Cold Hardiness in Animals: The Cryobiology of Amphibians

Year 2022, , 242 - 253, 31.12.2022

Taner Yoldas , Uğur Cengiz Erişmiş

https://doi.org/10.31594/commagene.1176451

Abstract

Organisms adapt to abiotic environmental conditions in order to survive. Especially environmental temperature changes are effective on their feeding, reproduction, development, and morphology. Extreme temperature changes can be fatal, especially for ectothermic animals. Terrestrial ectotherms have developed some special behavioral, physiological, and biochemical strategies to survive in freezing temperatures in nature. Some species avoid freezing temperatures by migrating and hibernating under water or soil. Others have to spend the winter exposed to freezing conditions. In general, cold hardiness depends on freeze avoidance (supercooling) and freeze tolerance strategies. In the case of freeze avoidance, the liquid form of body fluids is preserved at temperatures below the freezing point, while the freezing of more than 50% of the total water in their bodies can be tolerated in animals using the freeze tolerance strategy. The freeze tolerance strategy, which has also been found in some amphibian and reptile groups from terrestrial hibernator animals, enables them to survive in freezing winter conditions. These special species are protected from the deadly effects of freezing by the cryoprotective mechanisms. These animals, whose vital activities are completely stopped during freezing, return to normal life in a short time after thawing. The research of this miraculous mechanism not only explains the complex adaptation of animals but also provides resources for tissue and cell cryopreservation technology. This review will contribute to those who want to do research on this subject, which has not yet been studied enough, by providing information on the freeze tolerance strategies of amphibians.

Keywords

Ectoterm hibernation, Freeze tolerance, Freeze avoidance, Cryoprotectants, Antifreeze proteins, Antioxidant defense

Hayvanlarda Soğuğa Dayanıklılık: Çift Yaşarların Kriyobiyolojisi

Abstract

Organizmalar yaşamlarını devam ettirebilmek için abiyotik çevresel koşullara uyum sağlarlar. Özellikle ortam sıcaklığındaki değişimler; canlıların beslenme, üreme, gelişim ve morfolojileri üzerinde etkilidir. Sıra dışı sıcaklık değişimleri özellikle ektotermik hayvanlar için ölümcül olabilir. Karasal ektotermler. doğada donma noktasının altındaki sıcaklıklarda hayatta kalabilmek için davranışsal, fizyolojik ve biyokimyasal bazı özel stratejiler geliştirmişlerdir. Bazı türler göç ederek su ya da toprak altında kış uykusuna yatmak suretiyle dondurucu sıcaklıklardan kaçınırlar. Bazıları ise donma koşullarına maruz kalarak kışı geçirmek zorundadırlar. Genel olarak dondurucu soğuğa dayanıklılık donmadan kaçınma (süper soğuma) ve donma toleransı stratejilerine bağlıdır. Donmadan kaçınma durumunda vücut sıvılarının donma noktasının altındaki sıcaklıklarda sıvı formu korunurken donma toleransı stratejisini kullanan canlılarda ise vücutlarındaki toplam suyun %50’sinden fazlasının donması tolere edilebilir. Karasal hibernatör hayvanlardan bazı amfibi ve sürüngen gruplarında da tespit edilen donma toleransı stratejisi onların dondurucu kış koşullarında hayatta kalmalarını sağlamaktadır. Bu özel türler kriyoprotektif mekanizmaları ile donmanın ölümcül etkilerinden korunurlar. Donma süresince yaşamsal faaliyetleri tamamen duran bu hayvanlar çözündükten sonra kısa bir süre içerisinde de normal yaşama dönerler. Bu mucizevi mekanizmanın araştırılması yalnızca hayvanların karmaşık adaptasyonunu açıklamakla kalmaz, aynı zamanda doku ve hücre kriyoprezervasyon teknolojisine de kaynak sağlar. Bu derleme amfibilerin donma toleransı stratejilerine dair bilgiler sunarak henüz yeterince çalışılmamış bu konuda araştırma yapmak isteyenlere katkı sağlayacaktır.

Keywords

Ektoterm kış uykusu, Donma toleransı, Donmadan kaçınma, Kriyoprotektanlar, Antifriz proteinler, Antioksidan savunma

References

• Al-attar, R., Wu, C.-W., Biggar, K. K., & Storey, K. B. (2020). Carb-Loading: Freeze-Induced Activation of the Glucose-Responsive ChREBP Transcriptional Network in Wood Frogs. Physiological and Biochemical Zoology, 93(1), 49–61. https://doi.org/10.1086/706463
• Amaral, M. C. F. do, Frisbie, J., Crum, R. J., Goldstein, D. L., & Krane, C. M. (2020). Hepatic Transcriptome of the Freeze-Tolerant Cope’s Gray Treefrog, Dryophytes chrysoscelis : Responses to Cold Acclimation and Freezing. BMC Genomics, 21(1), 1–18. https://doi.org/10.1186/s12864-020-6602-4
• Amaral, M. C. F. do, Frisbie, J., Goldstein, D. L., & Krane, C. M. (2018). The Cryoprotectant System of Cope’s Gray Treefrog, Dryophytes chrysoscelis: Responses to Cold Acclimation, Freezing, And Thawing. Journal of Comparative Physiology B, 188(4), 611–621. https://doi.org/10.1007/s00360-018-1153-6
• Baker, P. J., Costanzo, J. P., Iverson, J. B., & Lee, R. E. (2003). Adaptations to terrestrial overwintering of hatchling northern map turtles, Graptemys geographica. Journal of Comparative Physiology B, 173(8), 643–651. https://doi.org/10.1007/s00360-003-0373-5
• Bektaş, G. I., & Altıntaş, A. (2007). Antifriz Proteinler. Etlik Veteriner Mikrobiyoloji Dergisi, 18, 27–32.
• Berman, D. I., Bulakhova, N. A., & Meshcheryakova, E. N. (2017). Adaptive strategies of brown frogs (amphibia, anura, Rana) in relation to winter temperatures in the northern Palaearctic. Zoologicheskii Zhurnal, 96(11), 1392–1403. https://doi.org/10.7868/S0044513417110034
• Berman, D. I., Bulakhova, N. A., Meshcheryakova, E. N., & Shekhovtsov, S. V. (2020). Overwintering and cold tolerance in the Moor Frog ( Rana arvalis ) across its range. Canadian Journal of Zoology, 98(11), 705–714. https://doi.org/10.1139/cjz-2019-0179
• Berman, D. I., Leirikh, A. N., & Meshcheryakova, E. N. (2010). The Schrenck Newt (Salamandrella schrenckii, Amphibia, Caudata, Hynobiidae) is The Second Amphibian That Withstands Extremely Low Temperatures. Doklady Biological Sciences, 431(1), 131–134. https://doi.org/10.1134/S0012496610020171
• Berman, D. I., & Meshcheryakova, E. N. (2012). Is the western boundary of the Siberian salamander (Salamandrella keyserlingii, Amphibia, Caudata, Hynobiidae) range determined by the specific features of its wintering? Doklady Biological Sciences, 443(1), 97–100. https://doi.org/10.1134/S0012496612020068
• Biggar, K. K., Dubuc, A., & Storey, K. (2009). MicroRNA Regulation Below Zero: Differential Expression of miRNA-21 and miRNA-16 During Freezing in Wood Frogs. Cryobiology, 59(3), 317–321. https://doi.org/10.1016/j.cryobiol.2009.08.009
• Biggar, K. K., Kotani, E., Furusawa, T., & Storey, K. B. (2013). Expression of freeze-responsive proteins, Fr10 and Li16, from freeze-tolerant frogs enhances freezing survival of BmN insect cells. FASEB Journal, 27(8), 3376–3383. https://doi.org/10.1096/fj.13-230573
• Bulakhova, N. A., Mazanaeva, L. F., Meshcheryakova, E. N., & Berman, D. I. (2020). Resistance of the Iranian long-legged wood frog (Rana macrocnemis Boulenger, 1885) (Amphibia, Anura) to negative temperatures on land and to hypoxia in water during overwintering. Herpetology Notes, 13(December), 1079–1086.
• Cai, Q., & Storey, K. B. (1997). Upregulation of a Novel Gene by Freezing Exposure in The Freeze-Tolerant Wood Frog (Rana sylvatica). Gene, 198(1–2), 305–312. https://doi.org/10.1016/S0378-1119(97)00332-6
• Churchill, T. A., & Storey, K. B. (1994). Effects of Dehydration on Organ Metabolism In The Frog Pseudacris crucifer: Hyperglycemic Responses to Dehydration Mimic Freezing-Induced Cryoprotectant Production. Journal of Comparative Physiology B, 164(6), 492–498. https://doi.org/10.1007/BF00714587
• Churchill, T. A., & Storey, K. B. (1995). Metabolic Effects of Dehydration on An Aquatic Frog, Rana pipiens. The Journal of Experimental Biology, 198(Pt 1), 147–154. http://www.ncbi.nlm.nih.gov/pubmed/7891032
• Costanzo, J. P. (2005). Cryoprotection By Urea In A Terrestrially Hibernating Frog. Journal of Experimental Biology, 208(21), 4079–4089. https://doi.org/10.1242/jeb.01859
• Costanzo, J. P. (2019). Overwintering adaptations and extreme freeze tolerance in a subarctic population of the wood frog, Rana sylvatica. Journal of Comparative Physiology B, 189(1), 1–15. https://doi.org/10.1007/s00360-018-1189-7
• Costanzo, J. P., Amaral, M. C. F. do, Rosendale, A. J., & Lee, R. E. (2013). Hibernation Physiology, Freezing Adaptation and Extreme Freeze Tolerance In A Northern Population of The Wood Frog. Journal of Experimental Biology, 216(18), 3461–3473. https://doi.org/10.1242/jeb.089342
• Costanzo, J. P., Grenot, C., & Lee, R. E. (1995). Supercooling, ice inoculation and freeze tolerance in the European common lizard, Lacerta vivipara. Journal of Comparative Physiology B, 165(3), 238–244. https://doi.org/10.1007/BF00260815
• Costanzo, J. P., & Lee, R. E. (2008). Urea Loading Enhances Freezing Survival and Postfreeze Recovery In A Terrestrially Hibernating Frog. Journal of Experimental Biology, 211(18), 2969–2975. https://doi.org/10.1242/jeb.019695
• Costanzo, J. P., & Lee, R. E. (2013). Avoidance and Tolerance of Freezing In Ectothermic Vertebrates. Journal of Experimental Biology, 216(11), 1961–1967. https://doi.org/10.1242/jeb.070268
• Costanzo, J. P., Lee, R. E., DeVries, A. L., Wang, T., & Layne, J. R. (1995). Survival mechanisms of vertebrate ectotherms at subfreezing temperatures: applications in cryomedicine. The FASEB Journal, 9(5), 351–352. https://doi.org/10.1096/fasebj.9.5.7896003
• Costanzo, J. P., Lee, R. E., & Lortz, P. H. (1993). Physiological responses of freeze-tolerant and -intolerant frogs: clues to evolution of anuran freeze tolerance. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 265(4), R721–R725. https://doi.org/10.1152/ajpregu.1993.265.4.R721
• Costanzo, J. P., Lee, R. E., & Ultsch, G. R. (2008). Physiological ecology of overwintering in hatchling turtles. Journal of Experimental Zoology Part A: Ecological Genetics and Physiology, 309A(6), 297–379. https://doi.org/10.1002/jez.460
• Costanzo, J. P., Reynolds, A. M., Amaral, M. C. F. do, Rosendale, A. J., & Lee, R. E. (2015). Cryoprotectants and Extreme Freeze Tolerance In A Subarctic Population of The Wood Frog. PLOS ONE, 10(2), e0117234. https://doi.org/10.1371/journal.pone.0117234
• Croes, S. A., & Thomas, R. E. (2000). Freeze tolerance and cryoprotectant synthesis of the Pacific Tree Frog Hyla regilla. Copeia, 3, 863–868. https://doi.org/10.1643/0045-8511(2000)000[0863:FTACSO]2.0.CO;2
• Devries, A. L. (1971). Glycoproteins As Biological Antifreeze Agents In Antarctic Fishes. Science, 172(3988), 1152–1155. https://doi.org/10.1126/science.172.3988.1152
• Dieni, C. A., Bouffard, M. C., & Storey, K. B. (2012). Glycogen Synthase Kinase-3: Cryoprotection and Glycogen Metabolism In The Freeze-Tolerant Wood Frog. Journal of Experimental Biology, 215(3), 543–551. https://doi.org/10.1242/jeb.065961
• Donoso, D. P., Bauer, A. M., Meiri, S., & Uetz, P. (2013). Global Taxonomic Diversity of Living Reptiles. PLoS ONE, 8(3), e59741. https://doi.org/10.1371/journal.pone.0059741
• Duman, J. G. (2001). Antifreeze and Ice Nucleator Proteins in Terrestrial Arthropods. Annual Review of Physiology, 63(1), 327–357. https://doi.org/10.1146/annurev.physiol.63.1.327
• Duman, J. G. (2015). Animal Ice-Binding (Antifreeze) Proteins And Glycolipids: An Overview With Emphasis on Physiological Function. Journal of Experimental Biology, 218(12), 1846–1855. https://doi.org/10.1242/jeb.116905
• Duman, J. G., & Newton, S. S. (2020). Insect Antifreeze Proteins. In H. Ramløv & D. S. Friis (Eds.), Antifreeze Proteins Volume 1 (Vol. 1, pp. 131–187). Springer International Publishing. https://doi.org/10.1007/978-3-030-41929-5_6
• Duman, J. G., Wu D. W., Xu L., Tursman D., Olsen T. M. (1991). Adaptations of Insects to Subzero Temperatures, The Quarterly Review of Biology, 66(4), 387-410. https://doi.org/10.1086/417337
• Eskandari, A., Leow, T. C., Rahman, M. B. A., & Oslan, S. N. (2020). Antifreeze Proteins and Their Practical Utilization in Industry, Medicine, and Agriculture. Biomolecules, 10(12), 1649. https://doi.org/10.3390/biom10121649
• Geiser, F. (2004). Metabolic Rate and Body Temperature Reduction During Hibernation and Daily Torpor. Annual Review of Physiology, 66(1), 239–274. https://doi.org/10.1146/annurev.physiol.66.032102.115105
• Geiser, F. (2020). Seasonal Expression of Avian and Mammalian Daily Torpor and Hibernation: Not a Simple Summer-Winter Affair†. Frontiers in Physiology, 11(May), 1–19. https://doi.org/10.3389/fphys.2020.00436
• Güleç, S. (2019). Hibernasyonda ‘Pelophylax caralitanus’ (Amphibia: Anura)’da DNA Hasarının Araştırılması (536228). Retrieved from https://tez.yok.gov.tr/UlusalTezMerkezi/giris.jsp.
• Hawkins, L. J., Wang, M., Zhang, B., Xiao, Q., Wang, H., & Storey, K. B. (2019). Glucose and urea metabolic enzymes are differentially phosphorylated during freezing, anoxia, and dehydration exposures in a freeze tolerant frog. Comparative Biochemistry and Physiology Part D: Genomics and Proteomics, 30(December 2018), 1–13. https://doi.org/10.1016/j.cbd.2019.01.009
• Hillman, S. S., Withers, P. C., Drewes, R. C., & Hillyard, S. D. (2008). Ecological and Environmental Physiology of Amphibians. In Ecological and Environmental Physiology of Amphibians. Oxford University Press. https://doi.org/10.1093/acprof:oso/9780198570325.001.0001
• Hirota, A., Takiya, Y., Sakamoto, J., Shiojiri, N., Suzuki, M., Tanaka, S., & Okada, R. (2015). Molecular Cloning of cDNA Encoding an Aquaglyceroporin, AQP-h9, in the Japanese Tree Frog, Hyla japonica: Possible Roles of AQP-h9 in Freeze Tolerance. Zoological Science, 32(3), 296–306. https://doi.org/10.2108/zs140246
• Irwin, J. T., & Lee, J. R. E. (2003). Geographic Variation In Energy Storage and Physiological Responses to Freezing In The Gray Treefrogs Hyla versicolor and H. chrysoscelis. Journal of Experimental Biology, 206(16), 2859–2867. https://doi.org/10.1242/jeb.00500
• Jackson, D. C. (2002). Hibernating without Oxygen: Physiological Adaptations of the Painted Turtle. The Journal of Physiology, 543(3), 731–737. https://doi.org/10.1113/jphysiol.2002.024729
• Joanisse, D. R., & Storey, K. B. (1996). Oxidative Damage And Antioxidants In Rana sylvatica, The Freeze-Tolerant Wood Frog. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 271(3), R545–R553. https://doi.org/10.1152/ajpregu.1996.271.3.r545
• Kart Gür, M., Bulut, Ş., Gür, H., & Refinetti, R. (2014). Body Temperature Patterns And Use of Torpor In An Alpine Glirid Species, Woolly Dormouse. Acta Theriologica, 59(2), 299–309. https://doi.org/10.1007/s13364-013-0154-9
• Kart Gür, M., & Gür, H. (2017). Küçük Bir Memeli Türünün Ekofizyolojisi ve Evrimsel Coğrafyası: Anadolu Yer Sincabı. Kebikec: Insan Bilimleri Icin Kaynak Arastirmali Dergisi, 43, 189–198.
• Kelleher, M. J., Rickards, J., & Storey, K. B. (1987). Strategies of Freeze Avoidance In Larvae of The Goldenrod Gall Moth, Epiblema scudderiana: Laboratory Investigations of Temperature Cues In The Regulation of Cold Hardiness. Journal of Insect Physiology, 33(8), 581–586. https://doi.org/10.1016/0022-1910(87)90073-4
• Kültz, D. (2005). Molecular and Evolutionary Basis of the Cellular Stress Response. Annual Review of Physiology, 67(1), 225–257. https://doi.org/10.1146/annurev.physiol.67.040403.103635
• Layne, J. R., & Lee, R. E. (1987). Freeze tolerance and the dynamics of ice formation in wood frogs (Rana sylvatica) from southern Ohio. Canadian Journal of Zoology, 65(8), 2062–2065. https://doi.org/10.1139/z87-315
• Layne, J. R., & Lee, R. E. (1989). Seasonal variation in freeze tolerance and ice content of the tree frog Hyla versicolor. The Journal of Experimental Zoology, 249(2), 133–137. https://doi.org/10.1002/jez.1402490203
• Layne, J. R., & Stapleton, M. G. (2009). Annual Variation In Glycerol Mobilization and Effect of Freeze Rigor on Post-Thaw Locomotion In The Freeze-Tolerant Frog Hyla versicolor. Journal of Comparative Physiology B, 179(2), 215. https://doi.org/10.1007/s00360-008-0304-6
• Lima, M. H., & Savin, T. Z. (2002). Animal Response to Drastic Changes In Oxygen Availability and Physiological Oxidative Stress. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 133(4), 537–556. https://doi.org/10.1016/S1532-0456(02)00080-7
• MacDonald, J. A., & Storey, K. B. (1999). Regulation of Ground Squirrel Na+K+-ATPase Activity by Reversible Phosphorylation During Hibernation. Biochemical and Biophysical Research Communications, 254(2), 424–429. https://doi.org/10.1006/bbrc.1998.9960
• Merlin, C., & Liedvogel, M. (2019). The Genetics and Epigenetics of Animal Migration and Orientation: Birds, Butterflies and Beyond. Journal of Experimental Biology, 222(Pt Suppl 1), jeb191890. https://doi.org/10.1242/jeb.191890
• McNally, J. D., Sturgeon, C. M., & Storey, K. B. (2003). Freeze-Induced Expression of a Novel Gene, fr47, In The Liver of The Freeze-Tolerant Wood Frog, Rana sylvatica. Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression, 1625(2), 183–191. https://doi.org/10.1016/S0167-4781(02)00603-6
• McNally, J. D., Wu, S.-B., Sturgeon, C. M. C. M., & Storey, K. B. (2002). Identification and Characterization of a Novel Freezing Inducible Gene, li16, In The Wood Frog Rana sylvatica. The FASEB Journal, 16(8), 902–904. https://doi.org/10.1096/fj.02-0017fje
• Naing, A. H., & Kim, C. K. (2019). A brief review of applications of antifreeze proteins in cryopreservation and metabolic genetic engineering. 3 Biotech, 9(9), 329. https://doi.org/10.1007/s13205-019-1861-y
• Niu, Y., Cao, W., Wang, J., He, J., Storey, K. B., Ding, L., Tang, X., & Chen, Q. (2021). Freeze tolerance and the underlying metabolite responses in the Xizang plateau frog, Nanorana parkeri. Journal of Comparative Physiology B, 191(1), 173–184. https://doi.org/10.1007/s00360-020-01314-0
• Niu, Y., Wang, J., Men, S., Zhao, Y., Lu, S., Tang, X., & Chen, Q. (2018). Urea and Plasma Ice-Nucleating Pproteins Ppromoted The Modest Freeze Tolerance In Pleske’s High Altitude Frog Nanorana pleskei. Journal of Comparative Physiology B, 188(4), 599–610. https://doi.org/10.1007/s00360-018-1159-0
• Olijve, L. L. C., Meister, K., DeVries, A. L., Duman, J. G., Guo, S., Bakker, H. J., Voetsa, I. K., & Voets, I. K. (2016). Blocking Rapid Ice Crystal Growth Through Nonbasal Plane Adsorption of Antifreeze Proteins. Proceedings of the National Academy of Sciences, 113(14), 3740–3745. https://doi.org/10.1073/pnas.1524109113
• Roy, P., & Goswami, P. (2019). Freeze tolerance in wood frogs. Journal of Investigative Genomics, 6(1), 1–4. https://doi.org/10.15406/jig.2019.06.00078
• Sformo, T., Walters, K., Jeannet, K., Wowk, B., Fahy, G. M., Barnes, B. M., & Duman, J. G. (2010). Deep supercooling, vitrification and limited survival to -100°C in the Alaskan beetle Cucujus clavipes puniceus (Coleoptera: Cucujidae) larvae. Journal of Experimental Biology, 213(3), 502–509. https://doi.org/10.1242/jeb.035758
• Sinclair, B. J., Stinziano, J. R., Williams, C. M., MacMillan, H. A., Marshall, K. E., & Storey, K. B. (2013). Real-time measurement of metabolic rate during freezing and thawing of the wood frog, Rana sylvatica : implications for overwinter energy use. Journal of Experimental Biology, 216(2), 292–302. https://doi.org/10.1242/jeb.076331
• Stogsdill, B., Frisbie, J., Krane, C. M., & Goldstein, D. L. (2017). Expression of the aquaglyceroporin HC-9 in a freeze-tolerant amphibian that accumulates glycerol seasonally. Physiological Reports, 5(15). https://doi.org/10.14814/phy2.13331
• Storey, J. M., Wu, S., & Storey, K. B. (2021). Mitochondria and the Frozen Frog. Antioxidants, 10(4), 543. https://doi.org/10.3390/antiox10040543
• Storey, K. B. (2004). Strategies for exploration of freeze responsive gene expression: advances in vertebrate freeze tolerance. Cryobiology, 48(2), 134–145. https://doi.org/10.1016/j.cryobiol.2003.10.008
• Storey, K. B., & Storey, J. M. (1986). Freeze tolerance and intolerance as strategies of winter survival in terrestrially-hibernating amphibians. Comparative Biochemistry and Physiology Part A: Physiology, 83(4), 613–617. https://doi.org/10.1016/0300-9629(86)90699-7
• Storey, K. B., & Storey, J. M. (1987). Persistence of Freeze Tolerance in Terrestrially Hibernating Frogs after Spring Emergence. Copeia, 1987(3), 720. https://doi.org/10.2307/1445665
• Storey, K. B., & Storey, J. M. (2001). Signal Transduction and Gene Expression In The Regulation of Natural Freezing Survival. Cell and Molecular Response to Stress, 2(613), 1–19. https://doi.org/10.1016/S1568-1254(01)80003-6
• Storey, K. B., & Storey, J. M. (2004). Physiology, Biochemistry, and Molecular Biology of Vertebrate Freeze Tolerance: The Wood Frog. In E. Benson, B. Fuller, & N. Lane (Eds.), Life in the Frozen State (Vol. 274, pp. 243–274). CRC Press. https://doi.org/10.1201/9780203647073.ch7
• Storey, K. B., & Storey, J. M. (2007). Tribute to P. L. Lutz: Putting Life on `Pause’ - Molecular Regulation of Hypometabolism. Journal of Experimental Biology, 210(10), 1700–1714. https://doi.org/10.1242/jeb.02716
• Storey, K. B., & Storey, J. M. (2012). Insect cold hardiness: metabolic, gene, and protein adaptation. Canadian Journal of Zoology, 90(4), 456–475. https://doi.org/10.1139/z2012-011
• Storey, K. B., & Storey, J. M. (2013). Molecular Biology of Freezing Tolerance. Comprehensive Physiology, 3(3), 1283–1308. https://doi.org/10.1002/cphy.c130007
• Storey, K. B., & Storey, J. M. (2017). Molecular Physiology of Freeze Tolerance In Vertebrates. Physiological Reviews, 97(2), 623–665. https://doi.org/10.1152/physrev.00016.2016
• Storey, K. B., Storey, J. M., & Churchill, T. A. (1997). De Novo Protein Biosynthesis Responses to Water Stresses In Wood Frogs: Freeze–Thaw and Dehydration–Rehydration. Cryobiology, 34(3), 200–213. https://doi.org/10.1006/cryo.1997.2001
• Storey, K. B.., & Storey. (2011). Heat shock proteins and hypometabolism: adaptive strategy for proteome preservation. Research and Reports in Biology, 57. https://doi.org/10.2147/RRB.S13351
• Sullivan, K. J., Biggar, K. K., & Storey, K. B. (2015). Expression and Characterization of the Novel Gene fr47 During Freezing In The Wood Frog, Rana sylvatica. Biochemistry Research International, 2015, 1–8. https://doi.org/10.1155/2015/363912
• Sullivan, K. J., & Storey, K. B. (2012). Environmental Stress Responsive Expression of The Gene li16 In Rana sylvatica, The Freeze Tolerant Wood Frog. Cryobiology, 64(3), 192–200. https://doi.org/10.1016/j.cryobiol.2012.01.008
• Tan, Y. J., Xiong, Y., Ding, G. L., Zhang, D., Meng, Y., Huang, H. F., & Sheng, J. Z. (2013). Cryoprotectants up-regulate expression of mouse oocyte AQP7, which facilitates water diffusion during cryopreservation. Fertility and Sterility, 99(5), 1428–1435. https://doi.org/10.1016/j.fertnstert.2012.11.049
• Tang, Z., Chen, B., & Niu, C. (2021). Antioxidant defense response during hibernation and arousal in Chinese soft-shelled turtle Pelodiscus sinensis juveniles. Cryobiology, 99(January), 46–54. https://doi.org/10.1016/j.cryobiol.2021.01.015
• Tattersall, G. J., & Ultsch, G. R. (2008). Physiological Ecology of Aquatic Overwintering in Ranid Frogs. Biological Reviews, 83(2), 119–140. https://doi.org/10.1111/j.1469-185X.2008.00035.x
• Tejo, B. A., Asmawi, A. A., & Rahman, M. B. A. (2020). Antifreeze Proteins: Characteristics and Potential Applications Bimo. Makara Journal of Science, 24(1), 58–64. https://doi.org/10.7454/mss.v24i1.11728
• Ultsch, G. R. (2006). The Ecology of Overwintering Among Turtles: Where Turtles Overwinter and Its Consequences. Biological Reviews, 81(03), 339. https://doi.org/10.1017/S1464793106007032
• Voituron, Y., Barré, H., Ramløv, H., & Douady, C. J. (2009). Freeze Tolerance Evolution Among Anurans: Frequency and Timing of Appearance. Cryobiology, 58(3), 241–247. https://doi.org/10.1016/j.cryobiol.2009.01.001
• Voituron, Y., Eugene, M., & Barré, H. (2003). Survival and Metabolic Responses to Freezing by The Water Frog (Rana ridibunda). Journal of Experimental Zoology Part A: Comparative Experimental Biology, 299A(2), 118–126. https://doi.org/10.1002/jez.a.10285
• Voituron, Y., Heulin, B., & Surget-Groba, Y. (2004). Comparison of the cold hardiness capacities of the oviparous and viviparous forms of Lacerta vivipara. Journal of Experimental Zoology, 301A(4), 367–373. https://doi.org/10.1002/jez.a.20042
• Voituron, Y., Joly, P., Eugène, M., & Barré, H. (2005). Freezing Tolerance of The European Water Frogs: The Good, The Bad, and The Ugly. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 288(6), R1563–R1570. https://doi.org/10.1152/ajpregu.00711.2004
• Voituron, Y., Paaschburg, L., Holmstrup, M., Barré, H., & Ramløv, H. (2009). Survival and Metabolism of Rana arvalis During Freezing. Journal of Comparative Physiology B, 179(2), 223–230. https://doi.org/10.1007/s00360-008-0307-3
• Wijeneyaka, S., Storey, K. (2016) The Role of DNA Methylation During Anoxia Tolerance in a Freshwater Turtle (Trachemys scripta elegans). Journal of Comparative Physiology B., 186(3), 333-342. https://doi.org/10.1007/s00360-016-0960-x
• Woods, C. P., Czenze, Z. J., & Brigham, R. M. (2019). The avian “hibernation” enigma: thermoregulatory patterns and roost choice of the common poorwill. Oecologia, 189(1), 47–53. https://doi.org/10.1007/s00442-018-4306-0
• Yoldaş, T. (2021). Anadolu Dağ Kurbağalarının Kriyobiyoloji Üzerine Araştırmalar (689754). Retrieved from https://tez.yok.gov.tr/UlusalTezMerkezi/giris.jsp.
• Yoldas, T., & Erismis, U. C. (2021). Response of Anatolian mountain frogs (Rana macrocnemis and Rana holtzi) to freezing, anoxia, and dehydration: Glucose as a cryoprotectant. Cryobiology, 98(November 2020), 96–102. https://doi.org/10.1016/j.cryobiol.2020.11.019