury in the flesh fly, Sarcophaga crassipalpis. J. Comp. Physiol. B 174,611 -615.[CrossRef][Medline]
Related articles in JEB:
This article has been cited by other articles:
|
|
 |
|
  T. C. Hawes and J. S. Bale Plasticity in arthropod cryotypes J. Exp. Biol., August 1, 2007; 210(15): 2585 - 2592. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. Blackburn HOW MITES COPE WITH LIFE IN THE FREEZER J. Exp. Biol., February 15, 2007; 210(4): i - ii. [Full Text] [PDF]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
0.05); ***highly significant different
(P
