Abstract
Resprouting is a key functional trait for species in disturbance prone environments. In many semi-arid environments, woody plants face both fire and drought as recurring disturbances. Past work has demonstrated that oaks inhabiting sky-island forests of the northern Sierra Madre Oriental have differing microhabitat preferences and heavy stem dieback occured during the historic 2011 drought indicating potential xylem failure. These oak species, representing two sections within the genus, are all post-fire resprouters: they can resprout from underground storage organs when fire kills above ground tissue. Resprouts provide an opportunity to examine how functional traits may change as plastic responses to changing environmental conditions. Post-fire resprouts have increased root:shoot ratios relative to adults and therefore have access to more water relative to leaf demand. We expected that if resprouts exhibit plasticity in xylem function, they should favor water transport efficiency over safety: they should have higher maximum xylem conductivity, but greater susceptibility to drought-induced cavitation. We examined four oak species common in the Davis Mountains in west Texas and compared adult physiology with that of resprouts following wildfire. We found that species differed in degree of desiccation avoidance (isohydry) consistent with microhabitat preferences and that the species that were most desiccation tolerant as adults had resprouts significantly more susceptible to xylem cavitation. We found no evidence for a trade-off between efficiency and safety, however.
Similar content being viewed by others
References
Ackerly D (2004) Functional strategies of chaparral shrubs in relation to season water deficit and disturbance. Ecol Monogr 74:25–44
Alder N, Pockman W, Sperry J, Nuismer S (1997) Use of centrifugal force in the study of xylem cavitation. J Exp Bot 48:665–674. doi:10.1093/jxb/48.3.665
Allen CD, Breshears DD (1998) Drought-induced shift of a forest–woodland ecotone: rapid landscape response to climate variation. Proc Natl Acad Sci 95:14839–14842
Anderegg WRL (2015) Spatial and temporal variation in plant hydraulic traits and their relevance for climate change impacts on vegetation. New Phytol 205:1008–1014
Anderegg WR, Flint A, Huang Cy, Flint L, Berry JA, Davis FW, Sperry JS, Field CB (2015) Tree mortality predicted from drought-induced vascular damage
Bell DT (2001) Ecological response syndromes in the flora of southwestern Western Australia: Fire resprouters versus reseeders. Bot Rev 67:417–440
Bhaskar R, Ackerly DD (2006) Ecological relevance of minimum seasonal water potentials. Physiol Plant 127:353–359. doi:10.1111/j.1399-3054.2006.00718.x
Bond WJ, Midgley JJ (2001) Ecology of sprouting in woody plants: the persistence niche. Trends Ecol Evol 16:45–51
Bond WJ, van Wilgen BW (1996) Fire and plants. Chapman & Hall, London
Cavender-Bares J, Holbrook N (2001) Hydraulic properties and freezing-induced cavitation in sympatric evergreen and deciduous oaks with contrasting habitats. Plant, Cell Environ 24:1243–1256
Cavender-Bares J, Kitajima K, Bazzaz FA (2004) Multiple trait associations in relation to habitat differentiation among 17 Floridian oak species. Ecol Monogr 74:635–662
Charles-Dominique T, Beckett H, Midgley GF, Bond WJ (2015) Bud protection: a key trait for species sorting in a forest–savanna mosaic. New Phytol. doi:10.1111/nph.13406
Choat B, Drayton WM, Brodersen C, Matthews MA, Shackel KA, Wada H, McElrone AJ (2010) Measurement of vulnerability to water stress-induced cavitation in grapevine: A comparison of four techniques applied to a long-vesseled species. Plant, Cell Environ 33:1502–1512
Christman MA, Sperry JS, Smith DD (2012) Rare pits, large vessels and extreme vulnerability to cavitation in a ring-porous tree species. New Phytol 193:713–720
Clarke PJ, Lawes MJ, Midgley JJ, Lamont BB, Ojeda F, Burrows GE, Enright NJ, Knox KJE (2013) Resprouting as a key functional trait: How buds, protection and resources drive persistence after fire. New Phytol 197:19–35. doi:10.1111/nph.12001
Cochard H, Herbette S, Barigah T, Badel E, Ennajeh M, Vilagrosa A (2010) Does sample length influence the shape of xylem embolism vulnerability curves? A test with the cavitron spinning technique. Plant, Cell Environ 33:1543–1552
Corcuera L, Camarero JJ, Gil-Pelegrín E (2004) Effects of a severe drought on Quercus ilex radial growth and xylem anatomy. Trees 18:83–92
Corcuera L, Cochard H, Gil-Pelegrin E, Notivol E (2011) Phenotypic plasticity in mesic populations of Pinus pinaster improves resistance to xylem embolism (P50) under severe drought. Trees 25:1033–1042. doi:10.1007/s00468-011-0578-2
Davis SD, Ewers FW, Wood J, Reeves JJ, Kolb KJ (1999) Differential susceptibility to xylem cavitation among three pairs of Ceanothus species in the transverse mountain ranges of southern California. Ecoscience 6:180–186
Falster DS, Westoby M (2005) Tradeoffs between height growth rate, stem persistence and maximum height among plant species in a post-fire succession. Oikos 111:57–66
Gleason SM, Westoby M, Jansen S, Choat B, Hacke UG, Pratt RB, Bhaskar R, Brodribb TJ, Bucci SJ, Cao K-F, Cochard H, Delzon S, Domec J-C, Fan Z-X, Feild TS, Jacobsen AL, Johnson DM, Lens F, Maherali H, Martínez-Vilalta J, Mayr S, McCulloh KA, Mencuccini M, Mitchell PJ, Morris H, Nardini A, Pittermann J, Plavcová L, Schreiber SG, Sperry JS, Wright IJ, Zanne AE (2015) Weak tradeoff between xylem safety and xylem-specific hydraulic efficiency across the world’s woody plant species. New Phytol. doi:10.1111/nph.13646
Hacke UG, Sperry JS, Pittermann J (2000) Drought experience and cavitation resistance in six shrubs from the Great Basin, Utah. Basic Appl Ecol 1:31–41
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 Physiol 125:779–786
Hacke UG, Sperry JS, Wheeler JK, Castro L (2006) Scaling of angiosperm xylem structure with safety and efficiency. Tree Physiol 26:689–701
Hacke UG, Venturas MD, MacKinnon ED, Jacobsen AL, Sperry JS, Pratt RB (2015) The standard centrifuge method accurately measures vulnerability curves of long-vesselled olive stems. New Phytol 205:116–127. doi:10.1111/nph.13017
Hessl AE (2011) Pathways for climate change effects on fire: Models, data, and uncertainties. Prog Phys Geogr 35:393–407
Hipp AL, Eaton DA, Cavender-Bares J, Fitzek E, Nipper R, Manos PS (2014) A framework phylogeny of the American oak clade based on sequenced RAD data. PLoS ONE 9:e93975
Holbrook NM, Burns MJ, Field CB (1995) Negative xylem pressures in plants: A test of the balancing pressure technique. Science 270:1193–1193
IPCC (2014) Climate change 2014: Synthesis report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. IPPC, Geneva, Switzerland
Jacobsen AL, Pratt RB (2012) No evidence for an open vessel effect in centrifuge-based vulnerability curves of a long-vesselled liana (Vitis vinifera). New Phytol 194:982–990. doi:10.1111/j.1469-8137.2012.04118.x
Jacobsen AL, Pratt RB, Davis SD, Ewers FW (2007) Cavitation resistance and seasonal hydraulics differ among three arid Californian plant communities. Plant, Cell Environ 30:1599–1609
Jacobsen AL, Pratt RB, Davis SD, Ewers FW (2008) Comparative community physiology: Nonconvergence in water relations among three semi-arid shrub communities. New Phytol 180:100–113. doi:10.1111/j.1469-8137.2008.02554.x
Jacobsen AL, Pratt RB, Davis SD, Tobin MF (2014) Geographic and seasonal variation in chaparral vulnerability to cavitation. Madroño 61:317–327
Keeley JE (1991) Seed germination and life history syndromes in the California chaparral. Bot Rev 57:81–116
Koepke DF, Kolb TE, Adams HD (2010) Variation in woody plant mortality and dieback from severe drought among soils, plant groups, and species within a northern Arizona ecotone. Oecologia 163:1079–1090
Lamy J-B, Delzon S, Bouche PS, Alia R, Vendramin GG, Cochard H, Plomion C (2014) Limited genetic variability and phenotypic plasticity detected for cavitation resistance in a Mediterranean pine. New Phytol 201:874–886
Li Y, Sperry J, Taneda H, Bush S, Hacke U (2008) Evaluation of centrifugal methods for measuring xylem cavitation in conifers, diffuse- and ring-porous angiosperms. New Phytol 177:558–568
Maherali H, Pockman WT, Jackson RB (2004) Adaptive variation in the vulnerability of woody plants to xylem cavitation. Ecology 85:2184–2199
Maherali H, Moura CF, Caldeira MC, Willson CJ, Jackson RB (2006) Functional coordination between leaf gas exchange and vulnerability to xylem cavitation in temperate forest trees. Plant, Cell Environ 29:571–583
Manos PS, Doyle JJ, Nixon KC (1999) Phylogeny, biogeography, and processes of molecular differentiation in Quercus subgenus Quercus (Fagaceae). Mol Phylogenet Evol 12:333–349
McDowell N, Pockman W, Allen C, Breshears D, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DG, Yepez EZ (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol 178:719–739
McIntyre PJ, Thorne JH, Dolanc CR, Flint AL, Flint LE, Kelly M, Ackerly DD (2015) Twentieth-century shifts in forest structure in california: Denser forests, smaller trees, and increased dominance of oaks. Proc Natl Acad Sci 112:1458–1463. doi:10.1073/pnas.1410186112
Meinzer FC, Woodruff DR, Marias DE, McCulloh KA, Sevanto S (2014) Dynamics of leaf water relations components in co-occurring iso- and anisohydric conifer species. Plant, Cell Environ 37:2577–2586. doi:10.1111/pce.12327
Melcher PJ, Zwieniecki MA, Holbrook NM (2003) Vulnerability of xylem vessels to cavitation in sugar maple. scaling from individual vessels to whole branches. Plant Physiol 131:1775
Melcher PJ, Michele Holbrook N, Burns MJ, Zwieniecki MA, Cobb AR, Brodribb TJ, Choat B, Sack L (2012) Measurements of stem xylem hydraulic conductivity in the laboratory and field. Methods Ecol Evol 3:685–694. doi:10.1111/j.2041-210X.2012.00204.x
Mencuccini M, Comstock J (1997) Vulnerability to cavitation in populations of two desert species, Hymenoclea salsola and Ambrosia dumosa, from different climatic regions. J Exp Bot 48:1323–1334
Mencuccini M, Minunno F, Salmon Y, Martínez-Vilalta J, Hölttä T (2015) Coordination of physiological traits involved in drought-induced mortality of woody plants. New Phytol. doi:10.1111/nph.13461
Moritz MA, Parisien M-A, Batllori E, Krawchuk MA, Van Dorn J, Ganz DJ, Hayhoe K (2012) Climate change and disruptions to global fire activity. Ecosphere 3: art49
Muller CH (1940) Oaks of Trans-Pecos Texas. Am Midl Nat 24:703–728
Nielsen-Gammon JW (2012) The 2011 Texas drought. Texas Water J 3:59–95
Nolan RH, Mitchell PJ, Bradstock RA, Lane PN (2014) Structural adjustments in resprouting trees drive differences in post-fire transpiration. Tree Physiol 4:123–136
Ogle K, Barber JJ, Willson C, Thompson B (2009) Hierarchical statistical modeling of xylem vulnerability to cavitation. New Phytol 182:541–554
Pausas JG, Pratt RB, Keeley JE, Jacobsen AL, Ramirez AR, Vilagrosa A, Paula S, Kaneakua-Pia IN, Davis SD (2015) Towards understanding resprouting at the global scale. New Phytol. doi:10.1111/nph.13644
Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-Plus. Springer, New York
Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2015) nlme: linear and nonlinear mixed effects models. http://CRAN.R-project.org/package=nlme
Pittermann J, Sperry JS, Wheeler JK, Hacke UG, Sikkema EH (2006) Mechanical reinforcement of tracheids compromises the hydraulic efficiency of conifer xylem. Plant, Cell Environ 29:1618–1628
Plavcová L, Hacke UG (2012) Phenotypic and developmental plasticity of xylem in hybrid poplar saplings subjected to experimental drought, nitrogen fertilization, and shading. J Exp Bot. doi:10.1093/jxb/ers303
Pockman WT, Sperry JS (2000) Vulnerability to xylem cavitation and the distribution of Sonoran desert vegetation. Am J Bot 87:1287–1299
Poulos HM (2014) Tree mortality from a short-duration freezing event and global-change-type drought in a Southwestern piñon-juniper woodland. USA PeerJ 2:e404. doi:10.7717/peerj.404
Poulos HM, Camp AE (2010) Topographic influences on vegetation mosaics and tree diversity in the Chihuahuan Desert Borderlands. Ecology 91:1140–1151
Poulos HM, Taylor AH, Beaty RM (2007) Environmental controls on dominance and diversity of woody plant species in a Madrean, Sky Island ecosystem, Arizona, USA. Plant Ecol 193:15–30. doi:10.1007/s11258-006-9245-x
Powell AM (1998) Trees & shrubs of the Trans-Pecos and adjacent areas. University of Texas Press
Pratt RB, North GB, Jacobsen AL, Ewers FW, Davis SD (2010) Xylem root and shoot hydraulics is linked to life history type in chaparral seedlings. Funct Ecol 24:70–81. doi:10.1111/j.1365-2435.2009.01613.x
Pratt RB, Jacobsen AL, Ramirez AR, Helms AM, Traugh CA, Tobin MF, Heffner MS, Davis SD (2014) Mortality of resprouting chaparral shrubs after a fire and during a record drought: physiological mechanisms and demographic consequences. Glob Chang Biol 20:893–907
Pratt R, MacKinnon E, Venturas M, Crous C, Jacobsen A (2015) Root resistance to cavitation is accurately measured using a centrifuge technique. Tree Physiol 35:185–196
Ramirez A, Pratt R, Jacobsen A, Davis S (2012) Exotic deer diminish post-fire resilience of native shrub communities on Santa Catalina Island, southern California. Plant Ecol 213:1037–1047
Rigling A, Bigler C, Eilmann B, Feldmeyer-Christe E, Gimmi U, Ginzler C, Graf U, Mayer P, Vacchiano G, Weber P et al (2013) Driving factors of a vegetation shift from scots pine to pubescent oak in dry alpine forests. Glob Change Biol 19:229–240
Savage JA, Cavender-Bares JM (2011) Contrasting drought survival strategies of sympatric willows (genus: Salix): Consequences for coexistence and habitat specialization. Tree Physiol 31:604–614
Schwilk DW, Ackerly DD (2001) Flammability and serotiny as strategies: correlated evolution in pines. Oikos 94:326–336
Schwilk DW, Gaetani MS, Poulos HM (2013) Oak bark allometry and fire survival strategies in the Chihuahuan Desert Sky Islands, Texas, USA. PLoS ONE 8:e79285
Sperry J, Saliendra N (1994) Intra-and inter-plant variation in xylem cavitation in Betula occidentalis. Plant, Cell Environ 17:1233–1241
Sperry JS, Hacke UG, Pittermann J (2006) Size and function in conifer tracheids and angiosperm vessels. Am J Bot 93:1490–1500
Sperry JS, Meinzer FC, McCulloh KA (2008) Safety and efficiency conflicts in hydraulic architecture: scaling from tissues to trees. Plant, Cell Environ 31:632–645
Sperry JS, Christman MA, Torres-Ruiz JM, Taned H, Smith DD (2012) Vulnerability curves by centrifugation: is there an open vessel artifact, and are “r” shaped curves necessarily invalid?
Taneda H, Sperry JS (2008) A case-study of water transport in co-occurring ring-versus diffuse-porous trees: contrasts in water-status, conducting capacity, cavitation and vessel refilling. Tree Physiol 28:1641–1651
Tardieu F, Simonneau T (1998) Variability among species of stomatal control under fluctuating soil water status and evaporative demand: modelling isohydric and anisohydric behaviours. J Exp Bot 49:419
Tobin MF, Pratt RB, Jacobsen AL, De Guzman ME (2013) Xylem vulnerability to cavitation can be accurately characterised in species with long vessels using a centrifuge method. Plant Biol 15:496–504
Tyree MT, Sperry JS (1989) Vulnerability of xylem to cavitation and embolism. Annu Rev Plant Biol 40:19–36
Tyree MT, Zimmermann MH (2002) Xylem structure and the ascent of sap, 2nd edn. Springer, Heidelberg
Tyree MT, Davis SD, Cochard H (1994) Biophysical perspectives of xylem evolution: is there a tradeoff of hydraulic efficiency for vulnerability to dysfunction? IAWA J 15:335–360
Tyree MT, Engelbrecht BM, Vargas G, Kursar TA (2003) Desiccation tolerance of five tropical seedlings in Panama. Relationship to a field assessment of drought performance. Plant Physiol 132:1439
Urli M, Lamy J-B, Sin F, Burlett R, Delzon S, Porté A (2015) The high vulnerability of Quercus robur to drought at its southern margin paves the way for Quercus ilex. Plant Ecol 216:177–187. doi:10.1007/s11258-014-0426-8
Utsumi Y, Bobich EG, Ewers FW (2010) Photosynthetic, hydraulic and biomechanical responses of Juglans californica shoots to wildfire. Oecologia 164:331–338
von Arx G, Archer SR, Hughes MK (2012) Long-term functional plasticity in plant hydraulic architecture in response to supplemental moisture. Annal Bot 109:1091–1100
Waring EF, Schwilk DW (2014) Plant dieback under exceptional drought driven by elevation, not by plant traits, in Big Bend National Park, Texas, USA. PeerJ 2:e477. doi:10.7717/peerj.477
Warshall P (1994) The Madrean sky island archipelago: A planetary overview. In: Proceedings of biodiversity and management of the madrean archipelago: The Sky Islands of Southwestern United States and Northwestern Mexico, Tucson, AZ. USDA Forest Service, Rocky Mountain Forest; Range Experiment Station, RM-GTR-264,
Wheeler JK, Sperry JS, Hacke UG, Hoang N (2005) Inter-vessel pitting and cavitation in woody rosaceae and other vesselled plants: a basis for a safety versus efficiency trade-off in xylem transport. Plant, Cell Environ 28:800–812
Whitehead D, Jarvis PG, Waring RH (1984) Stomatal conductance, transpiration, and resistance to water uptake in a pinus sylvestris spacing experiment. Can J For Res 14:692–700
Whittaker RH, Niering WA (1965) Vegetation of the Santa Catalina Mountains, Arizona: II a gradient analysis of the south slope. Ecology 46:429–452
Willson CJ, Jackson RB (2006) Xylem cavitation caused by drought and freezing stress in four co-occurring Juniperus species. Physiol Plant 127:374–382. doi:10.1111/j.1399-3054.2006.00644.x
Wortemann R, Herbette S, Barigah TS, Fumanal B, Alia R, Ducousso A, Gomory D, Roeckel-Drevet P, Cochard H (2011) Genotypic variability and phenotypic plasticity of cavitation resistance in Fagus sylvatica L. across Europe. Tree Physiol 31:1175–1182
Zeppel MJ, Harrison SP, Adams HD, Kelley DI, Li G, Tissue DT, Dawson TE, Fensham R, Medlyn BE, Palmer A et al (2015) Drought and resprouting plants. New Phytol 206:583–589
Acknowledgments
We thank Anna Jacobsen, Brandon Pratt, and Mike Tobin for sharing techniques and helping trouble-shoot our conductivity measurement methods. A grant from the Appleton-Whittell Research Ranch to R. Lackey supported some of our early work in this system and helped us develop methods and a grant from the USGS South-Central Climate Science Center to D. Schwilk supported some of the later work. T. Brown and J. Willms were in part supported by a Howard Hughes Medical Institute grant through the Undergraduate Biological Sciences Education Program to Texas Tech University. We thank Jason Wrinkle, Greg Crow, and the other helpful staff of the Nature Conservancy for essential support of this work. We thank the associate editor and two anonymous reviewers for very helpful comments on an earlier version of this manuscript. This article is dedicated to the memory of Christopher Rodriguez who planned to investigate drought susceptibility of post-fire oak resprouts and whose enthusiasm for learning and excitement for the project inspired others to continue.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Prof. Michael Lawes, Prof. Ross Bradstock, and Prof. David Keith.
Rights and permissions
About this article
Cite this article
Schwilk, D.W., Brown, T.E., Lackey, R. et al. Post-fire resprouting oaks (genus: Quercus) exhibit plasticity in xylem vulnerability to drought. Plant Ecol 217, 697–710 (2016). https://doi.org/10.1007/s11258-016-0568-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11258-016-0568-y