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Alday Echechipia, E., Pérez López, U., Fernández Marín, B., Puértolas Simón, J., González Ródrigez, Águeda M., Martín Esquivel, J. L., & García Plazaola, J. I. Cold Air Pools (CAPs) as Natural Freezers for the Study of Plant Responses to Low Temperatures. Plant Ecophysiology. 2025. doi: https://doi.org/10.53941/plantecophys.2025.100006

Review

Cold Air Pools (CAPs) as Natural Freezers for the Study of Plant Responses to Low Temperatures

Enara Alday 1,*, Usue Pérez-López 1, Beatriz Fernández-Marín 1,2, Jaime Puértolas 2, Águeda M. González-Rodríguez 2, José Luis Martin Esquivel 3 and José Ignacio García-Plazaola 1

1 Department of Plant Biology and Ecology, Faculty of Science and Technology, University of the Basque Country (UPV/EHU), Leioa 48940, Spain

2 Department of Botany, Ecology and Plant Physiology, Facultad de Farmacia, University of La Laguna, La Laguna 38200, Spain

3 Teide National Park, La Orotava, Tenerife, Islas Canarias 38300, Spain

* Correspondence: enara.alday@ehu.eus

Received: 18 October 2024; Revised: 26 March 2025; Accepted: 10 April 2025; Published: 16 April 2025

Abstract: The stratification of cold air is a phenomenon that typically occurs under certain topographic (closed ground depressions) and atmospheric conditions (stability and nocturnal radiative cooling). Under such conditions the drainage of the heavier cold air from the higher elevations causes its accumulation for days or weeks in the bottom of these depressions, leading temperatures to dramatically decrease and to decouple from regional climatic conditions. These particular locations which are frequent in karstic, volcanic and glacial landscapes, have been proposed to act as microrefugia of biodiversity in the context of climate warming. The existence of these cold air pools (CAPs) has been reported worldwide, and their biotic communities differ from equivalent sites out of these locations. However, there is an almost complete absence of ecophysiological studies concerning plant communities inhabiting CAPs. Thus, one of the objectives of this review is to hypothesize the effects of these specific conditions on the biology of the soil and the manner in which these plants should respond to such particular environmental conditions. Furthermore, given that temperature can decrease dramatically over short distances inside CAPs, in the present review we also propose their use as natural freezers for the study of plant responses to low temperatures. 

Keywords:

Cold Air Pool (CAP) microrefugia low temperature plant ecophysiology freezing-tolerance

References

  1. Bátori Z, Valkó O, Vojtkó A, Tölgyesi C, Farkas T, Frei K, Hábenczyus AA, Tóth Á, Li G, & Rádai Z. (2023). Environmental Heterogeneity Increases the Conservation Value of Small Natural Features in Karst Landscapes. Science of the Total Environment, 872, 162120. https://doi.org/10.1016/j.scitotenv.2023.162120
  2. Bátori Z, Vojtkó A, Farkas T, Szabó A, Havadtoi K, Vojtkó AE, Tölgyesi C, Cseh V, Erdos L, & Maák IE. (2017). Large- and Small-Scale Environmental Factors Drive Distributions of Cool-Adapted Plants in Karstic Microrefugia. Annals of Botany, 119(2), 301–309. https://doi.org/10.1093/aob/mcw233
  3. Ben-Haj-Salah H, & Tardieu F. (1995). Temperature Affects Expansion Rate of Maize Leaves without Change in Spatial Distribution of Cell Length (Analysis of the Coordination between Cell Division and Cell Expansion). Plant Physiology, 109(3), 861–870. https://doi.org/10.1104/pp.109.3.861
  4. Blennow K, & Lindkvist L. (2000). Models of Low Temperature and High Irradiance and Their Application to Explaining the Risk of Seedling Mortality. Forest Ecology and Management, 135(1–3), 289–301. https://doi.org/10.1016/S0378-1127(00)00287-5
  5. Blum, A. (2015). Stress, Strain, Signaling, and Adaptation-Not Just a Matter of Definition. Journal of Experimental Botany, 67(3), 562–565. https://doi.org/10.1093/jxb/erv497
  6. Bredow M, & Walker VK. Ice-Binding Proteins in Plants. Frontiers in Plant Science 2017, 8, 325466. https://doi.org/10.3389/fpls.2017.02153
  7. Brooks PD, Williams MW, & Schmidt SK. (1998). Inorganic Nitrogen and Microbial Biomass Dynamics before and during Spring Snowmelt. Biogeochemistry, 43, 1–15. https://doi.org/10.1023/A:1005947511910
  8. Buchner O, Neuner G, & Ball M. (2011). Winter Frost Resistance of Pinus Cembra Measured in situ at the Alpine Timberline as Affected by Temperature Conditions. Tree Physiology, 31(11), 1217–1227. https://doi.org/10.1093/treephys/tpr103
  9. Buchner O, Stoll M, Karadar M, Kranner I, & Neuner G. (2015). Application of Heat Stress in situ Demonstrates a Protective Role of Irradiation on Photosynthetic Performance in Alpine Plants. Plant, Cell & Environment, 38(4), 812–826. https://doi.org/10.1111/pce.12455
  10. Cabrera HM, Rada F, & Cavieres L. (1998). Effects of Temperature on Photosynthesis of Two Morphologically Contrasting Plant Species along an Altitudinal Gradient in the Tropical High Andes. Oecologia, 114, 145–152. https://doi.org/10.1007/s004420050430
  11. Chung U, Seo HH, Hwang KH, Hwang BS, Choi J, Lee JT, & Yun JI. (2006). Minimum Temperature Mapping over Complex Terrain by Estimating Cold Air Accumulation Potential. Agricultural and Forest Meteorology, 137(1–2), 15–24. https://doi.org/10.1016/j.agrformet.2005.12.011
  12. Cordeiro AMR, Orenlas A, & Silva DD. (2023). The importance of topography in the formation of cold‑air pooling in urban spaces. The example of the city of Coimbra (Portugal). Theoretical and Applied Climatology 152, 227–239. https://doi.org/10.1007/s00704-023-04401-8
  13. Cruz-Paredes C, Tájmel D, & Rousk J. (2021). Can Moisture Affect Temperature Dependences of Microbial Growth and Respiration? Soil Biology and Biochemistry, 156, 108223. https://doi.org/10.1016/j.soilbio.2021.108223
  14. Curtis JA, Flint LE, Flint AL, Lundquist JD, Hudgens B, Boydston EE, & Young JK. (2014). Incorporating Cold-Air Pooling into Downscaled Climate Models Increases Potential Refugia for Snow-Dependent Species within the Sierra Nevada Ecoregion, CA. PLoS ONE, 9, e106984. https://doi.org/10.1371/journal.pone.0106984
  15. Daly C, Smith JW, Smith JI, & McKane RB. (2007). High-Resolution Spatial Modeling of Daily Weather Elements for a Catchment in the Oregon Cascade Mountains, United States. Journal of Applied Meteorology and Climatology, 46(10), 1565–1586. https://doi.org/10.1175/JAM2548.1
  16. Demidchik V, Straltsova D, Medvedev SS, Pozhvanov GA, Sokolik A, & Yurin V. (2014). Stress-Induced Electrolyte Leakage: The Role of K+-Permeable Channels and Involvement in Programmed Cell Death and Metabolic Adjustment. Journal of Experimental Botany, 65(5), 1259–1270. https://doi.org/10.1093/jxb/eru004
  17. Duker R, Cowling RM, van der Vyver ML, & Potts AJ. (2020). Site Selection for Subtropical Thicket Restoration: Mapping Cold-Air Pooling in the South African Sub-Escarpment Lowlands. PeerJ, 8, e8980. https://doi.org/10.7717/peerj.8980
  18. Edwards AC, Scalenghe R, & Freppaz M. (2007). Changes in the Seasonal Snow Cover of Alpine Regions and Its Effect on Soil Processes: A Review. Quaternary International, 162–163, 172–181. https://doi.org/10.1016/j.quaint.2006.10.027
  19. Ensminger I, Busch F, & Huner NPA. (2005). Photostasis and Cold Acclimation: Sensing Low Temperature through Photosynthesis. Physiologia Plantarum, 126(1), 28–44. https://doi.org/10.1111/j.1399-3054.2006.00627.x
  20. Esteban R, Fernández-Marín B, Becerril JM, & García-Plazaola JI. (2008). Photoprotective Implications of Leaf Variegation in E. dens-canis L. and P. officinalis L. Journal of Plant Physiology, 165(12), 1255–1263. https://doi.org/10.1016/j.jplph.2007.07.024
  21. Frei K, Vojtkó A, Farkas T, Erdős L, Barta K, E-Vojtkó A, Tölgyesi C, & Bátori Z. (2023). Topographic Depressions Can Provide Climate and Resource Microrefugia for Biodiversity. iScience, 26(11), 108202. https://doi.org/10.1016/j.isci.2023.108202
  22. García-Plazaola JI, Hernández A, Olano JM, & Becerril JM. (2003). The Operation of the Lutein Epoxide Cycle Correlates with Energy Dissipation. Functional Plant Biology, 30(3), 319–324. https://doi.org/10.1071/FP02224
  23. Giovagnoli L, & Tasinazzo S. (2014). The Dolina System Vegetation of the Northern Glacio-Karst Sector of the Asiago Plateau (Venetian Prealps-NE Italy). Plant Sociology, 51, 83–116. https://doi.org/10.7338/pls2014512/06
  24. Grossiord C, Buckley TN, Cernusak LA, Novick KA, Poulter B, Siegwolf RTW, Sperry JS, & McDowell NG. (2020). Plant responses to rising vapor pressure deficit. New Phytologist, 226(6), 1550–1566. https://doi.org/10.1111/nph.16485
  25. Hall SJ, Maurer G, Hoch SW, Taylor R, & Bowling DR. (2014). Wasatch Impacts of anthropogenic emissions and cold air pools on urban to montane gradients of snowpack ion concentrations in the Wasatch Mountains, Utah. Atmospheric Environment 98, 231–241. https://doi.org/10.1016/j.atmosenv.2014.08.076
  26. Halloy S, & González JA. (1993). An Inverse Relation between Frost Survival and Atmospheric Pressure. Arctic, Antarctic, and Alpine Research, 25(2), 117–123. https://doi.org/10.1080/00040851.1993.12002991
  27. Hartman K, & Tringe SG. (2019). Interactions between Plants and Soil Shaping the Root Microbiome under Abiotic Stress. Biochemical Journal, 476(19), 2705–2724. https://doi.org/10.1042/BCJ20180615
  28. Hudson MA, & Idle DB. (1962). The Formation of Plant Tissues. Planta, 57, 718–730. https://doi.org/10.1007/BF01930351
  29. Hussain HA, Hussain S, Khaliq A, Ashraf U, Anjum SA, Men S, & Wang L. (2018). Chilling and Drought Stresses in Crop Plants: Implications, Cross Talk, and Potential Management Opportunities. Frontiers in Plant Science, 9, 393. https://doi.org/10.3389/fpls.2018.00393
  30. Iglesisas Noromet. (2021, July 1). Asociación Meorológica Del Noroeste Peninsular. Available online: https://noromet.org/.
  31. Iijima Y, & Shinoda M. (2002). The Influence of Seasonally Varying Atmospheric Characteristics on the Intensity of Nocturnal Cooling in a High Mountain Hollow. Journal of Applied Meteorology, 41(7), 734–743. https://doi.org/10.1175/1520-0450(2002)041<0734:TIOSVA>2.0.CO;2
  32. John A, Olden JD, Oldfather MF, Kling MM, & Ackerly DD. (2024). Topography Influences Diurnal and Seasonal Microclimate Fluctuations in Hilly Terrain Environments of Coastal California. PLoS ONE, 19(3), e0300378. https://doi.org/10.1371/journal.pone.0300378
  33. Körner C. (2021). Alpine Plant Life: Functional Plant Ecology of High Mountain Ecosystems. Springer International Publishing.
  34. Körner C, & Miglietta F. (1994). Long Term Effects of Naturally Elevated CO2 on Mediterranean Grassland and Forest Trees. Oecologia, 99, 343–351. https://doi.org/10.1007/BF00627748
  35. Kusunoki K, & Ueno K. (2022). Development of a Nocturnal Temperature Inversion in a Small Basin Associated with Leaf Area Ratio Changes on the Mountain Slopes in Central Japan. Journal of the Meteorological Society of Japan, 100(6), 913–926. https://doi.org/10.2151/jmsj.2022-047
  36. Larcher W. (2003). Physiological Plant Ecology. Ecophysiology and Stress Physiology of Functional Groups (4th ed.). Oxford University Press.
  37. Lazar VR. (1996). Geländeklimastiche Untersuchungen Auf Teneriffa (Insbesondere in Den Cañadas). Wetter und Leben, 48, 217–240.
  38. Lembrechts JJ, Aalto J, Ashcroft MB, De Frenne P, Kopecký M, Lenoir J, Luoto M, Maclean IMD, Roupsard O, Fuentes-Lillo E, García RA, Pellissier A, Pitteloud G, Alatalo JM,…& Nijs I. (2020). SoilTemp: A Global Database of near-Surface Temperature. Global Change Biology, 26(11), 6616–6629. https://doi.org/10.1111/gcb.15123
  39. Lipson DA, Raab TK, Schmidt SK, & Monson RK. (1999). Variation in Competitive Abilities of Plants and Microbes for Specific Amino Acids. Biology and Fertility of Soils, 29, 257–261. https://doi.org/10.1007/s003740050550
  40. López Díez A, Antequera PJD, Pacheco JD, Esquivel JLM, & Gómez MVM. (2022). Rasgos Climáticos Del Parque Nacional Del Teide. Singularidad y Diversidad. In MD Villalonga & JLM Esquivel (Eds.), Ciencia en el Parque Nacional del Teide (pp. 119–138). Publicaciones Turquesa S.L.
  41. Lundquist JD, Pepin N, & Rochford C. (2008). Automated Algorithm for Mapping Regions of Cold-Air Pooling in Complex Terrain. Journal of Geophysical Research: Atmospheres, 113(D22). https://doi.org/10.1029/2008JD009879
  42. Manzoni S, Ding Y, Warren C, Banfield C.C, Dippold MA, & Mason-Jones K. (2021). Intracellular Storage Reduces Stoichiometric Imbalances in Soil Microbial Biomass–A Theoretical Exploration. Frontiers in Ecology and Evolution, 9, 714134. https://doi.org/10.3389/fevo.2021.714134
  43. Martz F, Vuosku J, Ovaskainen A, Stark S, & Rautio P. (2016). The Snow Must Go on: Ground Ice Encasement, Snow Compaction and Absence of Snow Differently Cause Soil Hypoxia, CO2 Accumulation and Tree Seedling Damage in Boreal Forest. PLoS ONE, 11, e0156620. https://doi.org/10.1371/journal.pone.0156620
  44. Mason-Jones K, Robinson SL, Veen GF, Manzoni S, & van der Putten WH. (2022). Microbial Storage and Its Implications for Soil Ecology. The ISME Journal, 16, 617–629. https://doi.org/10.1038/s41396-021-01110-w
  45. Matusick G, Ruthrof KX, Brouwers NC, & Hardy GSJ. (2014). Topography Influences the Distribution of Autumn Frost Damage on Trees in a Mediterranean-Type Eucalyptus Forest. Trees, 28, 1449–1462. https://doi.org/10.1007/s00468-014-1048-4
  46. McCaffrey K, Wilczak JM, Bianco L, Grimit E, Sharp J, Banta R, Friedrich K, Fernando HJS, Krishnamurthy R, Leo LS, & Muradyan P. (2019). Identification and Characterization of Persistent Cold Pool Events from Temperature and Wind Profilers in the Columbia River Basin. Journal of Applied Meteorology and Climatology, 58(12), 2533–2551. https://doi.org/10.1175/JAMC-D-19-0046.1
  47. Miglietta F. (2006). Natural CO2 Springs in Italy: A Resource for Examining Long-Term Response of Vegetation to Rising Atmospheric CO2 Concentrations. Plant Cell Environment, 16(7), 873–878. https://doi.org/10.1111/j.1365-3040.1993.tb00510.x
  48. Ninyerola M, Pons X, & Roure JM. (2000). A methodological approach of climatological modelling of air temperature and precipitation through GIS techniques. International Journal of Climatology, 20(14), 1823–1841. https://doi.org/10.1002/1097-0088(20001130)20:14<1823::AID-JOC566>3.0.CO;2-B
  49. Novick KA, Oishi AC, & Miniat CF. (2016). Cold Air Drainage Flows Subsidize Montane Valley Ecosystem Productivity. Global Change Biology, 22(12), 4014–4027. https://doi.org/10.1111/gcb.13320
  50. Pastore MA, Classen AT, D’Amato AW, English ME, Rand K, Foster JR, & Adair EC. (2024). Frequent and Strong Cold-Air Pooling Drives Temperate Forest Composition. Ecology and Evolution, 14(4), e11126. https://doi.org/10.1002/ece3.11126
  51. Pastore MA, Classen AT, D’Amato AW, Foster JR & Adair EC. (2022). Cold-Air Pools as Microrefugia for Ecosystem Functions in the Face of Climate Change. Ecology, 103(8), e3717. https://doi.org/10.1002/ecy.3717
  52. Patsiou TS, Conti E, Theodoridis S, & Randin CF. (2017). The Contribution of Cold Air Pooling to the Distribution of a Rare and Endemic Plant of the Alps. Plant Ecology & Diversity, 10(1), 29–42. https://doi.org/10.1080/17550874.2017.1302997
  53. Pietikäinen J, Pettersson M, & Bååth E. (2005). Comparison of Temperature Effects on Soil Respiration and Bacterial and Fungal Growth Rates. FEMS Microbiology Ecology, 52(1), 49–58. https://doi.org/10.1016/j.femsec.2004.10.002
  54. Robson TM, Aphalo PJ, Banaś AK, Barnes PW, Brelsford CC, Jenkins GI, Kotilainen TK, Łabuz J, Martínez-Abaigar J, & Morales LO. (2019). A Perspective on Ecologically Relevant Plant-UV Research and Its Practical Application. In Proceedings of the Photochemical and Photobiological Sciences. Photochemical & Photobiological Sciences, 18, 970–988.
  55. Sakai, A, & Larcher, W. (1987). Frost Survival of Plants. Responses and Adaptation to Freezing Stress. Springer-Verlag.
  56. Schär C, Vidale PL, Lüthi D, Frei C, Häberli C, Liniger MA, & Appenzeller C. (2004). The Role of Increasing Temperature Variability in European Summer Heatwaves. Nature, 427, 332–336. https://doi.org/10.1038/nature02300
  57. Schnecker J, Spiegel F, Li Y, Richter A, Sandén T, Spiegel H, Zechmeister-Boltenstern S, & Fuchslueger L. (2023). Microbial Responses to Soil Cooling Might Explain Increases in Microbial Biomass in Winter. Biogeochemistry, 164, 521–535. https://doi.org/10.1007/s10533-023-01050-x
  58. Schubert M, Humphreys AM, Lindberg CL, Preston JC, & Fjellheim S. (2020). To Coldly Go Where No Grass Has Gone before: A Multidisciplinary Review of Cold Adaptation in Poaceae. Annual Plant Reviews Online, 3(4), 523–562. https://doi.org/10.1002/9781119312994.apr0739
  59. Soler MR, Infante C, Buenestado P, & Mahrt, L. (2002). Observation of Nocturnal Drainage Flow in a Shallow Gully. Boundary-Layer Meteorology, 105, 253–273. https://doi.org/10.1023/A:1019910622806
  60. Sun X, Ivey CE, Baker KR, Nenes A, Lareau NP, & Holmes HA. (2021). Salt Lake Confronting Uncertainties of Simulated Air Pollution Concentrations during Persistent Cold Air Pool Events in the Salt Lake Valley, Utah Environmental Science Technology 55(22), 15072–15081. https://doi.org/10.1021/acs.est.1c05467
  61. Thomashow MF. (1999). Plant cold acclimation: Freezing Tolerance Genes and Regulatory Mechanisms. Annual Review of Plant Biology, 50, 571–599. https://doi.org/10.1146/annurev.arplant.50.1.571
  62. Verhoeven A, García-Plazaola JI, & Fernández-Marín B. (2018). Shared Mechanisms of Photoprotection in Photosynthetic Organisms Tolerant to Desiccation or to Low Temperature. Environmental and Experimental Botany, 154, 66–79. https://doi.org/10.1016/j.envexpbot.2017.09.012
  63. Vosper SB, Hughes JK, Lock AP, Sheridan PF, Ross AN, Jemmett-Smith B, & Brown AR. (2014). Cold-Pool Formation in a Narrow Valley. Quarterly Journal of the Royal Meteorological Society, 140(679), 699–714. https://doi.org/10.1002/qj.2160
  64. Vuosku J, Martz F, Hallikainen V, & Rautio P. (2022). Changing Winter Climate and Snow Conditions Induce Various Transcriptional Stress Responses in Scots Pine Seedlings. Frontiers in Plant Science, 13, 1050903. https://doi.org/10.3389/fpls.2022.1050903
  65. Ward SE, Schulze M, & Roy B. (2018). A Long-Term Perspective on Microclimate and Spring Plant Phenology in the Western Cascades. Ecosphere, 9(10), e02451. https://doi.org/10.1002/ecs2.2451
  66. Whittaker RH. (1975). Communities and Ecosystems (2nd ed.). MacMillan Publishing Co.
  67. Wipf S, Sommerkorn M, Stutter MI, Wubs ERJ, & Van Der Wal R. (2015). Snow Cover, Freeze-Thaw, and the Retention of Nutrients in an Oceanic Mountain Ecosystem. Ecosphere, 6(10), 1–16. https://doi.org/10.1890/ES15-00099.1