Journal of Insect Physiology 46 2000 1387–1396 www.elsevier.comlocatejinsphys
Seasonal changes in tolerance to cold and desiccation in Phauloppia sp. Acari, Oribatida from Finse, Norway
Heidi Sjursen , Lauritz Sømme
University of Oslo, Department of Biology, P.O. Box 1050 Blindern, N-0316, Oslo, Norway Received 17 November 1999; accepted 2 March 2000
Abstract
In the alpine region at Finse, Norway, Phauloppia spp. Acari, Oribatida inhabit lichens on top of boulders. Adult mites are about 0.5 mm in length and have a mean weight of ca. 15
µ g. Temperatures in the lichens may drop below 235
° C in winter and
increase to 55 °
C in the summer. Large seasonal variations were recorded in supercooling points and body fluid osmolality. Mean January values of SCPs and osmolality were 235.3
° C and 3756 mOsm, while July values were 29.4
° C and 940 mOsm, respectively.
Thermal hysteresis proteins were present in both summer and winter acclimated mites. In mid-winter, some of the mites survived more than 49 days in a water vapor saturated atmosphere at 219
° C, and more than 42 days enclosed in ice at the same temperature.
The mites showed high tolerance to desiccation. Specimens collected in October survived up to 23 days at 22 °
C and 5 RH. The tolerance to desiccation was lower in specimens collected during the winter. Some mites survived the loss of up to 90 of
their total water content and were reactivated when given access to water. Length measurements of individual Phauloppia sp. showed that both male and female mites are clearly divided in two size groups, suggesting that they belong to two closely related
species or different populations.
2000 Elsevier Science Ltd. All rights reserved.
Keywords: Oribatid mites; Phauloppia-sp.; Cold hardiness; Resistance to desiccation
1. Introduction
1.1. Cold hardiness Terrestrial arthropods are widely distributed in tem-
perate and polar regions, and overwinter in many differ- ent habitats. Some species overwinter in the ground, pro-
tected from extreme conditions by plant litter and snow cover; others are exposed to low temperatures under bark
or on branches of trees, or in moss and lichen on wind- swept mountain ridges. Several groups of arthropods
have successfully adapted to survive exposure to subzero temperatures. Both behavioral and physiological adap-
tations are required for successful overwintering. Funda- mental physiological differences lie in whether or not
the organism can survive freezing e.g. Salt, 1961;
Corresponding author. Present address: National Environmental Research Institute, Vejlsøvej 25, P.O. Box 314, DK-8600 Silkeborg,
Denmark. Tel.: +
45-8920-1400; fax: +
45-8920-1413. E-mail address: hesdmu.dk H. Sjursen.
0022-191000 - see front matter
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Sømme, 1981; Zachariassen, 1985; Cannon and Block, 1988.
The ecology and physiology of oribatid mites Acari, Oribatida have been studied in different environments,
but systematics have been the main topic of most studies Grandjean, 1953; Trave´, 1961; Krantz, 1978; Norton
and Behan-Pelletier, 1986; Behan-Pelletier, 1991. Earl- ier studies on overwintering strategies in oribatid mites
have shown that they are freeze susceptible e.g. Sømme and Conradi-Larsen, 1977; Cannon and Block, 1988;
Webb and Block, 1993. Low supercooling points SCPs, high concentrations of low-molecular weight
substances in the haemolymph, the absence of ice nucle- ating agents INAs and the presence of antifreeze pro-
teins are the most important characteristics seen in freeze susceptible terrestrial arthropods.
Mean SCPs for most species of oribatid mites tested to date lie between 220 and 230
° C in winter-acclimated
individuals Schatz and Sømme, 1981; Block, 1982, and somewhat higher in summer-acclimated individuals
Sømme, 1981, although populations from Antarctica may maintain their ability to supercool to temperatures
1388 H. Sjursen, L. Sømme Journal of Insect Physiology 46 2000 1387–1396
well below 220 °
C even during the summer Block and Sømme, 1982; Shimada et al., 1992; Sømme et al., 1993;
Sugawara et al., 1995. A common feature of oribatid SCP distributions is that they show a marked bimodality;
often called high and low groups Cannon and Block, 1988.
Low molecular weight solutes such as glycerol depress the supercooling point of a solution about twice
as much as they depress the melting point Zachariassen, 1985; Cannon and Block, 1988. In addition, the solutes
have other important cryoprotective functions, e.g. stabi- lizing proteins and enzymes against denaturation,
inhibiting lipid phase transitions, increasing the pro- portion of unfreezable water, and protection against cold
shock Duman and Horwath, 1983; Baust, 1983; Storey, 1984; Lee et al., 1986. Thermal hysteresis proteins
THPs lower the freezing point of the haemolymph by a noncolligative mechanism but do not affect the melting
point, thus producing a difference between melting point and freezing point termed thermal hysteresis. THPs are
found in the haemolymph of overwintering terrestrial arthropods Zachariassen, 1985; Duman et al., 1991,
and have been shown to prevent inoculative freezing in beetles Gehrken, 1992; Olsen et al., 1998.
Probably because of their small size, few studies have been carried out on thermal hysteresis and osmolality in
mites. Thermal hysteresis has been described in both the nymphs and adults of the Antarctic oribatid mite Alasko-
zetes antarcticus Block and Duman, 1989. Haemo- lymph osmolality in Maudheimia wilsoni from Dronning
Maud Land, Antarctica ranges from 500 to 800 mOsm and thermal hysteresis freezing points from 24.7 to
26.1
° C. Sømme et al., 1993.
Time aspect is an important factor in insect cold hardi- ness. Overwintering species have to survive long periods
at subzero temperatures but may be injured or killed at temperatures well above their SCP Sømme, 1996. Very
few studies have examined long term exposure to freez- ing temperatures in microarthropods. As an example,
more than 85 of winter acclimated Alaskozetes antarc- ticus survived exposures up to 100 days at 210 and
215
° C Cannon, 1987, and Marshall 1996 maintained
specimens of Maudheimia petronia at 215 °
C for six months. In Amblyomma americanum Acari: Ixodidae,
however, unfed immatures as well as fed and unfed adults showed high mortality after exposure to 210
° C
for 12 days Needham et al., 1996. 1.2. Desiccation resistance
The rate at which water is lost in an arthropod depends on the chemical potential, the total mass of water in the
body fluids and the permeability of the outer protecting layers of the body Wharton, 1985. Ring and Danks
1994 linked resistance to desiccation with cold hardi- ness, suggesting that physiological adaptations to dry
and cold environments overlap in several ways. Dehy- dration results in an increase in concentration of cryopro-
tectants, which will depress supercooling points in freeze susceptible organisms Zachariassen, 1985.
Some oribatid mites survive longer at low tempera- tures 0–4
° C than at high temperatures, probably due to
lower desiccation stress Cannon and Block, 1988. In the maritime Antarctic, Alaskozetes antarcticus shows
little seasonal variation in water content, with values between 65 and 75 of fresh weight Block, 1981. In
this species the rate of water loss is less than 0.5 of fresh weight h
21
at 0 °
C and 5 RH Worland and Block, 1986, while Halozetes belgicae lost 0.7 of
fresh weight h
21
under similar conditions. In the sub- Antarctic mites Podacarus auberti and Halozetes fulvus,
water loss rates at 15 °
C and 5 RH were 0.60 and 0.65 of fresh weight h
21
, respectively Marshall, 1996.
In Dronning Maud Land, Continental Antarctica, Maudheimia petronia lives on nunataks in a habitat prac-
tically devoid of free water, except during thawing in the summer Marshall, 1996. At 15
° C and 5 RH the
mean rate of water loss in this species during the first 45 h of desiccation was 0.42 of body water h
21
. This value is close to a rate of 0.44 of body water h
21
at 15
° C and 10 RH in M. wilsoni Sømme et al., 1993.
1.3. Purpose of the present study In the alpine zone at Finse, Norway, the oribatid mites
Phauloppia spp.
family Oribatulidae
experience extreme climatic conditions. The mites inhabit lichens
on top of large boulders, and are exposed to freezing temperatures and desiccation stress in winter, as well as
desiccation stress during the summer. The purpose of the present study was to determine changes in supercooling
points, osmolality, water content and water loss, and in survival during prolonged exposure to cold in these spec-
ies, as a function of season and temperature.
2. Material and methods
