Cryoprotectants and Extreme Freeze Tolerance in a Subarctic Population of the Wood Frog

Costanzo, Jon P.; Reynolds, Alice M.; Amaral, M. Clara F. do; Rosendale, Andrew J.; Lee, Richard

doi:10.1371/journal.pone.0117234

Cited by 65 publications

(61 citation statements)

References 67 publications

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“…We also note that wood frogs may use protein in addition to lipids to meet their energy needs via aerobic metabolism between freezes. Though extensive muscle atrophy may be disadvantageous to spring breeding activities, proteolysis is important in autumn glycogen synthesis and urea acclimation of Alaskan wood frogs (Costanzo et al , 2015. Future studies could measure size of muscle glycogen and protein stores in relation to whole body mass to assess potential contribution to winter survival.…”

Section: Modeling Wood Frog Physiology At Landscape Scalesmentioning

confidence: 99%

Modeling the distribution of niche space and risk for a freeze‐tolerant ectotherm, Lithobates sylvaticus

et al. 2019

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Many animals depend on stable below‐the‐snow (subnivium) conditions to survive winter in seasonally cold regions. Freeze‐tolerant ectotherms may experience increased ice content and/or energy expenditure in suboptimal subnivium conditions, with implications for overwinter survival and body reserves available for spring reproduction. We used a novel mechanistic modeling approach to explore effects of winter climate on the microclimate conditions, energy expenditure, and ice dynamics of the freeze‐tolerant, subnivium‐dwelling wood frog (Lithobates sylvaticus) in the Upper Midwest and Great Lakes Basin region of the United States. We hypothesized that (1) frogs would experience the greatest energy cost to survive winter in southern regions of our study area, where air temperatures are warmer and shallower snow could allow for increased numbers of freeze–thaw cycles, and (2) frogs would be most vulnerable to lethal freezing in the cold, dry northwest portion of our study region. We found that total winter energy expenditure changed little with latitude because the effect of warmer soil temperatures (higher metabolic rates) to the south was offset by a shorter winter duration. Energy expenditures were greatest in the snowbelts of the Great Lakes, characterized by more persistent snow cover and relatively warm soil temperatures. In contrast, highest ice contents occurred in the northwest of the study region where air temperatures were coldest and snow was shallow. Thus, it appears that wood frogs experience a trade‐off between risk of lethal ice content and extensive use of body reserves across geographic space. Simulations showed that interpopulation differences in burrow depth and cryoprotectant concentration can influence risk of lethal ice content and overuse of body reserves prior to spring breeding, and those risks vary in relation to winter climate. Our mechanistic modeling approach is a novel tool for predicting risk and shifting niche space for cold‐adapted and subnivium‐dependent species.

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Section: Modeling Wood Frog Physiology At Landscape Scalesmentioning

confidence: 99%

Modeling the distribution of niche space and risk for a freeze‐tolerant ectotherm, Lithobates sylvaticus

et al. 2019

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“…This leads to the predication that mobility in these animals may be impaired by elevated glycerol. Wood frogs, Rana sylvatica, elevate urea as a cryoprotectant in the months leading to winter (Costanzo et al, 2013(Costanzo et al, , 2015. Interestingly, wood frogs also significantly elevate an additional unidentified osmolyte in winter (Costanzo et al, 2015).…”

Section: Discussionmentioning

confidence: 99%

“…In contrast, rainbow smelt do show 'positive' effects of TMAO on muscle force production and power output, suggesting that the response of smelt muscle proteins to the stabilizing effects of TMAO is not simply a property of all myosins, for instance, but reflects a difference between trout and smelt. Glycerol and urea, both of which are cryoprotectant molecules (Raymond, 1992;Zimmerman et al, 2007;Costanzo et al, 2015), had significantly negative impacts on muscle force and power production. In smelt, the impact of urea and glycerol appears to be mitigated by the counteracting osmolyte TMAO.…”

Section: Discussionmentioning

confidence: 99%

“…Wood frogs, Rana sylvatica, elevate urea as a cryoprotectant in the months leading to winter (Costanzo et al, 2013(Costanzo et al, , 2015. Interestingly, wood frogs also significantly elevate an additional unidentified osmolyte in winter (Costanzo et al, 2015). From a muscle physiology perspective, this unidentified osmolyte would likely be a counteracting osmolyte that would balance the destabilizing effects of urea.…”

Section: Discussionmentioning

confidence: 99%

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Elevated osmolytes in rainbow smelt: the effects of urea, glycerol and trimethylamine oxide on muscle contractile properties

Coughlin

Long

Gezzi

et al. 2016

Journal of Experimental Biology

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Rainbow smelt, Osmerus mordax, experience a wide range of temperatures in their native habitat. In response to cold, smelt express anti-freeze proteins and the osmolytes glycerol, trimethylamine N-oxide (TMAO) and urea to avoid freezing. The physiological influences of these osmolytes are not well understood. Urea destabilizes proteins, while TMAO counteracts the proteindestabilizing forces of urea. The influence of glycerol on muscle function has not been explored. We examined the effects of urea, glycerol and TMAO through muscle mechanics experiments with treatments of the three osmolytes at physiological concentrations. Experiments were carried out at 10°C. The contractile properties of fast-twitch muscle bundles were determined in physiological saline and in the presence of 50 mmol l −1 urea, 50 mmol l −1 TMAO and/or 200 mmol l −1 glycerol in saline. Muscle exposed to urea and glycerol produced less force and displayed slower contractile properties. However, treatment with TMAO led to higher force and faster relaxation by muscle bundles. TMAO increased power production during cyclical activity, while urea and glycerol led to reduced oscillatory power output. When muscle bundles were exposed to a combination of the three osmolytes, they displayed little change in contraction kinetics relative to control, although power output under lower oscillatory conditions was enhanced while maximum power output was reduced. The results suggest that maintenance of muscle function in winter smelt requires a balanced combination of urea, glycerol and TMAO.

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“…In this regard, the winter physiology of the wood frog (Rana sylvatica) presents an ideal study system. The most northerly distributed of North American amphibians, R. sylvatica hibernates for up to 8 months in a shallow, terrestrial form, where it readily endures chronic cold, dehydration, hypoxia, corporeal freezing, and extended aphagia (Costanzo et al 2015;Larson et al 2014). In the laboratory, winter-acclimatized frogs tolerate the loss of up to 40% of their body water, the freezing of up to 65-70% of their body water, and exposure to hypoxia for several days (Costanzo et al 1993;Holden and Storey 1997).…”

Section: Introductionmentioning

confidence: 99%

Nitric oxide metabolites in hypoxia, freezing, and hibernation of the wood frog, Rana sylvatica

et al. 2018

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Nitric oxide (NO) is a gaseous free radical that in diverse organisms performs many signaling and protective functions, such as vasoregulation, inhibition of apoptosis, antioxidation, and metabolic suppression. Increased availability of NO may be especially important during life-history periods when organisms contend with multiple stresses. We investigated dynamics of the NO metabolites, nitrite (NO) and nitrate (NO), in the blood plasma, heart, liver, and skeletal muscle of the wood frog (Rana sylvatica), an amphibian that endures chronic cold, freezing, hypoxia, dehydration, and extended aphagia during hibernation. We found elevated concentrations of NO and/or NO in the plasma (up to 4.1-fold), heart (3.1-fold), and liver (up to 4.1-fold) of frogs subjected to experimental hypoxia (24 h, 4 °C), and in the liver (up to 3.8-fold) of experimentally frozen frogs (48 h, - 2.5 °C), suggesting that increased NO availability aids in survival of these stresses. During a 38-week period of simulated hibernation, NO and/or NO increased in the plasma (up to 10.4-fold), heart (up to 3.3-fold), and liver (5.0-fold) during an initial 5-week winter-acclimatization regimen and generally remained elevated thereafter. In hibernation, plasma NO was higher in frogs indigenous to Interior Alaska than in conspecifics from a temperate locale (southern Ohio), suggesting that NO availability is matched to the severity of environmental conditions prevailing in winter. The comparatively high NO availability in R. sylvatica, a stress-tolerant species, together with published values for other species, suggest that the NO protection system is of general importance in the stress adaptation of vertebrates.

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Cryoprotectants and Extreme Freeze Tolerance in a Subarctic Population of the Wood Frog

Cited by 65 publications

References 67 publications

Modeling the distribution of niche space and risk for a freeze‐tolerant ectotherm, Lithobates sylvaticus

Modeling the distribution of niche space and risk for a freeze‐tolerant ectotherm, Lithobates sylvaticus

Elevated osmolytes in rainbow smelt: the effects of urea, glycerol and trimethylamine oxide on muscle contractile properties

Nitric oxide metabolites in hypoxia, freezing, and hibernation of the wood frog, Rana sylvatica

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