Freeze Tolerance and Supercooling Ability in the Italian Wall Lizard, Podarcis sicula, Introduced to Long Island, New York

Burke, Russell L.; Hussain, Ahmed; Storey, Janet M.; Storey, Kenneth B.

doi:10.1643/0045-8511(2002)002[0836:ftasai]2.0.co;2

Cited by 34 publications

(28 citation statements)

References 10 publications

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“…R. ridibunda and probably other species listed in Table 3 correspond to this definition. However, important variation could occur within this group between amphibians and reptiles: indeed, recent studies showed that Podarcis sp die if ice content goes beyond 20% of body fluids (Claussen et al, '90;Burke et al, 2002) while R. ridibunda survive to 55% of ice (this study). Further studies focused on the physiological mechanisms occurring (or not) in response to freezing in these animals are needed.…”

Section: Discussionmentioning

confidence: 53%

Survival and metabolic responses to freezing by the water frog (Rana ridibunda)

Voituron¹,

Eugène²,

Barré³

2003

J. Exp. Zool.

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We studied the ability of the marsh frog Rana ridibunda to survive freezing exposure and the associated subsequent metabolic variations. This species that typically overwinters under water tolerates the conversion of 55% of its body water into ice. This ice content is attained after a few hours (between 8 and 36 hours depending on the mass of the individual and the environmental temperature) but death occurs at greater than 58% ice. Freezing stimulated a significant increase in blood carnitine and trimethylamine levels (respectively 4.5+/-2.5 and 0.5+/-0.2 micromol.l(-1) for controls versus 27.0+/-18.9 and 3.6+/-4.1 micromol.l(-1) after thawing) but these increases had no significant effect on plasma osmolality which was unchanged between control and freeze exposed frogs (252.6+/-20.3 versus 240.2+/-25.0 mOsmol.l(-1), respectively). Freezing also induced a significant dehydration of heart, liver and muscles (respectively 4.2, 3.2 and 2.8%) but the observed levels are low compared to values found in highly freeze tolerant species. This species could be classified as "partially freeze tolerant" enduring the transformation of a significant part of its body water into ice but not the completion of the exotherm. The existence of freeze tolerance in an aquatic hibernator that does not accumulate cryoprotectant, exhibiting low organ dehydration after freezing and low hypoxia tolerance, raises the possibility that a tolerance of nearly 60% ice within the body is common among anurans.

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Section: Discussionmentioning

confidence: 53%

Survival and metabolic responses to freezing by the water frog (Rana ridibunda)

Voituron¹,

Eugène²,

Barré³

2003

J. Exp. Zool.

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“…The sand lizard L. agilis and the wall lizards Podarcis sicula and Podarcis muralis are not able to survive even for short periods (30 to 120 min) when kept below À1.11C and never tolerated more than 28% of their body fluid converted into ice (Weigmann, '29;Claussen et al, '90;Burke et al, 2002).…”

Section: Y Voituron Et Almentioning

confidence: 99%

“…There are a few species of reptiles, however, known to have various degrees of freeze tolerance. Some of them, e.g., the wall lizards, Podarcis muralis and P. sicula, and the boreal adder, Vipera berus, only tolerate conversion of a limited proportion of their body fluid into ice for a very brief period (less than 30% for less than 4h) (Claussen et al, '90;Andersson and Johansson, 2001;Burke et al, 2002). Others, such as the European common lizard Lacerta vivipara, the common garter snake Thamnophis sirtalis, the painted turtle Chrysemys picta, and the box turtles Terrapene carolina and T. ornata, are able to survive freezing for 24 hours and more with 30-50% of body fluids converted into ice (Storey et al, '88;Costanzo and Lee, '88;Costanzo and Claussen, '90;Costanzo et al, '95;Voituron et al, 2002a).…”

Section: Introductionmentioning

confidence: 99%

Comparison of the cold hardiness capacities of the oviparous and viviparous forms of Lacerta vivipara

Voituron¹,

Heulin²,

Surget‐Groba³

2004

J. Exp. Zool.

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The lizard Lacerta vivipara has allopatric oviparous and viviparous populations. The cold hardiness strategy of L. vivipara has previously been studied in viviparous populations, but never in oviparous ones. The present study reveals that both the oviparous and viviparous individuals of this species are able to survive in a supercooled state at -3 degrees C for at least one week when kept on dry substrates. The mean crystallisation temperatures of the body, around -4 degrees C on dry substrata and -2 degrees C on wet substrata, do not differ between oviparous and viviparous individuals. All the individuals are able to tolerate up to 48-50% of their body fluid converted into ice, but only viviparous individuals were able to stabilize their body ice content at 48%, and hence were able to survive even when frozen at -3 degrees C for times of up 24 hours. Ice contents higher than 51% have been constantly found lethal for oviparous individuals. This suggests that, in L. vivipara, the evolution towards a higher degree of freezing tolerance could parallel the evolution of the viviparous reproductive mode, a feature believed to be strongly selected under cold climatic conditions. This is the first report, among reptiles, of an intraspecific variation regarding the freeze tolerance capacities.

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“…Metabolic activity under freezing conditions, even if very low, is still present. It would seem important now to conduct similar experiments on highly freeze-tolerant vertebrates such as Rana sylvatica, which can endure several weeks of freezing (27), and also poorly freezetolerant vertebrates such as Podarcis sicula (4). Such comparison between animals exhibiting different levels of freeze tolerance could provide deeper insight into the evolutionary physiology of temperate ectothermic species.…”

Section: Perspectivesmentioning

confidence: 99%

The respiratory metabolism of a lizard (Lacerta vivipara) in supercooled and frozen states

Voituron¹,

Verdier²,

Grenot³

2002

American Journal of Physiology-Regulatory, Integrative and Comp

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Voituron, Yann, Bruno Verdier, and Claude Grenot. The respiratory metabolism of a lizard (Lacerta vivipara) in supercooled and frozen states. Am J Physiol Regulatory Integrative Comp Physiol 283: R181-R186, 2002; 10.1152/ajpregu.00378.2001.-We investigated the respiratory metabolism of the overwintering lizard Lacerta vivipara while in either supercooled or frozen states. With a variable pressure and volume microrespirometer and a chromatograph, we show that the oxygen consumption of the supercooled animals showed a nonlinear relationship with temperature and an aerobic metabolism demand between 0.5 and Ϫ1.5°C. A significant increase in the respiratory quotient (RQ) values indicated an increasing contribution by the anaerobic pathways with decreasing temperature. In the frozen state, two phases are easily detectable and are probably linked to the ice formation within the body. During the first 5-6 h, the animals showed an oxygen consumption of 3.52 Ϯ 0.28 l ⅐ g Ϫ1 ⅐ h Ϫ1 and a RQ value of 0.52 Ϯ 0.09. In contrast, after ice equilibrium, oxygen consumption decreased sharply (0.55 Ϯ 0.09 l ⅐ g Ϫ1 ⅐ h Ϫ1 ) and the RQ values increased (2.49 Ϯ 0.65). The present study confirms the fact that supercooled invertebrates and vertebrates respond differently to subzero temperatures, in terms of aerobic metabolism, and it shows that aerobic metabolism persists under freezing conditions. oxygen consumption; anaerobiosis; respiratory quotient; Lacertidae MOST TEMPERATE ECTOTHERMS avoid subfreezing temperatures by migration or by using insulated hibernacula. However, some species, particularly terrestrial hibernators (i.e., certain amphibians, reptiles, and insects), have developed specific physiological mechanisms that allow them to evade cold injuries even during Arctic winter. The cold-hardiness strategies of such animals can be divided into two main groups: freeze tolerance, in which the animal endures the conversion of a fraction of its body water into ice; and freeze avoidance, in which the animal prevents crystallization (i.e., remaining in a metastable supercooled state) and preserves the liquid state of body fluids even at very low temperatures.Organs such as the lungs, heart, and liver are strongly affected by these two different strategies:freezing induces a cessation of heart activity and circulation, imposing an anoxic state on tissue cells (19). In contrast, in the supercooled state, the heart continues to beat even if the rate of contraction changes with temperature (3), and the lungs remain functional even if anaerobic metabolism takes on greater importance as temperature decreases (12).To compare the metabolic balance (anaerobic vs. aerobic metabolism) under these two physiological states, we focused our study on O 2 consumption and CO 2 release during cooling, supercooling, and freezing states. In fact, it is well known that the gas exchange rate in ectotherms is strongly dependent on environmental conditions and the physiological state of the animal (7, 24), but few studies have assessed the gas flux in these...

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Freeze Tolerance and Supercooling Ability in the Italian Wall Lizard, Podarcis sicula, Introduced to Long Island, New York

Cited by 34 publications

References 10 publications

Survival and metabolic responses to freezing by the water frog (Rana ridibunda)

Survival and metabolic responses to freezing by the water frog (Rana ridibunda)

Comparison of the cold hardiness capacities of the oviparous and viviparous forms of Lacerta vivipara

The respiratory metabolism of a lizard (Lacerta vivipara) in supercooled and frozen states

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