Made available through Montana State University’s ScholarWorks Faster drought recovery in anisohydric beech compared with isohydric spruce Danielle E M Ulrich, Charlotte Grossiord This is a pre-copyedited, author-produced PDF of an article accepted for publication in Tree Physiology following peer review. The version of record [Faster drought recovery in anisohydric beech compared with isohydric spruce. Tree Physiology (2023)] is available online at: https:// doi.org/10.1093/treephys/tpad009. Title: Faster drought recovery in anisohydric beech compared to isohydric spruce Authors: Danielle E. M. Ulrich1, Charlotte Grossiord2,3 T Affiliations P 1Ecology Department, Montana State University, Bozeman, MT 59717 USA RI 2Swiss Federal Research Institute WSL, Zürcherstrasse 111, 8903 Birmensdorf, SwiCtzerland 3École Polytechnique Fédérale de Lausanne EPFL, School of Architecture, CivilS and Environmental Engineering ENAC, 1015 Lausanne, Switzerland U N Total word count: 1810 A Number of Figures: 2 M D Corresponding author: E Danielle Ulrich, danielle.ulrich@monCtanaT.edu Montana State University – EcoElogy 310 Lewis Hall R Bozeman MT 59717 URSA CO N U © The Author(s) 2023. Published by Oxford University Press. All rights reserved. For p ermissions, please e-mail: journals.permissions@oup.com 1 Downloaded from https://academic.oup.com/treephys/advance-article/doi/10.1093/treephys/tpad009/7008457 by Montana State University user on 31 January 2023 PT CRI S U N A Keywords: drought, recovery, resilience, isohydry, aniso hMydry Running head: Faster drought recovery in anisohyDdric species With drought and heat events increasinEg in frequency and intensity worldwide, global drought-induced tree decline (Allen eCt al. T2010, Hammond et al. 2022) has resulted in widespread interest in understanEding the physiological mechanisms that underlie tree death. Unprecedented mortality raRtes threaten forest function and ecosystem services, including carbon (C) sequestration, cleanR air and water, and recreational and emotional value. Researchers have aimed to understaOnd the mechanisms of tree mortality to better predict which trees will die or survive, infoCrm future forest dynamics, and improve forest management practices (McDowell et al. 200N8, 2011, Raffa et al. 2008, Sevanto et al. 2014, Gaylord et al. 2015, Adams et al. 2017). U With intense investigation of the physiological mechanisms of tree mortality, came research identifying species-specific stomatal regulation strategies along the iso-anisohydric 2 Downloaded from https://academic.oup.com/treephys/advance-article/doi/10.1093/treephys/tpad009/7008457 by Montana State University user on 31 January 2023 continuum (Tardieu and Simonneau 1998, Klein 2014), first identified by (Berger-Landefeldt 1936). More specifically, research addressed how contrasting stomatal regulation strategies under drought may contribute to species-specific mortality vulnerability (McDowell et al. 2008). An isohydric behavior is commonly described for species that exhibit a stringent stomatal T response to drought and close stomata with declining soil moisture to maintain constant midday P leaf water potentials. In contrast, anisohydric species exhibit a less severe stomatal respoRnse tIo drought than isohydric ones, allowing leaf water potentials to track declining soil moCisture. The initial appeal of classifying species based on isohydricity to predict tree mortalityS has led to a bourgeoning number of studies over recent years (Figure 1). Most of this wUork compared co- occurring species from opposite ends of the iso-anisohydric (isohydricNity) continuum, including (and not limited to): evergreen species (Pinus edulis, Juniperus mAonosperma (McDowell et al. 2008, Limousin et al. 2013, Woodruff et al. 2015); Picea wMilsonii, P. tabuliformis, J. przewalskii (Wang et al. 2021)), grapevine varieties (Vitis vinifDera) (Schultz 2003), deciduous hardwood species (Acer saccharum, Liriodendron tulipifEera, Quercus alba) (Kannenberg et al. 2019), shrubs (Sorbus aucuparia, SambucusC nigrTa) (Vogt 2001), and a mix of evergreen and deciduous species (Q. fusiformis, DiospyroEs texana, Prosopis glandulosa, J. ashei) (Johnson et al. 2018). Based on these findings, anRisohydric species are often viewed as more drought resistant than isohydric ones, as exhiRbited by their lower turgor loss point and osmotic potential at full turgor (Meinzer et al. 20O14, 2016), greater stored non-structural carbohydrates (NSCs; Dickman et al. 2015, WoodCruff et al. 2015), greater wood density (Meinzer et al. 2017, Chen et al. 2021), higher resistanNce to embolism (e.g., a more negative water potential at which 50% of hydraulic coUnductivity is lost, P50) (Linton et al. 1998, Martínez-Vilalta et al. 2014), and often, deeper rooting systems (e.g., Grossiord et al. 2017). However, the opposite has also been found with 3 Downloaded from https://academic.oup.com/treephys/advance-article/doi/10.1093/treephys/tpad009/7008457 by Montana State University user on 31 January 2023 anisohydric species having narrower hydraulic safety margins and lower embolism resistance (Benson et al. 2022) (which may be due to the anisohydric species in the study being ring-porous (Kannenberg et al. 2019)). Additionally, even anisohydric species that exhibit higher embolism resistance and hydraulic safety margins can experience higher mortality than co-occurring T isohydric ones (Johnson et al. 2018), which further complicates our understanding of the link P between isohydricity and drought vulnerability. RI However, while much attention has been directed towards investigating drouCght-induced mortality mechanisms and identifying functional responses that could improve oSur understanding of mortality trajectories, being able to predict drought recovery (resilience) Uis of equal importance. Research investigating drought recovery and resilience mNechanisms is ever more relevant today, given that we are undergoing warmer, drier climaAtes than we had anticipated decades ago. Moreover, extreme events are occurring mo reM frequently. Hence, the ability of trees to recover from past droughts is becoming a major Dcomponent shaping future forests. Just 64 of the 577 studies (11%) on isohydricity includedE the term “recovery” or “resilience” (Figure 1), and we encourage research efforts onC thisT critical knowledge gap to continue. Intensively examining how species spanningE a broad range of stomatal regulation strategies recover from drought and whether droughRt-resistant species are also more drought-resilient will improve our understanding of specieRs-specific drought vulnerability and enable more accurate predictions of forest dynamics. OThis is what makes studies like Hesse et al. in the latest issue of Tree Physiology eCver more needed. Their analysis and quantification of recovery time and resilience sheds nNew light on how isohydricity may be linked to drought recovery. U In Hesse et al., the authors compared the resilience and recovery time between relatively anisohydric European beech (Fagus sylvatica L.) and relatively isohydric spruce (Picea abies 4 Downloaded from https://academic.oup.com/treephys/advance-article/doi/10.1093/treephys/tpad009/7008457 by Montana State University user on 31 January 2023 (L.) Karst.). In this mature temperate mixed forest in southeast Germany, the authors imposed a drought using precipitation exclusion shelters that withheld all precipitation and runoff at the KROOF experiment (Grams et al. 2021). After five years, they watered the droughted plots to the level of the soil water content of the control plots and monitored available plant water, leaf T water potentials, stomatal conductance, osmoregulation, sap flow, and leaf abscisic acid (ABA) P concentration. Within two years, all traits (except spruce sap flow) achieved full resiliencRe (i.eI., no difference from control values) but varied in recovery times between species and Ctraits. Generally, isohydric spruce recovered more slowly than anisohydric beech. RecoSvery times were the fastest for leaf water potentials, followed by stomatal conductance and oUsmoregulation. In both species, the function that recovered the slowest was sap flow, wiNth spruce sap flow not fully recovering to control levels within two years. ABA, a plant hormAone involved in stomatal closure, did not change in response to drought in beech, b uMt increased in spruce before quickly and fully recovering within seven days after rewateDring. Hesse et al.’s results suggest that anisoEhydric beech trees were more drought resilient with a faster recovery time than isohyCdricT spruce (Figure 2). One might hypothesize that beech exhibited greater resilience and qEuicker recovery than spruce because the drought had less severe effects on the hydraulic funRctions in beech than spruce (i.e. beech was also more drought resistant than spruce). TRhis is important because greater stress severity can reduce recovery time in various physioOlogical traits, including gas exchange (Li et al. 2021), photosystem II function (Marias et alC. 2017), hydraulic functions (Brodribb and Cochard 2009), and traits related to C and waNter relations (Ruehr et al. 2019). In Hesse et al., predawn leaf water potentials of both spUecies dropped to –1.8 MPa after five years of drought. This predawn leaf water potential value for isohydric spruce should have more severe impacts on water use than for anisohydric beech. 5 Downloaded from https://academic.oup.com/treephys/advance-article/doi/10.1093/treephys/tpad009/7008457 by Montana State University user on 31 January 2023 For example, species that have greater embolism resistance (e.g., P50), wider hydraulic safety margins, and more negative turgor loss points may be more drought tolerant and able to continue functioning under drought, as is widely observed with increasing anisohydricity (Martínez- Vilalta et al. 2014, Meinzer et al. 2016, Fu and Meinzer 2019). However, given that higher T anisohydricity does not always indicate higher drought tolerance or survival (Johnson et al. 2018P, Kannenberg et al. 2019), it is clear that the iso-anisohydric continuum of stringency of plRant I water-status regulation involves coordination and trade-offs among multiple coevolvCed traits (Bartlett et al. 2016, Ratzmann et al. 2019). S Hesse et al.’s study highlights this need to consider multiple traits inU addition to stomatal sensitivity to drought in determining plant drought resistance, resilienNce, and recovery. For example, Hesse et al. and previous studies at the same experimenAtal site found beech and spruce to have similar P50 (-3.42 MPa, -3.74 MPa, respectively ( TMomasella et al. 2018)) and turgor loss point (-2.40 MPa, -2.43 MPa, respectively (Hesse eDt al.)). Unexpectedly, beech had a narrower hydraulic safety margin (1.54 MPa) than sprucEe (2.11 MPa) (Tomasella et al. 2018). Therefore, the findings of Hesse et al. suggest thCat otTher traits beyond those traits more frequently measured to assess drought resistance undeErlie the differences in recovery time between beech and spruce. These traits include ABA-dRriven stomatal closure in isohydric species versus more hydraulics- driven stomatal closureR in anisohydric ones; slower regrowth of leaf area in spruce than beech, lowering and delaOying the water demand by the spruce canopy; deeper rooting system of beech than spruce (CNikolova et al. 2009, Rötzer et al. 2017); slower regrowth of fine roots in spruce than beNech after drought release (Nickel et al. 2018, Zwetsloot and Bauerle 2021), limiting water upUtake of spruce after watering and promoting faster C turnover in beech than spruce (Nikolova et al. 2020); and the presence of vessels in angiosperms promoting more efficient water transport 6 Downloaded from https://academic.oup.com/treephys/advance-article/doi/10.1093/treephys/tpad009/7008457 by Montana State University user on 31 January 2023 versus the lack of vessels in gymnosperms (Figure 2). Spruce’s slower recovery compared to beech may also be related to reductions in stored C reserves that more likely occur in isohydric species due to drought-induced restrictions on stomatal conductance and C assimilation (Sevanto et al. 2014, Woodruff et al. 2015). Additionally, anisohydric juniper has exhibited greater T adjustment in response to hydration than isohydric pinyon (Meinzer et al. 2014), which may alsoP contribute to beech’s faster recovery. As emphasized by Hesse et al., isohydricity incorpoRrateIs coordination among multiple traits, including stomatal regulation of leaf water potenCtial under drought, drought resistance metrics (P50, turgor loss point, hydraulic safety margSin), and other traits (hormonal, morphological, structural, C balance and allocation) that dUeserve further attention. N Are more drought-resistant species also more drought-resAilient? Previous work has suggested a tradeoff between resistance and resilience in gMymnosperms (Li et al. 2020, Gebauer et al. 2020) and evergreen oak species (Fallon and CDavender-Bares 2018). However, Hesse et al.’s findings suggest that more resistant speciEes may also be more resilient, which may be independent of stomatal regulation stCrategTy (Kannenberg et al. 2019), and instead relate to wood density and hydraulic safety marEgins that increase drought resistance and resilience (Duan et al. 2013), as well as traits less Rfrequently measured including leaf ABA concentration, morphology, structure, and C balancRe and allocation (Hesse et al.). Reduced recovery (legacy effects) was consistently prevaOlent in dry ecosystems among Pinaceae and species with low hydraulic safety margins (AnCderegg et al. 2015). NHesse et al.’s study nicely exemplifies the type of future work needed to understand how otUher traits beyond stomatal regulation strategy affect drought recovery and to identify species’ drought vulnerability, resistance, and resilience. Like Hesse et al, we need more studies that 7 Downloaded from https://academic.oup.com/treephys/advance-article/doi/10.1093/treephys/tpad009/7008457 by Montana State University user on 31 January 2023 focus on long-term (i.e., multi-year) effects of drought, particularly work including drought recovery. Future work should also measure multiple types of traits, including stomatal regulation of leaf water potential under drought, drought resistance metrics (P50, turgor loss point, hydraulic safety margin), but also other traits that are less frequently included in our ecophysiology T toolbox (hormonal, morphological, structural, C balance and allocation) to holistically P understand plant physiological recovery mechanisms. Finally, more research should expaRnd I beyond these two species and assess resilience and recovery time in a wide range of Cspecies spanning leaf habit (evergreen, deciduous) as in Hesse et al., and the iso-anisohySdric continuum. With more research on recovery time and resilience across species and funcUtional groups, we may be able to identify an easier-to-measure proxy for recovery time aNnd resilience that may improve broader predictions of forest vulnerability and resilienceA to drought. 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Woodruff DR, Meinzer FC, Marias DE, SevanEto S, Jenkins MW, McDowell NG (2015) Linking nonstructural carbohydrate dynamics to gas exchange and leaf hydraulic behavior in Pinus edulis and Juniperus moCnospTerma. New Phytol 206:411–421. Zwetsloot MJ, Bauerle TL (2021) Repetitive seasonal drought causes substantial species-specific shifts in fine-root longevEity and spatio-temporal production patterns in mature temperate forest trees. New PhRytol 231:974–986. R CO N U 12 Downloaded from https://academic.oup.com/treephys/advance-article/doi/10.1093/treephys/tpad009/7008457 by Montana State University user on 31 January 2023 IP T CR Figure 1. Web of Science search for the terms “plant” and “*isohydr*” (190U0-20S22) yielded 577 articles in total (blue), and the number of these studies has increased substantially since 2008. Of these studies, 64 studies (11%) included the term “recovery” or “resilience” (orange). The number of recovery studies has been slowly increasing. N A M D TE C E Figure 2. Mechanisms underlying drought recovery of predawn leaf water potential (ψ), stomatal conductance (gs), sap flow,R and root growth in anisohydric beech (Fagus sylvatica) and isohydric spruce (Picea abies). HResse et al. found that physiological and biochemical traits such as ψ and gs recovered faster (from days to weeks) than traits related to morphology such as sap flow, which depends upOon root and leaf area regrowth (from months to years). C N U 13 Downloaded from https://academic.oup.com/treephys/advance-article/doi/10.1093/treephys/tpad009/7008457 by Montana State University user on 31 January 2023