Variation in hydraulic vulnerability of juvenile ponderosa pines in the southwestern United States

Abstract

Hydraulic vulnerability, the sensitivity of xylem embolism to water stress, is a major determinant trait associated with conifer mortality. This study investigated branch P50 (50% hydraulic conductivity loss) of adult and juvenile ponderosa pines across multiple locations in the southwestern United States (SWUS), and examined relationships between P50 and climatic conditions, soil properties and forest management. Juvenile ponderosa pines had significantly more negative P50 values than adults on average. Both age groups exhibited a latitudinal pattern in P50 associated with regional climate conditions. Across the SWUS, juvenile P50 was positively correlated with growing season precipitation and temperature, and negatively correlated with soil pH and clay content. In some cases, significant differences in juvenile P50 between SWUS locations were associated with growing season moisture deficit, whereas other significant differences were less attributable to climate and may attest to potential genetic variation between populations. Climate variation, soil properties and population-level acclimation and/or adaptation may all influence the hydraulic vulnerability of juvenile ponderosa pines in the SWUS, promoting differences in stress tolerance of ponderosa pine forests across the region.

Keywords

Drought / Vegetation response / Xylem embolism / Water stress tolerance / Hydraulic failure

References

[1] Adams HD, Zeppel MJB, Anderegg WRL, Hartmann H, Landhäusser SM, Tissue DT, Huxman TE, Hudson PJ, Franz TE, Allen CD, Anderegg LDL, Barron-Gafford GA, Beerling DJ, Breshears DD, Brodribb TJ, Bugmann H, Cobb RC, Collins AD, Dickman LT, Duan H, Ewers BE, Galiano L, Galvez DA, Garcia-Forner N, Gaylord ML, Germino MJ, Gessler A, Hacke UG, Hakamada R, Hector A, Jenkins MW, Kane JM, Kolb TE, Law DJ, Lewis JD, Limousin JM, Love DM, Macalady AK, Martínez-Vilalta J, Mencuccini M, Mitchell PJ, Muss JD, O’Brien MJ, O’Grady AP, Pangle RE, Pinkard EA, Piper FI, Plaut JA, Pockman WT, Quirk J, Reinhardt K, Ripullone F, Ryan MG, Sala A, Sevanto S, Sperry JS, Vargas R, Vennetier M, Way DA, Xu C, Yepez EA, McDowell NG. A multi-species synthesis of physiological mechanisms in drought-induced tree mortality. Nat Ecol Evol, 2017, 1(9): 1285-1291

[2] Alder NN, Pockman WT, Sperry JS, Nuismer S. Use of centrifugal force in the study of xylem cavitation. J Exp Bot, 1997, 48(3): 665-674

[3] Anderegg LDL, HilleRisLambers J. Drought stress limits the geographic ranges of two tree species via different physiological mechanisms. Glob Chang Biol, 2016, 22(3): 1029-1045

[4] Andrews CM, D’Amato AW, Fraver S, Palik B, Battaglia MA, Bradford JB. Low stand density moderates growth declines during hot droughts in semi-arid forests. J Appl Ecol, 2020, 57(6): 1089-1102

[5] Anfodillo T, Olson ME. Tree mortality: testing the link between drought, embolism vulnerability, and xylem conduit diameter remains a priority. Front for Glob Change, 2021, 4: 704670

[6] Arend M, Link RM, Patthey R, Hoch G, Schuldt B, Kahmen A (2021) Rapid hydraulic collapse as cause of drought-induced mortality in conifers. In: Proceedings national academy science USA, 118(16): e2025251118. https://doi.org/10.1073/pnas.2025251118

[7] Bacher E (2022) Conductor: create tours in Shiny apps using ‘shepherd.js’. R package version 0.1.1. https://CRAN.R-project.org/package=conductor

[8] Bennett AC, McDowell NG, Allen CD, Anderson-Teixeira KJ. Larger trees suffer most during drought in forests worldwide. Nat Plants, 2015, 1: 15139

[9] Berner LT, Law BE, Meddens AJH, Hicke JA. Tree mortality from fires, bark beetles, and timber harvest during a hot and dry decade in the western United States (2003–2012). Environ Res Lett, 2017, 12(6): 065005

[10] Berner LT, Law BE, Meddens AJH, Hicke JA. Corrigendum: tree mortality from fires, bark beetles, and timber harvest during a hot and dry decade in the western United States (2003–2012). Environ Res Lett, 2019, 14: 059501

[11] Bordoloi R, Das B, Yam G, Pandey PK, Tripathi OP. Modeling of water holding capacity using readily available soil characteristics. Agric Res, 2019, 8(3347-355

[12] Bottero A, D’Amato AW, Palik BJ, Bradford JB, Fraver S, Battaglia MA, Asherin LA. Density-dependent vulnerability of forest ecosystems to drought. J Appl Ecol, 2017, 54(61605-1614

[13] Bouche PS, Larter M, Domec JC, Burlett R, Gasson P, Jansen S, Delzon S. A broad survey of hydraulic and mechanical safety in the xylem of conifers. J Exp Bot, 2014, 65(15): 4419-4431

[14] Bouffier L, Gartner B, Domec J. Wood density and hydraulic properties of ponderosa pine from the Willamette valley vs. the Cascade mountains. Wood Fiber Sci, 2003, 35: 217-233

[15] Bradford JB, Shriver RK, Robles MD, McCauley LA, Woolley TJ, Andrews CA, Crimmins M, Bell DM. Tree mortality response to drought-density interactions suggests opportunities to enhance drought resistance. J Appl Ecol, 2022, 59(2): 549-559

[16] Chaney NW, Minasny B, Herman JD, Nauman TW, Brungard CW, Morgan CLS, McBratney AB, Wood EF, Yimam Y. POLARIS soil properties: 30-m probabilistic maps of soil properties over the contiguous United States. Water Resour Res, 2019, 55(4): 2916-2938

[17] Clute T, Martin J, Looker N, Hu J. Correction to: hydraulic traits of co-existing conifers do not correlate with local hydroclimate condition: a case study in the northern rocky mountains U.S.A. Oecologia, 2021, 196(2): 605

[18] Cochard H, Cruiziat P, Tyree MT. Use of positive pressures to establish vulnerability curves: further support for the air-seeding hypothesis and implications for pressure-volume analysis. Plant Physiol, 1992, 100(1205-209

[19] Covington WW, Moore MM. Southwestern ponderosa forest structure: changes since Euro-American settlement. J for, 1994, 92(1): 39-47

[20] Davis KT, Dobrowski SZ, Higuera PE, Holden ZA, Veblen TT, Rother MT, Parks SA, Sala AN, Maneta MP (2019) Wildfires and climate change push low-elevation forests across a critical climate threshold for tree regeneration. In: Proceedings national academy science USA, 116(13): 6193–6198. https://doi.org/10.1073/pnas.1815107116

[21] Davis KT, Robles MD, Kemp KB, Higuera PE, Chapman T, Metlen KL, Peeler JL, Rodman KC, Woolley T, Addington RN, Buma BJ, Cansler CA, Case MJ, Collins BM, Coop JD, Dobrowski SZ, Gill NS, Haffey C, Harris LB, Harvey BJ, Haugo RD, Hurteau MD, Kulakowski D, Littlefield CE, McCauley LA, Povak N, Shive KL, Smith E, Stevens JT, Stevens-Rumann CS, Taylor AH, Tepley AJ, Young DJN, Andrus RA, Battaglia MA, Berkey JK, Busby SU, Carlson AR, Chambers ME, Dodson EK, Donato DC, Downing WM, Fornwalt PJ, Halofsky JS, Hoffman A, Holz A, Iniguez JM, Krawchuk MA, Kreider MR, Larson AJ, Meigs GW, Roccaforte JP, Rother MT, Safford H, Schaedel M, Sibold JS, Singleton MP, Turner MG, Urza AK, Clark-Wolf KD, Yocom L, Fontaine JB, Campbell JL (2023) Reduced fire severity offers near-term buffer to climate-driven declines in conifer resilience across the western United States. In: Proceedings national academy science USA, 120(11): e2208120120. https://doi.org/10.1073/pnas.2208120120

[22] Domec JC, Gartner BL. Relationship between growth rates and xylem hydraulic characteristics in young, mature and old-growth ponderosa pine trees. Plant Cell Environ, 2003, 26(3): 471-483

[23] Domec JC, Pruyn ML. Bole girdling affects metabolic properties and root, trunk and branch hydraulics of young ponderosa pine trees. Tree Physiol, 2008, 28(10): 1493-1504

[24] Domec JC, Warren JM, Meinzer FC, Brooks JR, Coulombe R. Native root xylem embolism and stomatal closure in stands of Douglas-fir and ponderosa pine: mitigation by hydraulic redistribution. Oecologia, 2004, 141(1): 7-16

[25] Domec JC, Pruyn ML, Gartner BL. Axial and radial profiles in conductivities, water storage and native embolism in trunks of young and old-growth ponderosa pine trees. Plant Cell Environ, 2005, 28(9): 1103-1113

[26] Domec JC, Warren JM, Meinzer FC, Lachenbruch B. Safety factors for xylem failure by implosion and air-seeding within roots, trunks and branches of young and old conifer trees. IAWA J, 2009, 30(2): 101-120

[27] Duursma R, Choat B. Fitplc - an R package to fit hydraulic vulnerability curves. J Plant Hydraul, 2017, 4: e002

[28] Feeney SR, Kolb TE, Covington WW, Wagner MR. Influence of thinning and burning restoration treatments on presettlement ponderosa pines at the Gus Pearson natural area. Can J for Res, 1998, 28(9): 1295-1306

[29] Fernández-de-Uña L, Martínez-Vilalta J, Poyatos R, Mencuccini M, McDowell NG. The role of height-driven constraints and compensations on tree vulnerability to drought. New Phytol, 2023, 239(62083-2098

[30] Hacke UG, Sperry JS, Ewers BE, Ellsworth DS, Schäfer KR, Oren R. Influence of soil porosity on water use in Pinus taeda. Oecologia, 2000, 124(4): 495-505

[31] Hacke UG, Sperry JS, Pockman WT, Davis SD, McCulloh KA. Trends in wood density and structure are linked to prevention of xylem implosion by negative pressure. Oecologia, 2001, 126(4): 457-461

[32] Hardage K, Wheelock SJ, Gaffney R, O’Halloran T, Serpa B, Grant G, Coppoletta M, Csank A, Tague C, Staudacher M, Tyler S. Soil moisture and micrometeorological differences across reference and thinned stands during extremes of precipitation, southern Cascade range. Front for Glob Change, 2022, 5: 898998

[33] He PC, Gleason SM, Wright IJ, Weng ES, Liu H, Zhu SD, Lu MZ, Luo Q, Li RH, Wu GL, Yan ER, Song YJ, Mi XC, Hao GY, Reich PB, Wang YP, Ellsworth DS, Ye Q. Growing-season temperature and precipitation are independent drivers of global variation in xylem hydraulic conductivity. Glob Chang Biol, 2020, 26(3): 1833-1841

[34] Hietz P, Rosner S, Sorz J, Mayr S. Comparison of methods to quantify loss of hydraulic conductivity in Norway spruce. Ann for Sci, 2008, 65(5502

[35] Howell J. The development of seedlings of ponderosa pine in relation to soil types. J for, 1932, 30: 944-947

[36] Hultine KR, Koepke DF, Pockman WT, Fravolini A, Sperry JS, Williams DG. Influence of soil texture on hydraulic properties and water relations of a dominant warm-desert phreatophyte. Tree Physiol, 2006, 26(3313-323

[37] Jarvis N, Koestel J, Messing I, Moeys J, Lindahl A. Influence of soil, land use and climatic factors on the hydraulic conductivity of soil. Hydrol Earth Syst Sci, 2013, 17(12): 5185-5195

[38] Jiang X, Choat B, Zhang Y-J, Guan X-Y, Shi W, Cao K-F. Variation in xylem hydraulic structure and function of two mangrove species across a latitudinal gradient in Eastern Australia. Water, 2021, 13(6): 850

[39] Johnson KM, Brodribb TJ. Evidence for a trade-off between growth rate and xylem cavitation resistance in Callitris rhomboidea. Tree Physiol, 2023, 43(71055-1065

[40] Kilgore JS, Jacobsen AL, Telewski FW. Hydraulics of Pinus (subsection ponderosae) populations across an elevation gradient in the santa Catalina mountains of southern Arizona. Madroño, 2020, 67(4): 218-226

[41] Kolb TE, Grady KC, McEttrick MP, Herrero A. Local-scale drought adaptation of ponderosa pine seedlings at habitat ecotones. For Sci, 2016, 62(6): 641-651

[42] Kolb TE, Dixit A, Burney O. Challenges and opportunities for maintaining ponderosa pine forests in the southwestern U.S. Tree Plant Notes, 2019, 62: 104-112

[43] Korb JE, Fornwalt PJ, Stevens-Rumann CS. What drives ponderosa pine regeneration following wildfire in the western United States?. For Ecol Manag, 2019, 454: 117663

[44] Li XM, Blackman CJ, Choat B, Duursma RA, Rymer PD, Medlyn BE, Tissue DT. Tree hydraulic traits are coordinated and strongly linked to climate-of-origin across a rainfall gradient. Plant Cell Environ, 2018, 41(3): 646-660

[45] Liu H, Gleason SM, Hao GY, Hua L, He PC, Goldstein G, Ye Q. Hydraulic traits are coordinated with maximum plant height at the global scale. Sci Adv, 2019, 5(2eaav332

[46] Lucani CJ, Brodribb TJ, Jordan GJ, Mitchell PJ. Juvenile and adult leaves of heteroblastic Eucalyptus globulus vary in xylem vulnerability. Trees, 2019, 33(41167-1178

[47] Maherali H, DeLucia EH. Xylem conductivity and vulnerability to cavitation of ponderosa pine growing in contrasting climates. Tree Physiol, 2000, 20(13): 859-867

[48] Maherali H, Williams BL, Paige KN, Delucia EH. Hydraulic differentiation of Ponderosa pine populations along a climate gradient is not associated with ecotypic divergence. Funct Ecol, 2002, 16(4): 510-521

[49] Mair P, Wilcox R. Robust statistical methods in R using the WRS2 package. Behav Res Methods, 2020, 52(2): 464-488

[50] Matzner SL, Rice KJ, Richards JH. Intra-specific variation in xylem cavitation in interior live oak (Quercus wislizenii A. DC.). J Exp Bot, 2001, 52(357): 783-789

[51] McDowell NG, Allen CD. Darcy’s law predicts widespread forest mortality under climate warming. Nat Clim Change, 2015, 5(7): 669-672

[52] Mencuccini M. Hydraulic constraints in the functional scaling of trees. Tree Physiol, 2002, 22(8): 553-565

[53] Miller DA, White RA. A conterminous United States multilayer soil characteristics dataset for regional climate and hydrology modeling. Earth Interact, 1998, 2(2): 1-26

[54] National Center for Environmental Information (2020) Climate maps of the United States. https://www.ncei.noaa.gov/data/climate-maps-deprecated/access/

[55] Olson ME, Anfodillo T, Gleason SM, McCulloh KA. Tip-to-base xylem conduit widening as an adaptation: causes, consequences, and empirical priorities. New Phytol, 2021, 229(4): 1877-1893

[56] Oyanoghafo OO, Brien CO, Choat B, Tissue D, Rymer PD. Vulnerability to xylem cavitation of Hakea species (Proteaceae) from a range of biomes and life histories predicted by climatic niche. Ann Bot, 2021, 127(7): 909-918

[57] Pastore M. Overlapping: a R package for estimating overlapping in empirical distributions. J Open Source Softw, 2018, 3(32): 1023

[58] Pearson G (1950) Management of Ponderosa Pine in the Southwest as developed by research and experimental practice. Agriculture Monograph No. 6. Washington, DC: U.S. Department of Agriculture, Forest Service, p 218.

[59] Petrie MD, Bradford JB, Lauenroth WK, Schlaepfer DR, Andrews CM, Bell DM. Non-analog increases to air, surface, and belowground temperature extreme events due to climate change. Clim Change, 2020, 163(42233-2256

[60] Petrie MD, Hubbard RM, Bradford JB, Kolb TE, Noel A, Schlaepfer DR, Bowen MA, Fuller LR, Moser WK. Widespread regeneration failure in ponderosa pine forests of the southwestern United States. For Ecol Manag, 2023, 545: 121208

[61] Pirtel NL, Hubbard RM, Bradford JB, Kolb TE, Litvak ME, Abella SR, Porter SL, Petrie MD. The aboveground and belowground growth characteristics of juvenile conifers in the southwestern United States. Ecosphere, 2021, 12(11): e03839

[62] Pittermann J, Sperry JS. Analysis of freeze-thaw embolism in conifers. The interaction between cavitation pressure and tracheid size. Plant Physiol, 2006, 140(1374-382

[63] Prendin AL, Mayr S, Beikircher B, von Arx G, Petit G. Xylem anatomical adjustments prioritize hydraulic efficiency over safety as Norway spruce trees grow taller. Tree Physiol, 2018, 38(81088-1097

[64] Puhlick JJ, Laughlin DC, Moore MM. Factors influencing ponderosa pine regeneration in the southwestern USA. For Ecol Manag, 2012, 264: 10-19

[65] Puhlick JJ, Laughlin DC, Moore MM, Sieg CH, Overby ST, Shaw JD. Soil properties and climate drive ponderosa pine seedling presence in the southwestern USA. For Ecol Manag, 2021, 486: 118972

[66] Putz TR, Urza AK, Hankin LE, Bisbing SM. Seasonal water availability drives trait variation in isolated Basin and Range Pinus ponderosa. For Ecol Manag, 2021, 488: 119022

[67] Rapport DJ. Historical changes in ponderosa pine forests since Euro-American settlement. Ecosyst Health, 1997, 3(3): 171-184

[68] Rehfeldt GE. Genetic variation in the ponderosae of the southwest. Am J Bot, 1993, 80(3330-343

[69] Rehfeldt GE, Leites LP, Bradley St Clair J, Jaquish BC, Sáenz-Romero C, López-Upton J, Joyce DG. Comparative genetic responses to climate in the varieties of Pinus ponderosa and Pseudotsuga menziesii: clines in growth potential. For Ecol Manag, 2014, 324: 138-146

[70] Rosner S. Wood density as a proxy for vulnerability to cavitation: Size matters. J Plant Hydraul, 2017, 4: e001

[71] Rosner S, Johnson DM, Voggeneder K, Domec JC. The conifer-curve: fast prediction of hydraulic conductivity loss and vulnerability to cavitation. Ann for Sci, 2019, 76(3): 82

[72] Sankey T, Tatum J. Thinning increases forest resiliency during unprecedented drought. Sci Rep, 2022, 12(19041

[73] Savi T, Tintner J, Da Sois L, Grabner M, Petit G, Rosner S. The potential of Mid-Infrared spectroscopy for prediction of wood density and vulnerability to embolism in woody angiosperms. Tree Physiol, 2019, 39(3503-510

[74] Schlaepfer D, Murphy R (2023) rSOILWAT2: an ecohydrological ecosystem-scale water balance simulation model. R package v6.0.2. https://github.com/DrylandEcology/rSOILWAT2

[75] Secchi F, Bevilacqua I, Agliassa C, Maghrebi M, Cavalletto S, Morabito C, Lembo S, Vigani G. Alkaline soil primes the recovery from drought in Populus nigra plants through physiological and chemical adjustments. Plant Physiol Biochem, 2023, 201: 107838

[76] Slessarev EW, Lin Y, Bingham NL, Johnson JE, Dai Y, Schimel JP, Chadwick OA. Water balance creates a threshold in soil pH at the global scale. Nature, 2016, 540(7634567-569

[77] Sohn JA, Saha S, Bauhus J. Potential of forest thinning to mitigate drought stress: a meta-analysis. For Ecol Manag, 2016, 380: 261-273

[78] Sperry JS, Hacke UG. Desert shrub water relations with respect to soil characteristics and plant functional type. Funct Ecol, 2002, 16(3367-378

[79] Sperry JS, Tyree MT. Mechanism of water stress-induced xylem embolism. Plant Physiol, 1988, 88(3): 581-587

[80] Sperry JS, Hacke UG, Pittermann J. Size and function in conifer tracheids and angiosperm vessels. Am J Bot, 2006, 93(10): 1490-1500

[81] Stevens-Rumann CS, Prichard SJ, Whitman E, Parisien MA, Meddens AJH. Considering regeneration failure in the context of changing climate and disturbance regimes in western North America. Can J for Res, 2022, 52(10): 1281-1302

[82] Stojnić S, Suchocka M, Benito-Garzón M, Torres-Ruiz JM, Cochard H, Bolte A, Cocozza C, Cvjetkovic B, de Luis M, Martinez-Vilalta J, Ræbild A, Tognetti R, Delzon S. Variation in xylem vulnerability to embolism in European beech from geographically marginal populations. Tree Physiol, 2018, 38(2): 173-185

[83] Stout DH, Sala AN. Xylem vulnerability to cavitation in Pseudotsuga menziesii and Pinus ponderosa from contrasting habitats. Tree Physiol, 2003, 23(1): 43-50

[84] Thornton M, Shrestha R, Wei Y, Thornton P, Kao S, Wilson B (2022) Daymet: daily surface weather data on a 1-km grid for North America, version 4 R1. ORNL DAAC, Oak Ridge, Tennessee, USA. https://doi.org/10.3334/ORNLDAAC/2129

[85] Tyree MT, Sperry JS. Vulnerability of xylem to cavitation and embolism. Annu Rev Plant Physiol Plant Mol Biol, 1989, 40: 19-36

[86] van der Sande MT, Poorter L, Schnitzer SA, Engelbrecht BMJ, Markesteijn L. The hydraulic efficiency-safety trade-off differs between lianas and trees. Ecology, 2019, 100(5): e02666

[87] Vaughan D, Auty D, Kolb TE, Sánchez Meador AJ, Mackes KH, Dahlen J, Moser WK. Climate has a larger effect than stand basal area on wood density in Pinus ponderosa var. scopulorum in the southwestern USA. Ann for Sci, 2019, 76(385

[88] Venturas MD, Todd HN, Trugman AT, Anderegg WRL. Understanding and predicting forest mortality in the western United States using long-term forest inventory data and modeled hydraulic damage. New Phytol, 2021, 230(51896-1910

[89] Vicente E, Didion-Gency M, Morcillo L, Morin X, Vilagrosa A, Grossiord C. Aridity and cold temperatures drive divergent adjustments of European beech xylem anatomy, hydraulics and leaf physiological traits. Tree Physiol, 2022, 42(9): 1720-1735

[90] Weithmann G, Link RM, Banzragch BE, Würzberg L, Leuschner C, Schuldt B. Soil water availability and branch age explain variability in xylem safety of European beech in Central Europe. Oecologia, 2022, 198(3): 629-644

[91] Wu DA, Shu MJ, Moran EV. Heritability of plastic trait changes in drought-exposed ponderosa pine seedlings. Ecosphere, 2023, 14(3e4454

RIGHTS & PERMISSIONS

Northeast Forestry University