Abstract
As trees grow tall and the resistance of the hydraulic pathway increases, water supply to foliage may decrease forcing stomata to close and CO2 uptake to decline. Several structural (e.g. biomass allocation) and physiological adjustments, however, may partially or fully compensate for such hydraulic constraints and prevent limitations on CO2 uptake and growth. The degree to which trees compensate for hydraulic constraints as they grow tall may depend on the costs and benefits associated with hydraulic compensation according to their ecology and life history. Because later successional Rocky Mountain conifers are more shade tolerant, optimization of CO2 uptake as trees grow tall and shade increases may confer greater benefits than in earlier successional species. If so, higher compensation for hydraulic constraints is expected in later successional species relative to co-occurring earlier successional species. I have examined height-related changes of crown stomatal conductance on a leaf area basis (G LA) and leaf to sapwood ratios (A L:A S) for five conifer species in the northern Rocky Mountains. Species were arranged in pairs, each pair consisting of an early and late successional species. For high elevations I used, respectively, whitebark pine (Pinus albicaulis) and subalpine fir (Abies lasiocarpa); for mid-elevations, western larch (Larix occidentalis) and Douglas-fir (Pseudotsuga menziesii); for lower elevations, ponderosa pine (Pinus ponderosa) and Douglas-fir. A L:A S either decreased (subalpine fir, ponderosa pine), remained constant (Douglas-fir, western larch) or increased (whitebark pine) with tree height. As hypothesized, earlier successional species (ponderosa pine, whitebark pine and western larch) exhibited significantly stronger decreases of G LA with tree height relative to their later successional pairs (Douglas-fir and subalpine fir), which fully compensated for height-related hydraulic constraints on G LA. A life history approach that takes into account the optimization of size- and species-specific ecological functions may also help researchers better understand biomass allocation and hydraulic function in trees.
Similar content being viewed by others
References
Addington RN, Donovan LA, Mitchell RJ, Vose JM, Pecot SD, Jack SB, Hacke UG, Sperry JS, Oren R (2006) Adjustments in hydraulic architecture of Pinus palustris maintain similar stomatal conductance in xeric and mesic habitats. Plant Cell Environ 29:535–545
Barnard HR, Ryan MG (2003) A test of the hydraulic limitation hypothesis in fast-growing Eucalyptus saligna. Plant Cell Environ 26:1235–1245
Becker P (1998) Limitations of a compensation heat pulse velocity system at low sap flow: implications for measurements at night in shaded trees. Tree Physiol 18:177–184
Becker P, Meinzer FC, Wullschleger SD (2000) Hydraulic limitation of tree height: a critique. Funct Ecol 14:4–11
Bond BJ, Ryan MG (2000) Comment on ‘Hydraulic limitation of tree height: a critique’ by Becker, Meinzer & Wullschleger. Funct Ecol 14:135–140
Bond BJ, Farnsworth BT, Coulombe RA, Winner WE (1999) Foliage physiology and biochemistry in response to light gradients in conifers with varying shade tolerance. Oecologia 120:183–192
Buckley TN, Roberts DW (2005) How should leaf area, sapwood area and stomatal conductance vary with tree height to maximize growth? Tree Physiol 26:145–157
Callaway RM, Sala A, Keane RE (2000) Succession may maintain high leaf area: sapwood area ratios and productivity in old subalpine forests. Ecosystems 3:254–268
Campbell GS, Norman JM (1998) An introduction to environmental biophysics. Springer, Berlin Heidelberg New York
Campbell GS, Calissendorff C, Williams JH (1991) Probe for measuring soil specific heat using a heat pulse method. Soil Sci Soc Am J 55:291–293
Clark JS (1996) Testing disturbance theory with long-term data: alternative life-history solutions to the distribution of events. Am Nat 148:976–996
Cohen Y, Fuchs M (1989) Problems in the heat pulse method for measuring sap flow in the stem of trees and herbaceous plants. Agronomie 9:321–326
Cohen Y, Fuchs M, Green GC (1981) Improvement of the heat pulse method for determining sap flow in trees. Plant Cell Environ 4:391–397
Cohen Y, Kelliher FM, Black TA (1985) Determination of sap flow in Douglas-fir (Pseudotsuga menziesii) tree using the heat pulse technique. Can J For Res 15:422–428
Coyea MR, Margolis HA (1992) Factors affecting the relationship between sapwood area and leaf area of balsam fir. Can J For Res 22:1684–1693
Delzon S, Sartore M, Burlett R, Dewar, Loustau D (2004) Hydraulic responses to height growth in maritime pine trees. Plant Cell Environ 27:1077–1087
Fischer DG, Kolb TE, DEWald LE (2002) Changes in whole-tree water relations during ontogeny of Pinus flexilis and Pinus ponderosa in a high elevation meadow. Tree Physiol 22:675–685
Ford CR, McGuire MA, Mitchell RJ, Teskey RO (2004) Assessing variation in the radial profile of sap flux density in Pinus species and its effect on daily water use. Tree Physiol 24:241–249
Friend AD (1993) The prediction and physiological significance of tree height. In: Solomon AM, Shugart HH (eds) Vegetation dynamics and global change. Chapman & Hall, New York, pp 101–115
Goldstein G, Andrade JL, Meinzer FC, Holbrook NM, Cavelier J, Jackson P, Celis A (1998) Stem water storage and diurnal patterns of water use in tropical forest canopy trees. Plant Cell Environ 21:397–406
Govindaraju DR (1984) Mode of colonization and patterns of life history in some North American conifers. Oikos 43:271–276
Greene DF, Johnson EA (1994) Estimating the mean annual seed production of trees. Ecology 75:642–647
Hellqvist J, Hillerdal-Hagströmer K, Mattson-Djos E (1980) Field studies of water relations and photosynthesis in Scots pine using manual techniques. Ecol Bull (Stockholm) 32:183–204
Henery ML, Westoby M (2001) Seed mass and seed nutrient content as predictors of seed output variation between species. Oikos 92:479–490
Hubbard RM, Bond BJ, Ryan MG (1999) Evidence that hydraulic conductance limits photosynthesis in old Pinus ponderosa trees. Tree Physiol 19:165–172
King DA (1990) The adaptive significance of tree height. Am Nat 135:809–828
Kira T, Shidei T (1967) Primary production and turnover of organic matter in different forest ecosystems of the western Pacific. Jan J Ecol 13:70–83
Kloeppel BD, Gower ST, Vogel JG, Reich PB (2000) Leaf-level resource use for evergreen and deciduous conifers along a resource availability gradient. Funct Ecol 14:281–292
Koch GW, Sillett SC, Jennings GM, Davis SD (2004) The limits of tree height. Nature 428:851–854
Koenig WD, Knops JMH (1998) Scale of mast-seeding and tree-ring growth. Nature 396:225–226
Körner C (2003) Carbon limitation in trees. J Ecol 91:4–17
Köstner B, Falge E, Tenhunen JD (2002) Age-related effects on leaf area/sapwood area relationships, canopy transpiration and carbon gain of Norway spruce stands (Picea abies) in the Fichtelgebirge, Germany. Tree Physiol 22:567–574
Kutscha NP, Sachs IB (1962) Color tests for differentiating heartwood and sapwood in certain softwood species. US Forestry Products Laboratory Report No 2246
Loehle C (1988) Tree life history strategies: the role of defenses. Can J For Res 18:209–222
Magnani F, Mencuccini M, Grace J (2000) Age-related decline in stand productivity: the role of structural acclimation under hydraulic constraints. Plant Cell Environ 23:251–263
Makkonen K, Helmisaari HS (2001) Fine root biomass and production in Scots pine stands in relation to stand age. Tree Physiol 21:193–198
McDowell NG, Barnard H, Bond BJ, Hinckley TM, Hubbard RM, Ishii H, Köstner B, Magnani F, Marshall JD, Meinzer FC, Phillips N, Ryan MG, Whitehead D (2002a) The relationship between tree height and leaf area: sapwood area ratio. Oecologia 132:12–20
McDowell NG, Phillips N, Lunch C, Bond BJ, Ryan MG (2002b) An investigation of hydraulic limitation and compensation in large, old Douglas-fir trees. Tree Physiol 22:763–774
Mencuccini M (2003) The ecological significance of long-distance water transport: short-term regulation, long-term acclimation and the hydraulic costs of stature across plant life forms. Plant Cell Environ 26:163–182
Mencuccini M, Grace J (1996) Developmental patterns of above-ground hydraulic conductance in a Scots pine (Pinus sylvestris L.) age sequence. Plant Cell Environ 18:357–364
Mencuccini M, Magnani F (2000) Comment on ‘Hydraulic limitation of tree height: a critique’ by Becker, Meinzer & Wullschleger. Funct Ecol 14:135–140
Mencuccini M, Martinez-Vilalta J, Vanderklein D, Hamid HA, Korakaki E, Lee S, Michiels B (2005) Size-mediated ageing reduces vigour in trees. Ecol Lett 8:1183–1190
Monserud RA, Marshall JD (1999) Allometric crown relations in three northern Idaho conifer species. Can J For Res 29:521–535
Noble IR, Sltayer RO (1980) The use of vital attributes to predict successional changes in plant communities subject to recurrent disturbances. Vegetatio 43:5–21
O’Hara KL, Valappil NI (1995) Sapwood-leaf area prediction equations for multi-aged ponderosa pine stands in western Montana and central Oregon. Can J For Res 25:1553–1557
Oren R, Werk KS, Schulze E-D (1986) Relationships between foliage and conducting xylem in Picea abies (L.) Karst. Trees 1:61–69
Pausch RC, Grote EE, Dawson TE (2000) Estimating water use by sugar maple trees: considerations when using heat-pulse methods in trees with deep functional sapwood. Tree Physiol 20:217–227
Pfister RD, Kovalchik BL, Arno SF, Presby RC (1977) Forest habitat types of Montana. USDA For Serv, Gen Tech Rep INT-34
Phillips NG, Bond BJ, McDowell NG, Ryan MG (2002) Canopy and hydraulic conductance in young, mature and old Douglas-fir trees. Tree Physiol 22:205–211
Phillips NG, Ryan MG, Bond BJ, McDowell NG, Hinckley TM, Čermák J (2003) Reliance on stored water increases with tree size in three species in the Pacific Northwest. Tree Physiol 23:237–245
Phillipson JJ (1990) Prospects for enhancing flowering of conifers and broadleaves of potential silvicultural importance in Britain. Forestry 63:223–240
Richardson SJ, Allen RB, Whitehead D, Carswell FE, Ruscoe WA, Platt KH (2005) Climate and net carbon availability determine temporal patterns of seed production by Nothofagus. Ecology 86:971–981
Rundel PW, Yoder BJ (1998) Ecophysiology of Pinus. In: Richardson DM (ed) Ecology and biogeography of Pinus. Cambridge University Press, New York, pp 296–323
Ryan MG, BJ Yoder (1997) Hydraulic limits to tree height and growth. Bioscience 47:235–242
Ryan MG, Bond BJ, Law BE, Hubbard RM, Woodruff D, Cienciala E, Kucera J (2000) Transpiration and whole-tree conductance in ponderosa pine trees of different heights. Oecologia 124:553–560
Sala A, Carey EV, Callaway RM (2001a) Dwarf mistletoe affects whole-tree water relations of Douglas-fir and western larch primarily through changes in leaf to sapwood ratios. Oecologia 126:42–52
Sala A, Carey EV, Keane RE, Callaway RM (2001b) Water use by whitebark pine and subalpine fir: potential consequences of fire exclusion in the northern Rocky Mountains. Tree Physiol 21:717–725
Schäfer KVR, Oren R, Tenhunen JD (2000) The effect of tree height on crown level stomatal conductance. Plant Cell Environ 23:365–375
Schiller G, Cohen Y (1998) Water balance of Pinus halepensis Mill. afforestation in an arid region. For Ecol Manage 105:121–128
Selås V, Piovesan G, Adams JM, Bernabei M (2002) Climate factors controlling reproduction and growth of Norway spruce in southern Norway. Can J For Res 32:217–225
Simpson DG (2000) Water use of interior Douglas-fir. Can J For Res 30:534–547
Tomback DF, Arno SF, Keane RE (2001) The compelling case for management intervention. In: Tomback DF, Arno SF, Keane RE (eds) Whitebark pine communities: ecology and restoration. Island Press, Washington, D.C., pp 3–25
Tyree MT, Sperry JS (1989) Vulnerability of xylem to cavitation and embolism. Annu Rev Plant Physiol Mol Biol 40:19–38
West GB, Brown JH, Enquist BJ (1999) A general model for the structure and allometry of plant vascular systems. Nature 400:664–667
Woodruff DR, Bond BJ, Meinzer FC (2004) Does turgor limit growth in tall trees? Plant Cell Environ 27:229–236
Wullschleger SD, Meinzer FC, Vertessy RA (1998) A review of whole-plant water use studies in trees. Tree Physiol 18:499–512
Yamauchi A (1996) Theory of mast reproduction in plants: storage-size dependent strategy. Evolution 50:1795–1807
Yoder BJ, Ryan MG, Waring RH, Schoettle AW, Kaufmann MR (1994) Evidence of reduced photosynthetic rates in old trees. For Sci 40:513–527
Acknowledgements
This research was supported by grants from the USDA Forest Service, Rocky Mountain Research Station, INT-95086-RJVA to R. Callaway and A. Sala, USDA NRIGCP 95-37101-1683 to R. Callaway and USDA NRIGP 97-35106-5061 to A. Sala. I am particularly indebted to R. Callaway for his enthusiasm, generosity with the data and helpful comments on the manuscript. This work could not have been possible without the help of E. Carey, R. Keane and S. Arno. I am very thankful to L. Ashley, E. Aschehoug, J. Bickley, T. Byker, T. Carlson, A. Carroll, K. Corwall, W. Foster, G. Hammon, T. Laboski, S. Mincemoyer, J. Moran, T. Palm, K. Simonin, J. Smith and G. Thelen for their invaluable help in the field and in the laboratory. Thanks to C. Fiedler, B. Rich, V. Applegate and F. Mauss for their help during site selection and to B. Geils, J. Schloss, and E. DeLucia for the loan of data loggers. J. Maron, E. Crone and two reviewers provided very helpful comments on earlier versions of this manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Todd E. Dawson
Rights and permissions
About this article
Cite this article
Sala, A. Hydraulic compensation in northern Rocky Mountain conifers: does successional position and life history matter?. Oecologia 149, 1–11 (2006). https://doi.org/10.1007/s00442-006-0420-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-006-0420-5