Supercool or dehydrate? An experimental analysis of overwintering strategies in small permeable arctic invertebrates (original) (raw)
Related papers
Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology, 1999
In this paper we present the results of physiological responses to winter acclimation and tissue freezing in a freeze-tolerant Siberian earthworm, Eisenia nordenskioeldi, and two freeze-intolerant, temperate earthworm species, Lumbricus rubellus and Aporrectodea caliginosa. By analysing the physiological responses to freezing of both types we sought to identify some key factors promoting freeze tolerance in earthworms. Winter acclimation was followed by a signi®cant increase in osmolality of body¯uids in E. nordenskioeldi, from 197 mosmol kg A1 in 10°C-acclimated animals to 365 mosmol kg A1 in animals acclimated to 0°C. Cold acclimation did not cause any change in body¯uid osmolality in the two freeze-intolerant species. As a response to ice formation in the body, the freeze-intolerant species produced copious amounts of slime and expulsion of coelomic¯uids, and thereby lost 10±30% of their total water content. Contrary to this, the freeze-tolerant species did not lose water upon freezing. At temperatures down to A6.5°C, the ice content in the freezetolerant E. nordenskioeldi was signi®cantly lower than in L. rubellus. At lower temperatures there were no dierences in ice content between the two species. Cold acclimated, but unfrozen, specimens of all three species had low levels of ammonia, urea, lactate, glycerol and glucose. As a response to ice formation, glucose levels signi®cantly increased within the ®rst 24 h of freezing. This was most pronounced in E. nordenskioeldi where a 153-fold increase of glucose was seen (94 mmol á l A1 ). In L. rubellus and A. caliginosa a 19-fold and 17-fold in-crease in glucose was seen. This is the ®rst study on physiological mechanisms promoting freeze tolerance in E. nordenskioeldi, or any other oligochaete. Our results suggest that the cryoprotective system of this species more closely resembles that of freeze-tolerant anurans, which synthesize cryoprotectants only after tissues begin to freeze, than that of cold-hardy invertebrates which exhibit a preparatory accumulation of cryoprotectants during seasonal exposure to low temperature.
Dehydration of earthworm cocoons exposed to cold: a novel cold hardiness mechanism
Journal of Comparative Physiology B, 1994
Mechanisms involved in cold hardiness of cocoons of the lumbricid earthworm Dendrobaena octaedra were elucidated by osmometric and calorimetric studies of water relations in cocoons exposed to subzero temperatures. Fully hydrated cocoons contained ca. 3 g water.g dry weight-l; about 15% of this water (0.5 g.g dry weight -1) was osmotically inactive or "bound". The melting point of the cocoon fluids in fully hydrated cocoons was -0.20~ Exposure to frozen surroundings initially resulted in supercooling of the cocoon fluids, but over a period of 1-2 weeks the cocoons dehydrated (as a result of the vapour pressure difference at a given temperature between supercooled water and ice) to an extent where the vapour pressure of water in the body fluids was in equilibrium with the surrounding ice. This resulted in a profound dehydration of the cocoons, even at mild freezing exposures, and a concomitant slight reduction in the amount of osmotically inactive water. At temperatures around -8~ which cocoons readily survive, almost all (> 97%) osmotically active water had been withdrawn from the cocoons. It is suggested that cold injuries in D. octaedra cocoons observed at still lower temperatures may be related to the degree of dehydration, and possibly to the loss of all osmotically active water. The study indicates that ice formation in the tissues is prevented by equilibrating the body fluid melting point with the exposure temperature. This winter survival mechanism does not conform with the freeze tolerance/freeze avoidance classification generally applied to cold-hardy poikilotherms. Implications of this cold hardiness mechanism for other semi-terrestrial invertebrates are discussed.
Freeze tolerance in an arctic Alaska stonefly
Journal of Experimental Biology, 2008
SUMMARY Most aquatic insects do not survive subzero temperatures and, for those that do, the physiology has not been well characterized. Nemoura arctica is a species of stonefly widely distributed throughout arctic and subarctic Alaska. We collected nymphs from the headwaters of the Chandalar River, where we recorded streambed temperatures as low as –12.7°C in midwinter. When in contact with ice, autumn-collected N. arctica cool to –1.5±0.4°C before freezing, but individuals survived temperatures as low as –15°C, making this the first described species of freeze-tolerant stonefly. N. arctica clearly survive freezing in nature, as winter-collected nymphs encased in ice demonstrated high survivorship when thawed. In the laboratory, 87% of N. arcticanymphs frozen to –15°C for 2.5 weeks survived and, within one month of thawing, 95% of the last-instar nymphs emerged. N. arctica produce both glycerol and ice-binding factors (e.g. antifreeze protein) in response to low temperature. Hemoly...
Insect Cold-Hardiness: Insights from the Arctic
ARCTIC, 1994
Cold-hardiness and related adaptations of insects in the Arctic correspond to characteristic climatic constraints. Some species are long-lived and are cold-hardy in several stages. In the Arctic, diapause and cold-hardiness are less likely to be linked than in temperate regions, because life-cycle timing depends as much on the need to coincide development with the short summer as on the need to resist winter cold. Winter habitats of many species are exposed rather than sheltered from cold so that development in spring can start earlier. Several features of cold-hardiness in arctic species differ from the characteristics of temperate species: these include very cold-hardy insects with low supercooling points that are not freezing tolerant; freezing-tolerant species that supercool considerably rather than freezing at relatively high subfreezing temperatures; mitochondrial degradation linked with the accumulation of cryoprotectants; and the possibly limited occurrence of thermal hysteresis proteins in winter. Several interesting relationships between cold-hardiness and water have been observed, including different types of dehydration. Winter mortality in arctic insects appears to be relatively low. Adaptations to cold in summer include retention of cold-hardiness, even freezing tolerance; selection of warm sites; and behaviour such as basking that allows elevated body temperatures. Studies especially on the high-arctic moth Gynaephora groenlandica show that various factors including cold-hardiness and other summer and winter constraints dictate the structure of energy budgets and the timing of life cycles.
Survival of rapidly fluctuating natural low winter temperatures by High Arctic soil invertebrates
Journal of Thermal Biology, 2014
The extreme polar environment creates challenges for the resident invertebrate communities and the stress tolerance of some of these animals has been examined over many years. However, although it is well appreciated that standard air temperature records often fail to describe accurately conditions experienced at microhabitat level, few studies have explicitly set out to link field conditions experienced by natural multispecies communities with the more detailed laboratory ecophysiological studies of a small number of 'representative' species. This is particularly the case during winter, when snow cover may insulate terrestrial habitats from 3 extreme air temperature fluctuations. Further, climate projections suggest large changes in precipitation will occur in the polar regions, with the greatest changes expected during the winter period and, hence, implications for the insulation of overwintering microhabitats. To assess survival of natural High Arctic soil invertebrate communities contained in soil and vegetation cores to natural winter temperature variations, the overwintering temperatures they experienced were manipulated by deploying cores in locations with varying snow accumulation: No Snow, Shallow Snow (30cm) and Deep Snow (120cm). Air temperatures during the winter period fluctuated frequently between +3 and-24°C, and the No Snow soil temperatures reflected this variation closely, with the extreme minimum being slightly lower. Under 30cm of snow, soil temperatures varied less and did not decrease below-12°C. Those under deep snow were even more stable and did not decline below-2°C. Despite these striking differences in winter thermal regimes, there were no clear differences in survival of the invertebrate fauna between treatments, including oribatid, prostigmatid and mesostigmatid mites, Araneae, Collembola, Nematocera larvae or Coleoptera. This indicates widespread tolerance, previously undocumented for the Araneae, Nematocera or Coleoptera, of both direct exposure to at least-24°C and the rapid and large temperature fluctuations. These results suggest that the studied polar soil invertebrate community may be robust to at least one important predicted consequence of projected climate change.
Climatic variability and the evolution of insect freeze tolerance
Biological Reviews of the Cambridge Philosophical Society, 2003
Insects may survive subzero temperatures by two general strategies : Freeze-tolerant insects withstand the formation of internal ice, while freeze-avoiding insects die upon freezing. While it is widely recognized that these represent alternative strategies to survive low temperatures, and mechanistic understanding of the physical and molecular process of cold tolerance are becoming well elucidated, the reasons why one strategy or the other is adopted remain unclear. Freeze avoidance is clearly basal within the arthropod lineages, and it seems that freeze tolerance has evolved convergently at least six times among the insects (in the Blattaria, Orthoptera, Coleoptera, Hymenoptera, Diptera and Lepidoptera). Of the pterygote insect species whose cold-tolerance strategy has been reported in the literature, 29 % (69 of 241 species studied) of those in the Northern Hemisphere, whereas 85 % (11 of 13 species) in the Southern Hemisphere exhibit freeze tolerance. A randomization test indicates that this predominance of freeze tolerance in the Southern Hemisphere is too great to be due to chance, and there is no evidence of a recent publication bias in favour of new reports of freeze-tolerant species. We conclude from this that the specific nature of cold insect habitats in the Southern Hemisphere, which are characterized by oceanic influence and climate variability must lead to strong selection in favour of freeze tolerance in this hemisphere. We envisage two main scenarios where it would prove advantageous for insects to be freeze tolerant. In the first, characteristic of cold continental habitats of the Northern Hemisphere, freeze tolerance allows insects to survive very low temperatures for long periods of time, and to avoid desiccation. These responses tend to be strongly seasonal, and insects in these habitats are only freeze tolerant for the overwintering period. By contrast, in mild and unpredictable environments, characteristic of habitats influenced by the Southern Ocean, freeze tolerance allows insects which habitually have ice nucleators in their guts to survive summer cold snaps, and to take advantage of mild winter periods without the need for extensive seasonal cold hardening. Thus, we conclude that the climates of the two hemispheres have led to the parallel evolution of freeze tolerance for very different reasons, and that this hemispheric difference is symptomatic of many wide-scale disparities in Northern and Southern ecological processes.
Journal of Insect Physiology, 1989
The metabolic responses to repeated cycles of temperature change, alternating 24 h at -16 and +3"C, wer': compared for a freeze-tolerant (Eurosta soliduginis) vs a freeze-avoiding (Epiblema scudderiuna) insect. The two species differed most strongly in the response by cellular energetics. ATP content and energy charge were depressed in E. scudderiana larvae with each -16°C exposure but rebounded with each return to + 3°C; after 12 such cycles, final energy status at + 3°C was not significantly different than cc'ntrol values. By contrast, E. soliduginis larvae maintained a high energy charge (at the expense of a decrease in the total adenylate pool) over the first two cycles of freeze/thaw only. Subsequently energy stress was cumulative, with no recovery in the +3"C half of each cycle, and energy charge fell to 0.70-0.75.