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Freeze tolerance in neotropical frogs: an intrageneric comparison using Pristimantis species of high elevation and medium elevation

Published online by Cambridge University Press:  08 July 2021

Juan Manuel Carvajalino-Fernández Open the ORCID record for Juan Manuel Carvajalino-Fernández [Opens in a new window] ,
Maria Argenis Bonilla Gomez ,
Liliana Giraldo-Gutierréz  and
Carlos Arturo Navas
Juan Manuel Carvajalino-Fernández*
Affiliation:
Laboratory of Adaptations to Extreme Environments and Global Change Biology, University College of Cundinamarca, Bogotá, Colombia Laboratory of Ecophysiology and Evolutionary Physiology, Department of Physiology, Institute of Bioscience, University of São Paulo, São Paulo, SP, Brazil Grupo de Investigación Biología de Organismos Tropicales, Departamento de Biología, Universidad Nacional de Colombia, Bogotá, Colombia
Maria Argenis Bonilla Gomez
Affiliation:
Grupo de Investigación Biología de Organismos Tropicales, Departamento de Biología, Universidad Nacional de Colombia, Bogotá, Colombia
Liliana Giraldo-Gutierréz
Affiliation:
Departamento de Química. Facultad de Ciencias. Universidad Nacional de Colombia. Bogotá, Colombia
Carlos Arturo Navas
Affiliation:
Laboratory of Ecophysiology and Evolutionary Physiology, Department of Physiology, Institute of Bioscience, University of São Paulo, São Paulo, SP, Brazil
*
Author for correspondence:*Juan Manuel Carvajalino-Fernández, Email: jcarvajalio@unicolmayor.edu.co
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Abstract

Paramos are high-elevation tropical Andean ecosystems above the tree line that display variable temperature and frequent freezing spells. Because a significant anuran community lives in this environment, physiological protection against freezing must characterise individuals in this community. Antifreeze protection has been studied in amphibians from other communities, and it is likely that Paramo anurans rely on the same underlying molecules that convey such protection to Nearctic species. However, given the pervasive presence of freezing spells in the Paramos year-round, the processes of activating protection mechanisms may differ from that of seasonal counterparts. Accordingly, this study investigated cryoprotection strategies in high-elevation tropical frogs, using as a model the terrestrial and nocturnal genus Pristimantis, specifically P. bogotensis, P. elegans and P. nervicus from Paramos, and the warm ecosystem counterparts P. insignitus, P. megalops and P. sanctaemartae. We focused on freeze tolerance and its relationship with glucose accumulation and ice formation. Under field conditions, the highest elevation P. nervicus exhibited higher glucose concentration at dawn compared to noon (1.7 ± 0.6 mmol/L versus 3.5 ± 1.32 mmol/L). Under experimental thermal freeze exposure for 2 hours between −2 and −4 ºC, the glucose concentration of the three Paramo species increased but physiological diversity was evident (P. nervicus 126%; P. bogotensis 100%; and P. elegans 55%). During this test, body ice formation was assessed calorimetrically. The species with the highest body ice formation was P. bogotensis (17% ± 5.37; maximum value: 63%; n = 8), followed by P. nervicus (5% ± 3.27; maximum value: 11%; n = 5) and P. elegans (0.34% ± 0.09; maximum value: 1%; n = 4). The study shows physiological diversity both within a genus and across the amphibian community around the freezing contour. Overall, Paramo species differ in freezing physiology from their low-elevation counterparts. Thus, climate shifts increasing freezing spells may affect the structure of communities in this zone.

Keywords

amphibiansglucosefreezingParamotropical forests
Type
Research Article
Information
Journal of Tropical Ecology , Volume 37 , Issue 3 , May 2021 , pp. 118 - 125
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Copyright
© The Author(s), 2021. Published by Cambridge University Press

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References

Baust, JG and Nishino, M (1991) Freezing Tolerance in the Goldenrod Gall Fly (Eurosta solidaginis). In Denlinger, DL and Lee, REJ (eds), Insects at Low Temperature. Boston: Springer, pp. 260–275.CrossRefGoogle Scholar
Bernal, MH and Lynch, JD (2008) Review and analysis of altitudinal distribution of the Andean anurans in Colombia. Zootaxa 1826, 1–25.CrossRefGoogle Scholar
Block, W, Wharton, D and Sinclair, BJ (1998) Cold tolerance of a New Zealand alpine cockroach, Celatoblatta quinquemaculata (Dictyoptera, Blattidae). Physiological Entomology 23, 1–6.CrossRefGoogle Scholar
Cabrera, H (1996) Temperaturas bajas y límites altitudinales en ecosistemas de plantas superiores: respuestas de las especies al frío en montañas tropicales y subtropicales (Low temperatures and altitude limits in higher plant ecosystems: species’ responses to the cold in tropical and sub-tropical mountains). Revista Chilena de Historia Natural 69, 309–320.Google Scholar
Carvajalino-Fernández, JM, Bonilla Gomez, MA and Navas, CA (2011) Freezing Risk in Tropical High-Elevation Anurans: An Assessment Based on the Andean Frog Pristimantis nervicus (Strobomantidae). South American Journal of Herpetology 6, 73–78.CrossRefGoogle Scholar
Carvajalino-Fernández, JM, Saboya-Acosta, LP, Padilla, C, Escárraga Fajardo, MJ and Porras, MF (2012) New records of the harlequin frog Atelopus nahumae Ruíz-Carranza, Ardila-Robayo y Hernández-Camacho, 1994, in the Sierra Nevada de Santa Marta (Colombia), with notes of its distribution. Herpetozoa 24, 121–126.Google Scholar
Clausen, D and Costanzo, J (1990) A simple moder for estimating the ice content of freezing ectotherms. Journal of Thermal Biology 15, 223–231.CrossRefGoogle Scholar
Costanzo, J, Lee, R Jr and Wright, M (1991) Effect of cooling rate on the survival of frozen wood frogs, Rana sylvatica. Journal of Comparative Physiology B 161, 225–229.CrossRefGoogle ScholarPubMed
Costanzo, JP and Lee, RE (1993) Cryoprotectant production capacity of the freeze-tolerant wood frog, Rana sylvatica. Canadian Journal of Zoology 71, 71–75.CrossRefGoogle Scholar
Costanzo, JP and Lee, RE (2013) Avoidance and tolerance of freezing in ectothermic vertebrates. The Journal of Experimental Biology 216, 1961–1967.CrossRefGoogle ScholarPubMed
Costanzo, JP, Lee, RE and Lortz, PH (1993) Glucose concentration regulates freeze tolerance in the wood frog Rana sylvatica. The Journal of Experimental Biology 181, 245–255.CrossRefGoogle ScholarPubMed
Davenport, J (John) (1992) Animal life at low temperature. London: Chapman & Hall.CrossRefGoogle Scholar
Dobson, RT (2005) Thermal modelling of a night sky radiation cooling system. Journal of Energy in Southern Africa 16, 20–31.CrossRefGoogle Scholar
Farke, H, Riemann, F and Schrage, M (1984) High freezing tolerance of marine nematodes from intertidal sediments of the German Bight. Nematologica 30, 452–456.Google Scholar
Hawes, TC, Worland, MR and Bale, JS (2010) Cryobiology Freezing in the Antarctic limpet, Nacella concinna q. Cryobiology 61, 128–132.CrossRefGoogle Scholar
Heinicke, MP, Duellman, WE and Hedges, SB (2007) Major Caribbean and Central American frog faunas originated by ancient oceanic dispersal. Proceedings of the National Academy of Sciences of the United States of America 104, 10092–10097.CrossRefGoogle ScholarPubMed
Hernández-Camacho, J and Sánchez-Páez, H (1992) Biomas terrestres de Colombia. In Halffter G (ed.), 1992. La Diversidad Biológica de Iberoamerica I. Programa Iberoamericano de Ciencia y Tecnología Para EL Desarrollo. Xalapa, Mexico.Google Scholar
Kassambara, A (2020) Ggpubr: ‘ggplot2’ Based Publication Ready Plots. R package version 0.4.0. https://CRAN.R-project.org/package=ggpubr Google Scholar
Kassambara, A (2021). Rstatix: Pipe-Friendly Framework for Basic Statistical Tests. R package version 0.7.0. https://CRAN.R-project.org/package=rstatix Google Scholar
Kiss, AJ, Muir, TJ, Lee, RE and Costanzo, JP (2011) Seasonal variation in the hepatoproteome of the dehydrationand freeze-tolerant wood frog, Rana sylvatica. International Journal of Molecular Sciences 12, 8406–8414.CrossRefGoogle ScholarPubMed
Larson, DJ and Barnes, BM (2016) Cryoprotectant Production in Freeze-Tolerant Wood Frogs Is Augmented by Multiple Freeze-Thaw Cycles. Physiological and Biochemical Zoology 89, 340–346.CrossRefGoogle ScholarPubMed
Larson, DJ, Middle, L, Vu, H, Zhang, W, Serianni, AS, Duman, J and Barnes, BM (2014) Wood frog adaptations to overwintering in Alaska: new limits to freezing tolerance. The Journal of Experimental Biology 217, 2193–2200.Google ScholarPubMed
Layne, JR (1999) Freeze tolerance and cryoprotectant mobilization in the gray treefrog (Hyla versicolor). Journal of Experimental Zoology 283, 221–225.3.0.CO;2-Q>CrossRefGoogle Scholar
Layne, JR and Jones, AL (2001) Freeze tolerance in the gray treefrog: cryoprotectant mobilization and organ dehydration. The Journal of Experimental Zoology 290, 1–5.CrossRefGoogle ScholarPubMed
Layne, JR and Lee, RE (1995) Adaptations of frogs to survive freezing. Climate Research. 5, 53–59.Google Scholar
Lüddecke, H and Sanchez, OR (2002) Are Tropical Highland Frog Calls Cold-Adapted ? The Case of the Andean Frog Hyla labialis. Biotropica 34, 281–288.CrossRefGoogle Scholar
Madriñan, S (2004) Flora ilustrada del Páramo Chingaza : guía de campo de plantas comunes. First edition. University of the Andes Press., Bogotá. Colombia.Google Scholar
Marchand, PJ (1996) Life in the Cold: An Introduction to Winter Ecology. University Press of New England.Google Scholar
Moalem, S, Storey, KB, Percy, ME, Peros, MC and Perl, DP (2005) The sweet thing about Type 1 diabetes: A cryoprotective evolutionary adaptation. Medical Hypotheses 65, 8–16.CrossRefGoogle ScholarPubMed
Navas, C (1996a) Implications of microhabitat selection and patterns of activity on the thermal ecology of high elevation neotropical anurans. Oecologia 108, 617–626.CrossRefGoogle ScholarPubMed
Navas, C (1996b) Thermal Dependency of Field Locomotor and Vocal Performance of High-Elevation Anurans in the Tropical Andes. Journal of Herpetology 30, 478.CrossRefGoogle Scholar
Navas, C (1996c) The Effect of Temperature on the Vocal Activity of Tropical Anurans: A Comparison of High and Low-Elevation Species. Journal of Herpetology 30, 488.CrossRefGoogle Scholar
Navas, C (1997) Thermal extremes at high elevations in the Andes: physiological ecology of frogs. Journal of Thermal Biology 22: 467–477.CrossRefGoogle Scholar
Navas, C (2003) Herpetological diversity along Andean elevational gradients: links with physiological ecology and evolutionary physiology. Comparative Biochemistry and Physiology A 133, 469–485.CrossRefGoogle Scholar
Navas, CA, Carvajalino-Fernández, JM, Saboyá-Acosta, LP, Rueda-Solano, LA and Carvajalino-Fernández, MA (2013) The body temperature of active amphibians along a tropical elevation gradient: patterns of mean and variance and inference from environmental data. Functional Ecology 27, 1145–1154.CrossRefGoogle Scholar
Rexer-Huber, KMJ, Bishop, PJ and Wharton, D (2011) Skin ice nucleators and glycerol in the freezing-tolerant frog Litoria ewingii. Journal of Comparative Physiology B 181, 781–792.CrossRefGoogle ScholarPubMed
Rexer-Huber, KMJ, Bishop, PJ and Wharton, D (2015) Field ecology of freezing: Linking microhabitat use with freezing tolerance in Litoria ewingii Austral Ecology 40 (8), 933–940.CrossRefGoogle Scholar
Robinson, D, Hayes, A and Couch, S (2021) Broom: Convert Statistical Objects into Tidy Tibbles. R package version 0.7.6. https://CRAN.R-project.org/package=broom Google Scholar
Rueda-Solano, LAR, Navas, CA, Carvajalino-Fernández, JM and Amézquita, A (2016) Thermal ecology of montane Atelopus (Anura: Bufonidae): A study of intrageneric diversity. Journal of Thermal Biology 58, 91–98.CrossRefGoogle ScholarPubMed
Sandercock, B, Martin, K and Hannon, S (2005) Life history strategies in extreme environments: comparative demography of arctic and alpine ptarmigan. Ecology 86, 2176–2186.CrossRefGoogle Scholar
Sarmiento, G (1986). Ecological features of climate in high tropical mountains. In: Vuilleumier, F. & Monasterio, M. High altitude tropical biogeography. Oxford University Press, New Cork, United Kingdom. Pages 11–46.Google Scholar
Schmid, W (1982) Survival of Frogs in Low Temperature. Science 215, 697–698.CrossRefGoogle ScholarPubMed
Sinclair, BJ and Chown, SL (2005) Climatic variability and hemispheric differences in insect cold tolerance: Support from southern Africa. Functional Ecology 19, 214–221.CrossRefGoogle Scholar
Sinclair, BJ, Stinziano, JR, Williams, CM, Macmillan, HA, Marshall, KE and Storey, KB (2013) Real-time measurement of metabolic rate during freezing and thawing of the wood frog, Rana sylvatica: implications for overwinter energy use. The Journal of Experimental Biology 216, 292–302.CrossRefGoogle ScholarPubMed
Sinclair, BJ, Worland, MR and Wharton, DA (1999) Ice nucleation and freezing tolerance in New Zealand alpine and lowland weta, Hemideina spp. (Orthoptera; Stenopelmatidae). Physiological Entomology 24, 56–63.CrossRefGoogle Scholar
Storey, K.B. (1997). Organic solutes in freezing tolerance. Comparative biochemistry and physiology. Part A, Physiology 117, 319–326.CrossRefGoogle ScholarPubMed
Storey, KB and Storey, JM (1987) Persistence of Freeze Tolerance in Terrestrially Hibernating Frogs after Spring Emergence Persistence of Freeze Tolerance in Terrestrially Hibernating Frogs after Spring Emergence. Copeia 3, 720–726.CrossRefGoogle Scholar
Storey, KB and Storey, JM (1992) Natural freeze tolerance in ectothermic vertebrates. Annual Review of Physiology 54, 619–637.CrossRefGoogle ScholarPubMed
Storey, KB and Storey, JM (1996) Natural freezing survival in animals. Annual Review of Ecology and Systematics 27, 365–386.CrossRefGoogle Scholar
Storey, KB and Storey, JM (2017) Molecular Physiology of Freeze Tolerance in Vertebrates. Physiological Review 97, 623–665.Google Scholar
Theede, H, Scheneppenheim, R and Beress, L (1976) Frostschutzglykoproteine bei Mytilus edulis?. Marine Biology 136, 183–189.CrossRefGoogle Scholar
Vargas, O and Pedraza, P (2004) Parque Nacional Natural Chingaza. Bogotá: Gente Nueva Editorial.Google Scholar
Voituron, Y, Barré, H, Ramløv, H and Douady, CJ (2009a) Freeze tolerance evolution among anurans: Frequency and timing of appearance. Cryobiology 58, 241–247.CrossRefGoogle ScholarPubMed
Voituron, Y, Paaschburg, L, Holmstrup, M, Barré, H and Ramlov, H (2009b) Survival and metabolism of Rana arvalis during freezing. Journal of Comparative Physiology B 179, 223–230.CrossRefGoogle ScholarPubMed
Waller, C, Worland, M, Convey, P and Barnes, D (2006) Ecophysiological strategies of Antarctic intertidal invertebrates faced with freezing stress. Polar Biology 29, 1077.CrossRefGoogle Scholar
Wickham, H (2016). ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag New York. ISBN 978-3-319-24277-4, https://ggplot2.tidyverse.org.CrossRefGoogle Scholar
Wickham, H, Averick, M, Bryan, J, Chang, W, McGowan, LD, François, R, Grolemund, G, Hayes, A, Henry, L, Hester, J, Kuhn, M, Pedersen, TL, Miller, E, Bache, SM, Müller, K, Ooms, J, Robinson, D, Seidel, DP, Spinu, V, Takahashi, K, Vaughan, D, Wilke, C, Woo, K and Yutani, H (2019) “Welcome to the tidyverse.” Journal of Open Source Software 4(43), 1686.CrossRefGoogle Scholar