George Koch, Northern Arizona University; Stephen Sillett and Gregg Jennings, Humboldt State University; Stephen Davis, Pepperdine University

May, 2006

Plants grow tall where light competition is relatively strong and other essential resources–water and nutrients–are readily available and temperatures are not extreme. Thus, the tallest trees are found in temperate regions having high rainfall, moderate temperatures, and relatively fertile soils. The tallest trees on Earth today are coast redwoods, Sequoia sempervirens, of northern California. A total of 113 living redwoods are over 107 m tall, and the tallest individual is 112.5 m in height (Figure 1). Because 95% of the original redwood forests, including most prime habitat, has been logged, it is likely that individuals taller than today's record holders existed in the past. Anecdotal evidence indicates that individuals of Douglass fir, Pseudotsuga menziesii, from Washington and British Columbia may have exceeded 120 m, and mountain ash, Eucalyptus regnans, of Victoria, Australia may have been as tall as 114 m.

Figure 1   Stratosphere Giant, the tallest known living tree, 112.34 m (368' 7"), located in Humboldt County, California. Note researcher descending (circled in yellow). Photo by Thomas B. Dunklin.

What limits the height growth of trees has long puzzled plant physiologists. The respiratory burden of large support structures, declining nutrient availability, and mechanical failure have all been proposed, but largely dismissed. Recently the "hydraulic limitation hypothesis" of Ryan and Yoder (1997) has sparked interest in whether constraints on the capacity of the hydraulic system to deliver water to upper crown foliage might become increasingly limiting to stomatal conductance and photosynthesis as trees grow taller, thereby reducing carbon availability for further height growth. As trees grow taller, a larger soil-to-leaf water potential gradient is required to overcome the effect of gravity and the increased hydraulic resistance of a longer flow pathway. Low leaf water potential, however, causes a reduction in stomatal aperture, which reduces transpiration and counteracts further reduction in water potential, but also reduces photosynthesis. Why should stomatal conductance be reduced as water potential declines? First, it would act to maintain cell turgor pressure, which is needed for cell expansion. Second, and perhaps more important, it acts to reduce the risk of xylem cavitation, which if unchecked can lead to the death of shoots, branches, or entire trees (Tyree and Sperry, 1988). The postulated mechanism underlying the hydraulic limitation hypothesis of Ryan and Yoder (1997) implies that trees should grow to a physiological "ceiling" height that reflects the tradeoff between turgor maintenance or cavitation avoidance on the one hand and photosynthetic carbon gain on the other, with the balance of these factors being determined by the regulation of stomatal conductance.

To test whether stomatal limitation of photosynthesis might underlie the limits to tree height, we examined patterns of water potential, gas exchange, carbon isotope composition, and xylem vulnerability to cavitation in coast redwood trees at sites along the northern California coast.

The Experiments

Using standard rope techniques, we accessed the crowns of trees ranging in height from 95 m to 112.3 m with ecophysiological equipment (Figure 2). We measured xylem pressure potential with a Scholander-Hammel type pressure chamber (see Web Topic 3.5) on stems cut approximately 20 cm from the shoot tip. Photosynthesis, stomatal conductance, and transpiration were measured in ambient conditions of light, temperature, and vapor pressure with a LI6400 portable photosynthesis system (LiCor Inc. Lincoln, NE). Foliar carbon isotope composition (?¹³C, ‰) of dried and ground foliage was analyzed by isotope ratio mass spectrometry at the Colorado Plateau Stable Isotope Laboratory and used as an indicator of the time-integrated ratio of leaf internal to ambient CO₂ concentration (C_i/C_a; see textbook Chapter 9 and Web Topic 9.5; Farquhar et al., 1982). Xylem vulnerability to cavitation was measured by the centrifuge method (Pockman et al., 1995) on branch segments (8 to 9 mm diam.) collected in the upper crown (avg. ht. = 110 m) and lower crown (avg. ht. = 57 m) of 6 trees.

Figure 2   a) Rope technique used to access crown of coast redwoods. (b,c) Working platforms for ecophysiological studies. Note large epiphytic fern mat below researcher in c. a,c, photos by George Koch; b, photo by Thomas B. Dunklin.

The Results

Xylem pressure was strongly correlated with height, both at predawn and at midday when the leaf-to-air vapor pressure difference was highest (Figure 3, Part A). The slopes of the predawn gradients were not significantly different from that necessary to hold water against gravity (ca. –0.01 MPa m^–1). Slopes of midday gradients did not differ from predawn gradients during the wet season, but during the dry season were significantly higher for some trees, up to –0.014 MPa m^–1, indicative of the increased driving force necessary to move water rapidly through the xylem. Minimum xylem pressures were always above –2.0 MPa in the upper crown, similar to that of other conifers (Pinol and Sala, 2000).

Figure 3   (a) Height profiles of xylem pressure at predawn (open symbols) and midday (filled symbols) during the dry season for three coast redwood trees. (b) Height profiles of foliar carbon isotope composition for the same trees as in a.

Stomatal conductance and photosynthesis measured at saturating light in the upper crown (ca. 105 m) during the dry season decreased by an average of 43% and 33%, respectively, from mid-morning when air vapor pressure deficit (VPD) and xylem tension were low to mid afternoon when VPD and xylem tension reached their daily maxima. Values of C_i/C_a calculated from gas exchange measurements spanned a range that included the time-integrated estimates based on stable carbon isotope analysis (see below). Thus, stomatal conductance near maximum tree height responds to conditions associated with increasing water stress and is strongly limiting to photosynthesis at midday during the dry season.

Stable carbon isotope composition (?¹³C) of foliage was strongly and positively correlated with height in all study trees (Figure 3, Part B). Maximum values of nearly –21‰ at the tops of the tallest trees indicate low C_i/C_a ratios similar to those for perennial plants from extremely arid environments. Minimum δ¹³C within the crown ranged from –27‰ to –31‰ (see textbook, pp. 220–222), values indicating minor stomatal limitation of photosynthesis as occurs in plants from mesic environments.

Mean water potential for 50% cavitation (Ψ_50%) was estimated to be –6.1 MPa for all branches measured. In paired branches from upper and lower crown positions in each of 6 trees, lower crown branches were always more susceptible to water-stress-caused-embolism than top branches (Ψ_50% lower = –5.6 MPa, upper = –6.6 MPa, paired t-test: df = 5, t = –3.47, p = 0.018). The observed difference in Ψ_50% between upper and lower branches was not significantly different from the difference in the hydrostatic component of water potential between these heights (paired t-test: df = 5, t = –1.69, p = 0.15).

What Does It All Mean?

Our results for coast redwood support elements of the hydraulic limitation hypothesis of Ryan and Yoder (1997). We found that water potential increases with height as expected from the cohesion-tension model of water transport in plants (see Web Essay 4.3). Because the slope of this relationship was generally close to the gravitational potential gradient, it appears that the long transport path in tall redwoods does not impose a large amount of resistance to water flow. We note, however, that our study trees are all located in sites where soils are very moist throughout most years. The intercepts of the predawn water potential curves estimate that soil Ψ remained close to 0 MPa even during the dry season. It is likely that redwood trees experience larger soil water deficits on hill slopes and ridge tops, in very dry years, and toward the southern and inland limits of the species' distribution. In such conditions we expect the water potential gradient to be steeper and tree top values of water potential to be lower (more negative) than the minimum of about –2 MPa we measured.

Values of foliar δ¹³C were strongly correlated with height in all study trees, indicating that stomatal conductance becomes increasingly limiting to photosynthesis with height. Strong vertical gradients of light are common in dense forests, and this alone would tend to increase photosynthetic capacity in the upper crown and drive C_i lower even if stomatal conductance was invariant with height. While we do not yet know how stomatal conductance and photosynthesis vary with height, we expect that maximum values are higher in the upper crown. Our gas exchange data indicate that conductance is strongly regulated in the treetop, and we believe stomatal regulation is the main reason behind the high δ¹³C values in the upper crown. The δ¹³C values at the tree top approached –21‰, remarkably high considering redwoods occur in very moist environments.

A major component of the hydraulic limitation hypothesis is that stomatal conductance declines in response to low water potential. The observation of a decline in conductance at the time of day of minimum water potential supports this hypothesis. Stomatal conductance may decrease to reduce the risk of xylem cavitation. Given this, a surprising aspect of our study is the high resistance to cavitation observed in coast redwood. Essentially no loss of hydraulic conductivity (i.e., cavitation) was observed at water potentials near the minimum experienced during the dry season.

The large apparent safety margin for xylem cavitation in redwood contrasts with a number of other studies (Sperry, 1995) and has several possible explanations. First, xylem cavitation may be irreversible at great heights in tall trees because re-dissolution of gas emboli requires low xylem tensions, within a few tenths of a MPa, a situation that is precluded by the water potential necessary simply to hold water against gravity above a few tens of meters of height. Thus, redwood may be "over engineered" because the consequences of cavitation are particularly severe. Second, the high cavitation resistance of redwood may be advantageous during extreme and long-lasting droughts, which impose water potentials much lower than we have measured in the field. Such dry periods are known to have occurred during the past millennium and within the lifetime of our study trees. Finally, it may be that the hydraulic characteristics of redwood stems are in part byproducts of other features related to extreme height growth, (e.g., wood mechanical properties).

A final interesting note on redwood physiology concerns the role of fog in the water relations of this species. Summer fog characterizes much of redwood's geographic distribution. Dawson (1998) has clearly documented the importance of fog drip for soil moisture and root uptake. Recently, we have measured the capacity for direct foliar uptake of fog in coast redwood. Simulated fog events resulted in a significant increase in water potential compared to foliage covered with aluminum foil to prevent transpiration (Koch et al., unpublished data). Although we do not yet know the quantitative importance of direct absorption of fog, it does represent a means of acquiring water that circumvents the energetic requirement of lifting it from the soil. It is noteworthy that we have observed xylem pressures higher than the hydrostatic gradient following nights of rain or fog. Could it be that foliar absorption provides a mechanism for xylem tension to relax to the point where cavitation reversal is possible? We are confident that further study of coast redwood across a range of environments will answer this question and reveal the critical elements of physiology and functional morphology that affect and are affected by plant size.

References

Dawson, T. E. (1998) Fog in the redwood forest: Ecosystem inputs and use by plants. Oecologia 117: 476–485.

Farquhar, G. D., O'Leary, M. H., and Berry, J. A. (1982) On the relationship between carbon isotope discrimination and intercellular carbon dioxide concentration in leaves. Australian Journal of Plant Physiology 9: 121–137.

Pinol, J., and Sala, A. (2000) Ecological implications of xylem cavitation for several Pinaceae in the Pacific Northwestern USA. Functional Ecology 14: 538–545.

Pockman, W. T., Sperry, J. S., and O'Leary, J. W. (1995) Sustained and significant negative water pressure in xylem. Nature 378: 715–716.

Ryan, M. G., and Yoder, B. J. (1997) Hydraulic limits to tree height and tree growth. BioScience 47(4): 235–242.

Sperry, J. S. (1995) Limitations on stem water transport and their consequences. In Plant Stems: Physiology and Functional Morphology, B. L. Gartner, ed. Academic Press, San Diego, pp. 105–124.

Tyree, M. T., and Sperry, J. S. (1988) Do woody plants operate near the point of catastrophic xylem dysfunction caused by water stress? Plant Physiology 88: 574–580.