scholarly journals Hibernation strategies and patterns in sympatric arctic species, the Alaska marmot and the arctic ground squirrel

2015 ◽  
Vol 97 (1) ◽  
pp. 135-144 ◽  
Author(s):  
Trixie N. Lee ◽  
Franziska Kohl ◽  
C. Loren Buck ◽  
Brian M. Barnes

Abstract We compared patterns of core body temperature ( Tb ) change, including inter-individual synchrony, in 2 free-living arctic hibernators that differ in size and sociality, the Alaska marmot ( Marmota broweri ) and the arctic ground squirrel ( Urocitellus parryii ). We report overwinter Tb changes from 3 to 4 marmots from the same hibernaculum in each of 3 years and from 7 ground squirrels that hibernated at 2 nearby burrow sites in 1 year. Very close synchrony in the timing of torpor and arousal cycles in Alaska marmots indicates social hibernation and thermoregulation, while lack of synchrony in arctic ground squirrels further confirms solitary hibernation. The mean duration between the first and last marmot measured within the group to initiate an arousal was 3.7±2.5h and to recool to 30°C during torpor entrance was 5.7±3.7h. The minimum Tb recorded in marmots was 0.6°C and in ground squirrels was −2.0°C. Marmots entering torpor displayed an interrupted pattern of Tb change defined by 2 distinct rates of cooling, early and late during entry, that differed by 21-fold. Ground squirrels cooled in a continuous pattern, initially 3-fold slower than marmots during rapid cooling but 4-fold faster during slow cooling. Both species must minimize energy expenditure to survive long arctic winters; our results suggest that Alaska marmots do this through social thermoregulation, while arctic ground squirrels decrease Tb below freezing to minimize the difference between body and ambient temperatures.

1975 ◽  
Vol 53 (9) ◽  
pp. 1345-1355 ◽  
Author(s):  
Peter Morrison ◽  
William Galster

Cyclic patterns were defined in subspecies of arctic ground squirrels (Citellus undulatus) from the Brooks and Alaskan Ranges. In the annual cycle a heterothermal (hibernation) season with entry, maintenance, and emergence stages was distinguished from a homeothermal (active) season with reproductive, recovery/growth, maintenance, and fattening stages. The heterothermal season consisted of a series of short hibernation cycles in which heterothermal (hibernation) periods with reentry, refractory, and irritable phases were distinguished from homeothermal (active) periods with arousal, maintenance, and preparation phases. Squirrels in which exposure to darkness at 5 °C was delayed (Nov. vs. Sept.) showed a lesser response but emerged synchronously with the normal group. Entry was attenuated with a normal light cycle at 5 °C (8 vs. 3 weeks). Juveniles showed a 2- to 4-week delay in entry as compared to adults.


1974 ◽  
Vol 52 (10) ◽  
pp. 894-902 ◽  
Author(s):  
Hans W. Behrisch

Liver of the hibernating (H) Arctic ground squirrel (Citellus undulatus) contains a single species of pyruvate kinase (PyK) that is distinct from the single isoenzyme of pyK observed in the non-hibernating (NH) ground squirrel, which has been previously described (Behrisch &Johnson (1974) Can. J. Biochem. 52, 547–559). The H-PyK has a pI value of 5.7 and a molecular weight of 241 000 – 243 000. Affinity of the H-PyK for the substrates phosphoenolpyruvate (PEP) and ADP is not affected by changing temperature. It is argued that this stability of the apparent Km's for substrate over a wide temperature range permits the hibernator to take advantage of the Q10 effect in maintaining a low rate of the PyK reaction. Similarly, affinity of H-PyK for the allosteric activator fructose-1,6-phosphate (FDP) and the inhibitor ATP is also conspicuously independent of temperature, suggesting a fine stoichiometry in the relative concentrations of the regulatory ligands in control of H-PyK over a wide temperature range. Further, affinity of H-PyK for the inhibitor ATP is about three- to fourfold lower than that of the NH-PyK, a condition that would favor the maintenance of a high energy charge in the hibernating liver cell. ATP apparently inhibits PyK by causing a dissociation of the enzyme molecule into two "halves" of about 110 000 molecular weight each. This dissociation is offset and reversed by FDP. Removal of the ATP by dialysis does not of itself result in a reassociation of the PyK "halves"; FDP and/or the substrates are required for the two subunits of PyK to reassociate. As the apparent Ki of H-PyK for ATP is higher than that of NH-PyK, substantially higher concentrations of ATP are required to effect the dissociation of H-PyK. Similarly, elevated concentrations of FDP are required to offset the ATP-caused dissociation of the H-PyK.Hibernating Arctic ground squirrels that are preparing to emerge finally from the hibernating state already possess substantial activities of the NH-PyK isoenzyme. This suggests that the animal "anticipates" its transition from one metabolic state from another. On the basis of these data a formal mechanism is proposed for the regulation of liver PyK in the Arctic ground squirrel in both the non-hibernating and hibernating states.


2015 ◽  
Vol 42 (2) ◽  
pp. 176 ◽  
Author(s):  
Jeffery R. Werner ◽  
Charles J. Krebs ◽  
Scott A. Donker ◽  
Rudy Boonstra ◽  
Michael J. Sheriff

Context The arctic ground squirrel (Urocitellus parryii) comprised 17% of the biomass of herbivores in the Yukon boreal forest during the summer months from 1987 to 1996 and was responsible for 23% of the energy flow at the herbivore level. By 2000, ground squirrel populations in this region collapsed to nearly zero and have remained there. Aims We summarise the population monitoring (since 1975) and recent experimental work that has been done on this key herbivore in the Kluane area of the southern Yukon to test one mechanistic hypothesis as the possible explanation for this population collapse and subsequent lack of recovery: predation. Methods Ground squirrels are the preferred summer prey of bird and mammal predators when snowshoe hare (Lepus americanus) populations are declining. We used translocations into formerly occupied habitat and radiotelemetry to determine movements and causes of death from 2009 to 2014. We surveyed 158 sites between 2008 and 2013 to measure the disappearance of colonies in alpine and forest habitats over 25 000 km2. Key results Ground squirrels from 2000 to 2013 comprised a small fraction of the herbivore biomass in the boreal forest zone, down from 17% earlier. Most forest populations (~95%) are currently extinct, whereas just over half (65%) of low-elevation meadow populations are locally extinct. One hypothesis is that ground squirrels in the forest have been driven into a predator pit from which they cannot recover. They remain abundant in alpine tundra (93% occupancy rate) and around airport runways and human habitations (97% occupancy), but there is no apparent dispersal from alpine areas down into the boreal forest. Conclusion The predator pit hypothesis is a likely explanation for the initial collapse and sustained decline in population size from 2000 to 2013. Recent attenuation of the hare cycle and milder winter climate have allowed shrubs to expand throughout the forest, thereby reducing visibility and increasing predation risk. This conclusion will be tested in further research using reintroductions to formerly occupied sites. Implication If the loss of this herbivore from the boreal forest is not reversed, predator pressure on the other major herbivores of the montane forest zone is likely to change significantly.


1975 ◽  
Vol 228 (1) ◽  
pp. 325-330 ◽  
Author(s):  
W Galster ◽  
PR Morrison

The hibernation season in the arctic ground squirrel (Citellus undulatus) is broken into 8- to 18- day cycles by short homeothermal periods during which the carboydrate reserves depleted during hibernation are replenished. This study follows a number of metabolities in tissues and body fluids to assess the sources for reconstitution of the glucose reserves: lactate, urea, ammonia, free fatty acid, glycerol, triglyceride, and glucose in plasma; glycogen in liver and muscle; and urea and ammonia nitrogen in urine. Fat is the major energy source during both homeothermal and heterothermal periods, the contribution from glucose being limited to glycolysis. Reconstitution of glycogen is accomplished prior to reentry through maximal use of substrates from all sources including glycolysis, fat, and protein metabolism. Of the new gluconeogenic substrate, one-fourth is supplied from protein and three-fourths from fat.


1990 ◽  
Vol 68 (4) ◽  
pp. 757-760 ◽  
Author(s):  
Rudy Boonstra ◽  
Charles J. Krebs ◽  
Michelle Kanter

We document the first recorded evidence of predation of collared lemmings (Dicrostonyx kilangmiutak) by arctic ground squirrels (Spermophilus parryii). During an intensive study of lemming populations at Pearce Point, Northwest Territories, using livetrapping and radiotelemetry, we found one and six lemmings predated by arctic ground squirrels in 1987 and 1988, respectively. Predation involved some or all of the following: digging lemmings out of burrows, carrying them to temporary ground squirrel burrows, and partial or complete consumption. The best evidence was obtained during 1988, when a minimum of 4.5% (6/132) of radiotagged lemmings were killed by squirrels.


1976 ◽  
Vol 54 (1) ◽  
pp. 74-78 ◽  
Author(s):  
William Galster ◽  
Peter Morrison

The depletion or accumulation of body reserves is followed in terms of the weight and proportion of lipid, protein, water, and minerals in arctic ground squirrels during the entry, deep, and emergent phases of the hibernation season and after the reproductive phase of the active season. Average weight increased slowly through the summer, from a minimum of 346 g, until mid-August when 190 g accumulated in 3 weeks to be used subsequently during the 220-day hibernation season beginning in mid-September. During hibernation, the 325-g loss in weight represents 62% lipid, 26% water, 9% protein, and 2% mineral. Fat in lipid provides most of the energy but insufficient amounts of carbon for glucose synthesis during hibernation. However, protein provides an adequate gluconeogenic reserve. Significant loss of mineral indicates that skeletal reserves of calcium are important during hibernation. After hibernation, continued loss of weight by females indicates further utilization of reserves during gestation and nursing.


1987 ◽  
Vol 65 (12) ◽  
pp. 3197-3200
Author(s):  
Lawrence K. Duffy ◽  
Margaret M. Ehrhardt ◽  
Michael Romero ◽  
Gregory L. Florant

Hemoglobin β chains were isolated from both the arctic ground squirrel (Citellus parryii undulatus) and the yellow-bellied marmot (Marmota flaviventris). After various enzymatic and chemical cleavages, the primary structures of these β chains were determined. Only one sequence difference was found between the yellow-bellied marmot β chain and that of the European marmot (Marmota marmota). Ground squirrels (C. p. undulatus, Citellus townsendii, and Citellus citellus) showed more species-related differences than the marmots, with the β chain of the arctic ground squirrel differing from that of the townsend ground squirrel by four amino acid substitutions. In the amino terminal region of the β chain, a partial sequence analysis showed that Citellus tridecemlineatus was more similar to C. p. undulatus than to C. townsendii. These biochemical differences could reflect either an increased evolutionary rate of speciation in ground squirrels over that in the genus Marmota or a more recent origin of the species in the genus Marmota. The amino acid differences between these hemoglobins do not appear to be functionally significant in these ecologically similar animals.


1981 ◽  
Vol 59 (5) ◽  
pp. 754-760 ◽  
Author(s):  
Josefine C. Rauch ◽  
Hans W. Behrisch

Tissue concentrations of acetoacetate and β-hydroxybutyrate (ketone bodies) were determined for the blood, liver, caecum, heart, and axillary brown fat, from nonhibernating and hibernating arctic ground squirrels, Spermophilus undulatus, in late spring and during winter, respectively. AcetylCoA and acetoacetylCoA concentrations were measured in the liver, heart, and brown adipose tissue.Except that the concentration of acetylCoA remained unchanged in the liver, all tissues investigated showed elevated concentrations of acetylCoA, acetoacetylCoA, and ketone bodies during the hibernating state. From the increased concentrations of acetoacetate and β-hydroxybutyrate it was deduced that active ketone body metabolism occurs in the hibernating arctic ground squirrel, and that during hibernation, ketone bodies are probably an important source of energy.


2014 ◽  
Vol 80 (18) ◽  
pp. 5611-5622 ◽  
Author(s):  
Timothy J. Stevenson ◽  
Khrystyne N. Duddleston ◽  
C. Loren Buck

ABSTRACTWe examined the seasonal changes of the cecal microbiota of captive arctic ground squirrels (Urocitellus parryii) by measuring microbial diversity and composition, total bacterial density and viability, and short-chain fatty acid concentrations at four sample periods (summer, torpor, interbout arousal, and posthibernation). Abundance ofFirmicuteswas lower, whereas abundances ofBacteroidetes,Verrucomicrobia, andProteobacteriawere higher during torpor and interbout arousal than in summer. Bacterial densities and percentages of live bacteria were significantly higher in summer than during torpor and interbout arousal. Likewise, total short-chain fatty acid concentrations were significantly greater during summer than during torpor and interbout arousal. Concentrations of individual short-chain fatty acids varied across sample periods, with butyrate concentrations higher and acetate concentrations lower during summer than at all other sample periods. Characteristics of the gut community posthibernation were more similar to those during torpor and interbout arousal than to those during summer. However, higher abundances of the generaBacteroidesandAkkermansiaoccurred during posthibernation than during interbout arousal and torpor. Collectively, our results clearly demonstrate that seasonal changes in physiology associated with hibernation and activity affect the gut microbial community in the arctic ground squirrel. Importantly, similarities between the gut microbiota of arctic ground squirrels and thirteen-lined ground squirrels suggest the potential for a core microbiota during hibernation.


2014 ◽  
Vol 10 (11) ◽  
pp. 20140734 ◽  
Author(s):  
Rudy Boonstra ◽  
Kaiguo Mo ◽  
Douglas Ashley Monks

Androgens have benefits, such as promoting muscle growth, but also significant costs, including suppression of immune function. In many species, these trade-offs in androgen action are reflected in regulated androgen production, which is typically highest only in reproductive males. However, all non-reproductive Arctic ground squirrels, irrespective of age and sex, have high levels of androgens prior to hibernating at sub-zero temperatures. Androgens appear to be required to make muscle in summer, which, together with lipid, is then catabolized during overwinter. By contrast, most hibernating mammals catabolize only lipid. We tested the hypothesis that androgen action is selectively enhanced in Arctic ground squirrel muscle because of an upregulation of androgen receptors (ARs). Using Western blot analysis, we found that Arctic ground squirrels have AR in skeletal muscle more than four times that of Columbian ground squirrels, a related southern species that overwinters at approximately 0°C and has low pre-hibernation androgen levels. By contrast, AR in lymph nodes was equivalent in both species. Brain AR was also modestly but significantly increased in Arctic ground squirrel relative to Columbian ground squirrel. These results are consistent with the hypothesis that tissue-specific AR regulation prior to hibernation provides a mechanism whereby Arctic ground squirrels obtain the life-history benefits and mitigate the costs associated with high androgen production.


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