Range limits of forest species are frequently imposed by spatial gradients in climatic variables. Tolerance to maximum and minimum temperatures, including short-term extremes, and tolerance to desiccation are crucial limiting factors for plant survival and often appear interrelated (Box 1995; Choat et al. 2018). Increasing temperatures, more frequent and extreme droughts and late frost events associated with global climate change will affect the dynamics of forest ecosystems and have the potential to dramatically increase plant mortality and accelerate species range shifts if plants are not able to adapt in situ to the novel climate regimes (Parmesan 2006; Choat et al., 2012). This is particularly important at species range edges, where climatic conditions may not be sufficient to impose mortality on individuals directly, but trees experience greater physiological stress, which influences such factors as dispersal, habitat selection, and subsequent reproductive fitness (Parmesan 2006). In such marginal situations, where gene flow may be also restricted (López de Heredia et al. 2010), the effectiveness of adjustment through natural selection is limited resulting in increased vulnerability to extreme climatic events and to a higher risk of mortality of trees.
Tree responses to drought and frost have been extensively studied at many scales from ecophysiology to molecular biology across a large range of species inhabiting diverse biomes (Sakai and Larcher 1987; Bréda et al. 2006). Avoiding dehydration of tissues to maintain cellular viability and function is at the basis of the plant strategy to deal with both constraints as shown by Charrier et al. (2020). These authors go one step further and discuss the impact of the interaction of drought and frost on tree water status and carbon metabolism with special emphasis on the temporal context. Plants from temperate and boreal regions show changes in their resistance to freezing temperature throughout the year (Bower and Aitken 2006) and xylem becomes more resistant to cavitation with cambial age (Rodríguez-Zaccaro et al. 2019). Including timing in this framework involves incorporating phenology. This will be a fundamental step to model species distribution limits in the face of climate change since most observations of climate-change responses have involved alterations of species’ phenologies (Parmesan et al. 2006). For example, the onset of the growing season of trees in temperate Europe is 2.3 days ahead per decade during the last 40 years (Parmesan et al. 2006). Moreover, some studies have shown that climatic constraints limit species distribution mainly because of their impact in phenology rather than their impact on drought and frost mortality (Morin et al. 2007). However, longer growing seasons along with more frequent extreme events increase the probability of long-lived organisms such as trees to experience frosts and drought during the same growing season or one of them after uncompleted recovery of the other in some latitudes. Over the last decade much attention has been devoted to the recovery of growth and ecological function after stressful events (Lloret et al. 2011). Some dendroecological studies have shown for example that resilience to extreme droughts might be constrained by having experienced more frequent droughts, thus exceeding the potential for acclimation of the tree (Bose et al. 2020). Drought can result in chronic hydraulic impairment which can last moths to years (Anderegg et al. 2015) and for some species also in cavitation fatigue, i.e. a progressive increase in vulnerability to cavitation (Hacke et al. 2001), thus increasing vulnerability to subsequent drought and frost events.
Models have proved to be useful tools for synthetizing and integrating climate and soil properties with key functional traits in order to determine desiccation dynamics, carbon metabolism and plant survival during drought of frost (Martin-StPaul et al., 2017; Charrier et al. 2018; Blackman et al., 2019). However, models are currently limited by gaps in our understanding of the fundamental physiological mechanisms that constrain species ranges. Most common approaches to studying species range shifts are related to climatic niches and overlook the processes and traits involved in drought or frost tolerance (Cheaib et al. 2012). Process-based models based on plant hydraulics seem promising providing the link between environmental cues and plant responses, although disregarding carbon metabolism will not give us predictive understanding of system changes such as those due to climate fluctuations (Mackay et al. 2015). New modeling approaches need to be developed not only for better drought prediction performance but for the interaction of drought with other factors. Charrier et al. (2020) offer a framework for improving process-based models with the aim to provide better prediction of carbon and water economy, organ development and ultimately species distribution limits in the face of warmer winters and more frequent winter droughts at high altitudes and late frosts events.

References

Anderegg WR, Schwalm C, Biondi F, Camarero JJ, Koch G, Litvak M, Ogle K, Shaw JD, Shevliakova E, Williams A (2015) Pervasive drought legacies in forest ecosystems and their implications for carbon cycle models. Science 349: 528–532. doi: https://doi.org/10.1126/science.aab1833
Blackman CJ, Li X, Choat B, Rymer PD, De Kauwe MG, Duursma RA, Tissue DT, Medlyn BE (2019) Desiccation time during drought is highly predictable across species of Eucalyptus from contrasting climates. New Phytologist 224: 632-643. doi: https://doi.org/10.1111/nph.16042
Box EO (1995) Factors determining distributions of tree species and plant functional types. Vegetatio 121, 101–116 (1995). doi: https://doi.org/10.1007/BF00044676
Bower AD, Aitken SN (2006) Geographic and seasonal variation in cold hardiness of whitebark pine. Can J For Res 36:1842–1850. doi: https://doi.org/10.1139/x06-067
Bréda N, Huc R, Granier A, Dreyer E (2006) Temperate forest trees and stands under severe drought:  a review of  ecophysiological responses, adaptation processes  and long-term consequences. Ann. For. Sci. 63: 625-644. doi: https://doi.org/10.1051/forest:2006042
Charrier G, Lacointe A, Améglio T (2018) Dynamic modeling of carbon metabolism during the dormant period accurately predicts the changes in frost hardiness in walnut trees Juglans regia L. Frontiers in Plant Science, 9: 1746. doi: https://doi.org/10.3389/fpls.2018.01746
Charrier G, Martin-Stpaul N, Damesin C, Delpierre N, Hänninen H, Torres-Ruiz J, Hendrik Davi H (2020) Interaction of drought and frost in tree ecophysiology: rethinking the timing of risks. HAL, 02475505, ver. 4 peer-reviewed and recommended by PCI Forest & Wood Sciences. https://hal.archives-ouvertes.fr/hal-02475505v4
Cheaib A, Badeau V, Boe J, Chuine I, Delire C, Dufrêne E, François C, Gritti ES, Legay M, Pagé C (2012) Climate change impacts on tree ranges: model intercomparison facilitates understanding and quantification of uncertainty. Ecology Letters 15(6): 533-544. doi: https://doi.org/10.1111/j.1461-0248.2012.01764.x
Choat B, Jansen S, Brodribb TJ, Cochard H, Delzon S, et al. (2012) Global convergence in the vulnerability of forests to drought. Nature 491, 752–755. doi: https://doi.org/10.1038/nature11688
Choat B, Brodribb TJ, Brodersen CR, Duursma RA, López R, Medlyn BE (2018) Triggers of tree mortality under drought. Nature 558(7711): 531-539. doi: https://doi.org/10.1038/s41586-018-0240-x
Hacke UG, Stiller V, Sperry JS, Pittermann J, McCulloh KA (2001) Cavitation fatigue. Embolism and refilling cycles can weaken the cavitation resistance of xylem. Plant Physol., 125(2), 779–786. doi: https://doi.org/10.1104/pp.125.2.779
Lloret F, Keeling EG, Sala A (2011) Components of tree resilience: effects of successive low‐growth episodes in old ponderosa pine forests. Oikos, 120: 1909-1920. doi: https://doi.org/10.1111/j.1600-0706.2011.19372.x
López de Heredia U, Venturas M, López R, Gil L (2010) High biogeographical and evolutionary value of Canary Island pine populations out of the elevational pinebelt: the case of a relict coastal population. J. Biogeogr. 37, 2371–2383. doi: https://doi.org/10.1111/j.1365-2699.2010.02367.x
Mackay DS, Roberts DE, Ewers BE, Sperry JS, McDowell NG, Pockman WT (2015) Interdependence of chronic hydraulic dysfunction and canopy processes can improve integrated models of tree response to drought, Water Resour. Res., 51, 6156–6176. doi: https://doi.org/10.1002/ 2015WR017244
Martin-StPaul N, Delzon S, Cochard H (2017) Plant resistance to drought depends on timely stomatal closure. Ecology Letters 20(11): 1437-1447. doi: https://doi.org/10.1111/ele.12851
Morin X, Augspurger C, Chuine I (2007) Process-based modeling of species' distributions: what limits temperate tree species' range boundaries? Ecology 88(9):2280-2291. doi: https://doi.org/10.1890/06-1591.1 PMID: 17918406.
Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annual Review of Ecology and Systematics 37, 637–669. doi: https://doi.org/10.1146/annurev.ecolsys.37.091305.110100
Rodriguez‐Zaccaro FD, Valdovinos‐Ayala J, Percolla MI, Venturas MD, Pratt RB, Jacobsen AL (2019) Wood structure and function change with maturity: Age of the vascular cambium is associated with xylem changes in current‐year growth. Plant Cell Environ.42: 1816– 1831. doi: https://doi.org/10.1111/pce.13528
Sakai A, Larcher W (1987) Frost survival of plants. Ecol Stud. 62: 1– 321. doi: https://doi.org/10.1007/978-3-642-71745-1