Boston University Graduate School of Arts And
Transcript of Boston University Graduate School of Arts And
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Copyright by
HEIDI J. RENNINGER2010
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Approved by
First Reader ____________________________________________________Nathan G. Phillips, PhD
Associate Professor of Geography and Environment
Boston University
Second Reader ____________________________________________________
Guido Salvucci, PhDProfessor of Earth Sciences, Geography and Environment and
Chairman, Department of Earth SciencesBoston University
Third Reader ____________________________________________________
Mark Friedl, PhDProfessor of Geography and Environment
Boston University
Fourth Reader ____________________________________________________
N. Michele Holbrook, PhDProfessor of Biology and Charles Bullard Professor of Forestry,
Department of Organismic and Evolutionary Biology
Harvard University
Fifth Reader ____________________________________________________Curtis Woodcock, PhD
Professor of Geography and Environmentand Center for Energy and
Environmental StudiesBoston University
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ACKNOWLEDGMENTS
Acknowledgement text here
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HYDRAULIC PROPERTIES OF PALMS VARYING IN ONTOGENY AND
ENVIRONMENTAL GROWING CONDITIONS WITH IMPLICATIONS FOR
HYDRAULIC LIMITATION TO INCREASED HEIGHT GROWTH IN TALL
PALMS
(Order No. )
HEIDI J. RENNINGER
Boston University Graduate School of Arts and Sciences, 2010
Major Professor: Nathan G. Phillips, Associate Professor of Geography andEnvironment
ABSTRACT
Palms are an attractive group for physiological research because their columnar
trunks and simplistic leaf habit allow for estimation of variables important for hydraulic
functioning more easily than in more complex arborescent dicotyledons. Likewise,
palms grow in a wide variety of climates from the very dry (Washingtonia robusta in
Southern California) to tropical rainforests (Iriartea deltoidea andMauritia flexuosa)
which allowed for study of palm species across an environmental moisture gradient. As
well, within species comparisons across an ontogenetic gradient were conducted to
examine hydraulic functioning with changes in palm size in order to characterize the
hydraulic limitations and/or compensations that are made as trees grow taller, and
therefore, move water further distances. While both rainforest species exhibited differing
patterns in height growth rate along boles, height growth rates ultimately decreased in the
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tallest palms. Sapflux per unit leaf area was constant across palm height in all three
species, suggesting that taller palms are not showing evidence of hydraulic limitation.
However, inIriartea deltoidea, transpiration was more restricted by stomatal closure in
the dry season compared with the wet season. Both tropical species exhibited contrasting
patterns in both live frond number and frond leaf area with height that led to a
convergence in the pattern of increasing total leaf area with height in both species. In
contrast, sub-tropical Washingtonia robusta exhibited decreasing total leaf areas with
height. BothMauritia flexuosa and Washingtonia robusta showed an increased reliance
on stored water with height which likely compensated for the increased frictional
resistance to water flow. Regarding petiole conductivities, leaf specific conductivity was
similar both within species and between species forIriartea deltoidea and Washingtonia
robusta. As well,Iriartea deltoidea and Washingtonia robusta had similar P50 values
(point at which 50% of hydraulic conductivity is lost) in petioles averaged across height.
Comparing P50 values with measurements of midday leaf water potentials, as well as a
double-dye staining experiment, suggested that a fairly significant amount of embolism is
occurring on a daily basis. This could mean that these palm species, instead of avoiding
embolisms through tight stomatal control, repair embolisms on a daily basis.
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TABLE OF CONTENTS
APPROVAL PAGEiii
ACKNOWLEDGMENTS..................................................................................................iv
ABSTRACT........................................................................................................................v
TABLE OF CONTENTS..................................................................................................vii
CHAPTER 1 .......................................................................................................................1
INTRODUCTION...............................................................................................................1
CHAPTER 2......................................................................................................................22
COMPARATIVE HYDRAULIC AND ANATOMIC PROPERTIES IN PALM TREES
(WASHINGTONIA ROBUSTA) OF VARYING HEIGHTS: IMPLICATIONS FOR
HYDRAULIC LIMITATION TO INCREASED HEIGHT GROWTH...........................22
CHAPTER 3 ....................................................................................................................59
WET VERSUS DRY SEASON TRANSPIRATION IN AN ...........................................59
AMAZONIAN RAINFOREST PALM, IRIARTEA DELTOIDEA.................................59
CHAPTER 4......................................................................................................................94
INTRINSIC AND EXTRINSIC HYDRAULIC FACTORS IN VARYING SIZES OF
TWO AMAZONIAN PALM SPECIES (IRIARTEA DELTOIDEA AND MAURITIA
FLEXUOSA) DIFFERING IN DEVELOPMENT AND GROWING ENVIRONMENT
...........................................................................................................................................94
CHAPTER 5....................................................................................................................137
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HYDRAULIC PROPERTIES AND VULNERABILITY TO EMBOLISM IN PALM
FRONDS FROM SPECIES OF VARYING HEIGHT GROWING IN RAINFOREST
AND SUBTROPICAL ENVIRONMENTS....................................................................137
CHAPTER 6: OVERALL CONCLUSIONS.................................................................183
LITERATURE CITED....................................................................................................183
CURRICULUM VITAE..................................................................................................211
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LIST OF TABLES
Table 2.1: Basic characteristics of the Washingtonia robusta study palms including
number and locations of Granier sensors for each individual...........................................49
Table 2.2: Equations and r2 values for the regressions in Figure 2.3...............................50
Table 2.3: Maximum, minimum, mean and std. errors for the various physiological
variables measured across palm height where n represents the number of palms sampled
for a given variable............................................................................................................51
Table 3.4: Location (stilt root, bole, petiole) and number of Granier heat dissipation
sensors that were inserted and functioning in Iriartea deltoidea palms. Multiple sensors
were located in separate stilt roots and petioles and in opposite sides of the bole. Only
data from functioning sensors were used in the final analysis..........................................86
Table 3.5: Daily averages (standard errors) of micrometeorological and Iriartea deltoidea
sap flux data for both the wet season and dry season........................................................87
Table 5.6: Means and standard errors for Iriartea deltoidea and Mauritia flexuosa, both
Ecuadorian tropical rainforest species, and Washingtonia robusta, a subtropical, dry
climate species growing in Australia. Means with different letters within the same row
were significantly different at
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LIST OF FIGURES
Figure 2.1: Representative diurnal sap flux (g m-2 s-1) (bottom panel) on Julian day 210
from a single outer sapflow sensor for eight individuals of varying heights. The middle
panel represent vapor pressure deficit (VPD) (kPa) and the top panel represents solar
radiative flux density (W m-2). The solar flux sensor was shaded early in the morning,
therefore solar radiation measurements are artificially low in this time interval. The
dotted line represents a clear-day estimate of solar radiation and the likely light
environment for the crowns of the palms..........................................................................52
Figure 2.2: Tree height (m) vs. means and standard errors of (a) total daily bole sap flux
(kg day-1 m-2 leaf area) and (b) total daily petiolar sap flux (kg day-1 m-2 leaf area). For
bole sap flux, standard error bars represent 4 to 8 replicate days and 2 or 3 sensor
locations. For petiole sap flux, standard error bars represent 3 replicate days and 2
petioles...............................................................................................................................53
Figure 2.3: Daily time courses of (a) stomatal conductance (mol H2O m-2 s-1), (b)
photosynthetic assimilation rate (mol CO2 m-2 s-1) and (c) leaf water potentials
(MPa). Closed circles = 2 m palm, open circles = 8 m palm, closed triangles = 18 m
palm, open triangles = 22 m palm, closed squares = 28 m palm, open squares = 34 m
leaning palm. Equations and r2 values are presented in Table 2.2....................................54
Figure 2.4: Tree height (m) vs. (a) maximum daily stomatal conductance (mol H2O m-2
s-1) calculated from the daily time courses of stomatal conductance (Fig. 2.3a), (b)
maximum daily photosynthetic assimilation rate (mol CO2 m-2 s-1) calculated from the
daily time courses of photosynthetic assimilation rate (Fig 2.3b)(y = 0.23x + 10.2) and (c)
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mean leaf mass per area (LMA; g m-2) where std. error bars represent 5 replicate leaflets.
...........................................................................................................................................56
Figure 2.5: Tree height (m) vs. (a) minimum daily leaf water potential (; MPa) (y =
-1.9 x0.18) and (b) the time at which minimum leaf water potential occurred (y =
0.08x + 16.0), both calculated from the daily time courses of leaf water potential (Fig.
2.3c)...................................................................................................................................57
Figure 2.6: Tree height (m) vs. (a) the number of live leaves per palm (y =
44.6 x-0.24), (b) leaf area (m2)(y = 5.59 x -0.55) and (c) average leaf epidermal cell area
(m2) for a given leaf. Errors bars represent the standard error from the two leaves per
palm measured and the standard error around average leaf epidermal cell size. Leaf
epidermal cell sizes for the 28m and 34m palms are significantly lower than the shorter
palms and well as being significantly different from each other (p-value
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Figure 3.8: Calibration of the Granier sensor performed on a piece of small Iriartea
deltoidea bole with sap flux density (u)(m3 m-2 s-1 * 106) vs sap flux index
(T(0)/T(u) 1)..............................................................................................................89
Figure 3.9: Average petiole sap flux from three small Iriartea deltoidea palms for
representative days during (A) the 2006 wet season and (B) the 2007 dry season,
corresponding vapor pressure deficits (VPD) during (C) the 2006 wet season and (D) the
2007 dry season and average bole sap flux from four medium-sized Iriartea deltoidea
palms during (E) the 2006 wet season and (F) the 2007 dry season. Dotted lines
represent standard errors....................................................................................................90
Figure 3.10: Average sap flux of the stilt roots of three large Iriartea deltoidea palms
during representative days in (A) the 2006 wet season and (B) the 2007 dry season,
corresponding vapor pressure deficits (VPD) during (C) the 2006 wet season and (D) the
2007 dry season and average sap flux of the boles of three large Iriartea deltoidea palms
during (E) the 2006 wet season and (F) the 2007 dry season. The dotted lines represent
standard errors...................................................................................................................91
Figure 3.11: Average sap fluxes corresponding to vapor pressure deficit values ranging
from 0.1 to 3.4 kPa in 0.1 kPa increments for (A) the petioles of small palms, (B) the stilt
roots of large palms, (C) the boles of medium-sized palms and (D) the boles of large
palms. Wet-season sap fluxes are represented by the closed circles, dry-season sap fluxes
by the open circles.............................................................................................................92
Figure 3.12: Average sap fluxes corresponding to photosynthetic photon flux density
(PPFD) values ranging from 0 to 2000 (mol/ m2 sec) in 50 mol/ m2 sec increments for
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(A) the petioles of small palms, (B) the stilt roots of large palms, (C) the boles of
medium-sized palms and (D) the boles of large palms. Wet-season sap fluxes are
represented by the closed circles, dry-season sap fluxes by the open circles....................93
Figure 4.13: Internode lengths (m) along the boles of (A) Iriartea deltoidea and (B)
Mauritia flexuosa. Points with standard error bars represent the mean and variance of
four or five individuals....................................................................................................128
Figure 4.14: Relationship between Palm height (m) and (A) number of fronds lost per
year for Iriartea deltoidea (y = -0.062x + 2.56) and Mauritia flexuosa (y = 1.34x0.44), (B)
number of live fronds in Iriartea deltoidea (y = 3.83 x0.17) and Mauritia flexuosa (y =
0.32x +3.62), (C) individual frond leaf area (m2) in Iriartea deltoidea (y = 0.40x +0.64)
and Mauritia flexuosa (y = 3.25 x0.19) and (D) total palm leaf area (m2) in Iriartea
deltoidea and Mauritia flexuosa where a single regression (y = 2.53x + 5.95) fits the data
for both species................................................................................................................129
Figure 4.15: The relationship between palm height (m) and (A) leaf epidermal cell sizes
(m2) in Iriartea deltoidea (y = 77 +21x-1.3x2) and Mauritia flexuosa (y = -7.2x+350),
(B) stomatal density (mm-2) in Iriartea deltoidea (y = 52x0.47) and Mauritia flexuosa (y
= 37e-0.076x) and (C) guard cell length (m) in Iriartea deltoidea (y = 29.4e-0.028x) and
Mauritia flexuosa (y = 14.7 +0.001x +0.007x2). Guard cell lengths and stomatal
densities were used to calculate stomatal pore area indices (SPI) which are plotted vs.
palm height (inset) for Iriartea deltoidea and Mauritia flexuosa (y = 0.081e-0.066x).. ..130
Figure 4.16: The relationship between palm height (m) and (A) Iriartea deltoidea sapflux
(kg/day) measured in the boles during the wet season and the subsequent dry season.
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Sapflux increased linearly in taller palms (y = 0.27x +0.41); however, there is no
relationship when sapflux is presented on a per leaf area basis (inset). (B) Mauritia
flexuosa sapflux (kg/day) measured in the boles and in the petioles. Sapflux increased
linearly in taller palms (y = 3.95x + 1.82); however, there is no relationship when sapflux
is presented on a per leaf area basis (inset)......................................................................132
Figure 4.17: Bole water storage estimation for Mauritia flexuosa where left panels
represent no lag between bole and petiole sapflux (g m-2 s-1) and right panels
represent a lag that maximizes the r2 of the regression. Top panels, (A) and (B) represent
data from a 6 m tall palm, middle panels (C) and (D) represent data from an 18 m tall
palm and bottom panels (E) and (F) represent data from a 22.5 m tall palm. All data were
collected on the same day; Feb. 28, 2008........................................................................133
Figure 4.18: Percent parenchyma on an area basis vs. height of sample (m) in the outer
bole (lower left picture, x-section, 40X, stained with Toluidine Blue O) and the inner bole
(upper right picture, x-section, 40X, stained with Toluidine Blue O) in Iriartea deltoidea
palms. The inset graph presents bole cross-sectional area measured at breast height (m2)
vs. palm height (y = 0.0018x + 0.0008) in Iriartea deltoidea (Bars =1 mm)...................134
Figure 4.19: Vascular conduit sizes and distributions in the outer bole, inner bole and
stilt roots from Iriartea deltoidea palms of various heights. (A) Metaxylem vessel
diameters (m) vs. sample height above ground (m) for outer and inner bole (y = 71x
0.43) and pooled stilt roots, (B) vascular bundle density (mm-2) vs. palm height (m) for
outer bole (y = 17 x -0.97), the inner bole (y = 27 x -1.6) and pooled stilt roots and (C)
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calculated Hagen-Poiseuille conductivity (kg m-1 s-1 MPa-1) vs. palm height for
outer bole (y = 6.4x 1.2), inner bole (y = 1.3 x 1.6), and pooled stilt roots....................135
Figure 4.20: Vascular bundle density (mm-2) vs. metaxylem vessel diameter (m) for
samples from Iriartea deltoidea palms collected from the outer bole and inner bole at
various heights, and from stilt roots of palms of varying height. The following equation
was fitted to the data: y = 68.5 e -0.023x........................................................................136
Figure 5.21: Vulnerability curves for petioles taken from palm of differing heights of a)
Iriartea deltoidea and b) Washingtonia robusta. closed circles = 1m, open circles = 3m,
closed triangle (pointing down) = 5m, open triangle (pointing down) = 7m, closed square
= 9m, open square = 11m, closed diamond = 13m, open diamond = 15m for Iriartea
deltoidea, 14m for Washingtonia robusta, closed triangle (pointing up) = 16m
Washingtonia robusta. In a) solid line is fitted to all points, b) solid line is fitted to the
average of 1m, 3m, and 5m; dashed line is fitted to the average of 7m, 9m, and 11m; and
a dotted line is fitted to the average of 13m, 14m and 16m.............................................177
Figure 5.22: Palm height (m) vs. a) individual frond leaf area (m2) and b) individual
frond Huber values for Iriartea deltoidea closed circles, Washingtonia robusta growing
in Australia and Los Angeles open and closed squares respectively, and Mauritia
flexuosa open triangles. ..............................................................................................178
Figure 5.23: Palm height (m) vs. a) petiole specific conductivity (KS) (kg m-1 s-1 MPa-
1) and b) leaf specific conductivity (KL) (kg m-1 s-1 MPa-1) from petioles from Iriartea
deltoidea closed circles, Washingtonia robusta - open squares and Mauritia flexuosa
open triangles. .................................................................................................................179
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Figure 5.24: Palm height (m) vs. a) maximum vessel length (cm) in petioles from Iriartea
deltoidea closed circles and Washingtonia robusta open squares, b) average vessel
diameter (m) and c) vascular bundle density (# mm-2) in petioles from Iriartea deltoidea
closed circles, Washingtonia robusta open squares and Mauritia flexuosa- open
triangles............................................................................................................................180
Figure 5.25: Palm height (m) vs. a) the water potential at which 50% petiole conductivity
was lost (P50) (-MPa) obtained from vulnerability curves (Fig. 5.1) and b) midday leaf
water potentials (-MPa) measured on a cloudless day in Iriartea deltoidea closed circles
and Washingtonia robusta open squares.......................................................................181
Figure 5.26: Cross section (20X) of a petiole from a 1m tall Washingtonia robusta palm
where the double dye staining procedure was performed. The red dye (Basic Fuchsin)
was introduced in the afternoon and the blue dye (Toluidine Blue) was introduced the
following morning. Vessels that were stained red were functional in the afternoon, while
vessels that were stained blue were embolized in the afternoon but refilled overnight.
Vessels that are purple presumably received both dyes and did not embolize in the
afternoon..........................................................................................................................182
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1
CHAPTER 1
INTRODUCTION
1.1 OVERVIEWOFTHE HYDRAULIC LIMITATION HYPOTHESIS
Foresters have known for a long time that as trees mature their growth reaches a
peak, at which point further increases in height and diameter begin to decrease (Smith et
al., 1997; Bond-Lamberty et al., 2004; Litvak et al., 2003). It has also been noted that in
very old trees of species such as Douglas-fir and coastal redwoods, height growth is
significantly reduced when compared to shorter trees of the same species (McDowell et
al., 2002a, Koch et al., 2004). There are several possible reasons why forest growth and
tree height in particular would begin to decline as trees get older and taller. One
possibility is that larger trees have larger respiratory demands leaving less carbon
available for growth (Ryan and Yoder, 1997). However, Ryan and Waring (1992) found
that maintenance respiration of woody tissues was only slightly and insignificantly higher
in a 245 yr old lodgepole pine (Pinus contorta) stand compared to a 40 yr old stand.
Another possibility is that as trees get taller, they also become older and that growth is
reduced in older tissues relative to younger ones. However, a study done by Mencuccini
et al. (2005) found that when shoots from the tops of old ash (Fraxinus excelsior),
sycamore (Acer pseudoplatanus), poplar (Populus sp.), and Scots pine (Pinus sylvestris)
trees were grafted onto young rootstock, their relative growth rates and net
photosynthetic rates recovered to values similar to that of younger, smaller trees. It is
also possible that limitations in phloem loading at the tops of tall trees and phloem
transport across long distances may limit height growth in trees (Koch and Fredeen,
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2005; Zimmermann, 1973). Another possibility is that as trees grow taller, the
mechanical stresses on the stem increase, making trees more susceptible to uprooting and
wind damage. Meng et al. (2006) found some evidence for this by tethering tall
lodgepole pines to reduce their bending moment. They found that six years of tethering
resulted in a 40% increase in height growth relative to the previous period when the trees
were not tethered.
With experimental evidence disproving many of these previous hypotheses, the
hydraulic limitation hypothesis remains as a viable explanation for height growth rates
declines in very tall trees (Ryan and Yoder, 1997, Koch et al., 2004). Hydraulic
limitations could begin to impact taller trees because, as trees grow in height, the
gravitational potential increases as well as the path length of water travel. This means
that taller trees are, by virtue, less efficient at transporting water to their leaves relative to
shorter trees. In order to overcome this inefficiency, taller trees require a more negative
leaf water potential to move the same quantity of water as shorter trees. Since trees of a
given species also tend to exhibit representative minimum leaf water potentials in order
to protect their water conducting conduits, the tallest trees of a given species will reach
their minimum leaf water potential sooner than shorter trees, causing stomatal closure,
and reduced photosynthesis and carbon gain (Ryan and Yoder, 1997). This phenomenon
is thought to then act as a negative feedback on further height growth in very tall trees
and would tend to set characteristic maximum heights for given tree species growing in
given environmental conditions.
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Since its proposal, several studies have found evidence in support of the hydraulic
limitation hypothesis. For example, in a study of European beech (Fagus sylvatica),
Schfer et al. (2000) found that at similar environmental conditions, stomatal
conductance, and in turn, the amount of carbon dioxide available in the leaf for
photosynthesis was decreased by 60% for a given 30m increase in tree height. Ryan et al.
(2000) found that water flux and whole tree stomatal conductance was half as much in
36m tall ponderosa pines (Pinus ponderosa) as in 12m tall trees. Additionally, Hubbard
et al. (1999) found that old ponderosa pines had 53% lower whole tree sapflow per unit
leaf area than younger trees. In maritime pines (Pinus pinaster), Phillips et al. (2003a)
found that not only did taller Oregon white oaks (Quercus garryana) have decreased
sapflux compared to shorter trees, but they also had more leaf area for a given sapwood
area, compounding the effects of hydraulic limitation to carbon gain. Another
consequence of the hydraulic limitation hypothesis may also include decreased turgor
pressure at the tops of tall trees which could limit cell expansion unless osmotic
adjustment occurs (Koch et al., 2004; Woodruff et al., 2004; Meinzer et al., 2008).
Decreased turgor represents another way in which height growth could be limited in tall
trees because, although not affecting stomatal conductance, decreases in total leaf area
will reduce carbon gain by decreasing the area of leaf tissue available for photosynthesis.
If osmotic adjustment does occur to maintain turgor, this represents an additional carbon
requirement in tall trees relative to shorter ones.
Although hydraulic limitation seems reasonable given the physical laws of water
transport in tall trees, there are also data which seem to contradict or a least complicate
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this issue. For example, in their study of old-growth Douglas-fir trees, McDowell et al.
(2002a) found that stomatal conductance, photosynthetic assimilation and leaf-specific
hydraulic conductance were not significantly different among trees of different heights
and Barnard and Ryan (2003) also found that taller Eucalyptus trees had similar
photosynthetic assimilation, sapflux per unit leaf area and whole tree stomatal
conductance than their shorter counterparts. Additionally, West et al. (1999) propose that
if conduits taper sufficiently, hydraulic resistance can become independent of path length,
because hydraulic resistance is inversely proportional to the fourth power of conduit
radius, but only linearly related to length (Becker et al., 2000, Zimmermann, 1983).
Tall trees can also make alterations to their anatomy and physiology in order to
alleviate some of the affects of hydraulic limitations on photosynthesis and carbon gain.
One way in which taller trees can move as much water as their shorter counterparts is by
increasing the tension the water is under and exhibiting more negative leaf water
potentials. In fact, both Barnard and Ryan (2003) and McDowell et al. (2002a) saw this
adjustment in leaf water potential made in the trees they studied. According to the
hydraulic limitation hypothesis, taller trees should not exhibit more negative water
potentials (Ryan and Yoder, 1997) because more negative water potentials increase the
risk of disfunction of the water conducting vessels or tracheids in terms of embolism
formation(Zimmermann, 1983). Embolisms occur when air is pulled into a water
conducting conduit that is under a large negative pressure (the air-seeding hypothesis) or
when the water column itself freezes in the vascular tissues of plants (freeze-thaw
embolism) (Zimmermann, 1983; Tyree and Sperry, 1989). These embolism events
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reduce conductivity (Zimmermann, 1983) and cause reductions in transpiration and
photosynthesis (Sperry et al., 1993; Hubbard et al., 2001). However, taller trees could
sustain more negative water potentials if they construct conduits that are more resistant to
embolism formation. This phenomenon was seen in old growth Douglas-fir trees by
Woodruff et al. (2007) and Domec et al. (2008).
There is some contradictory information about whether the conductivity in taller
trees will increase to offset the path length and gravitational effect, or decrease as a result
of increased resistance to embolisms. Increases of sapwood conductivity with height
have been seen in several studies of conifer trees (Pothier et al., 1989; Domec and
Gartner, 2003; Burgess et al., 2006). However, it is generally assumed that there is a
tradeoff between conductivity and embolism resistance. This trade-off is described for
vessels by Hacke et al. (2006) in that vessels with smaller pit pore areas are more
embolism resistant but limited in length and diameter, leading to lower conductances.
One way that tall trees could sustain more negative water potentials than shorter trees, but
avoid any tradeoffs between embolism resistance and conductivity may be efficient
refilling of conduits that embolize. Recent study has shown that trees may be able to
reverse embolisms that have formed in their conduits, in many cases while the leaves are
still transpiring and the water column is still under tension (Zwieniecki and Holbrook,
(1998; Bucci et al., 2003; Stiller et al., 2005).
Tall trees can also make biometric adjustments in leaf area to bole area ratios in
order decrease the water demanding to water supply area and increase their capacity for
bole water storage. Leaf area to sapwood area ratios have generally been found to
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decrease as trees grow taller (Schfer et al., 2000; Phillips et al., 2001; Sterck and
Bongers, 2001; McDowell et al., 2002b; Barnard and Ryan, 2003). However, the
DESPOT model which optimizes carbon gain in trees predicts that leaf area to sapwood
area ratios should increase with tree height (Buckley and Roberts, 2006). Even though
lowering leaf area for a given sapwood area can alleviate restrictions on stomatal
conductance in tall trees, this can still be considered a hydraulic limitation because
taller trees would need to put more of a carbon investment into water conducting tissues
over leaf tissue serving to further limit their carbon gain ability (Phillips et al. 2003a).
Taller trees have also been shown to have a greater reliance on stored water in their boles
than shorter trees (Goldstein et al., 1998; Phillips et al., 2003b). However, Meinzer et al.
(2004) found that although larger tropical trees had greater use of stored water, they also
had greater daily water use than smaller trees. Therefore, the contribution of stored water
to daily water use was equivalent across tree size.
It is obvious that trees are very complex organisms and the study of physiological
phenomena can be difficult. With regard to validating the hydraulic limitation
hypothesis, the complicated branching patterns of many species mean that each leaf on
the tree will have a different path length from the ground. Additionally, the hydraulic
architecture of many trees is designed in such a way that branches receiving more
sunlight are hydraulically favored over lower branches (Protz et al., 2000). Much of this
complexity could be avoided by focusing on tree species that have a much simpler form.
Palms have all the criteria to make them a model organism because, compared to other
tree species, they are structurally, very simple with a relatively fixed crown size and
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vascular system (Zimmermann et al., 1982; Tomlinson, 1987). In particular, palms are a
good tree form to use because unlike most trees, palms lack complex branching patterns
making the path length of water flow easily measurable. In addition, their small, compact
crowns allow for a very accurate estimate of leaf area.
1.2 DISTINCTIVE PHYSIOLOGICAL FEATURESOF PALMS
Palms are very distinctive members of the plant world in many ways. They are
one of the few members of the monocot class that are able to reach significant heights
with the tallest palm species (Ceroxylon quinduiense) reaching 60m in height (Henderson
et al., 1995). In doing so, they are able to transport water very long distances, matching
many dicotyledonous species. However as monocots, palms lack a vascular cambium
and therefore do not have any secondary woody growth for vascular transport. All
vascular transport and mechanical support is accomplished through thousands of vascular
bundles which are comprised of primary xylem vessels, phloem sieve tube cells and
fibers. This makes the boles of palms very heterogenous in nature where they have been
shown to encompass an entire range of published wood density values within a single
stem (Rich, 1987b). Although the crowns of palms are very simple compared with many
other tree species, they are unique in many ways. One important difference between
palms and dicotyledonous trees is that vertical growth in palms is directly tied to leaf
production by the apical meristem (Rich, 1986). Palm leaves are extraordinary within the
plant world holding records for both the longest pinnate self-supporting leaf inRaphia
regalis Becc.at 25m as well as the largest palmately compound self-supporting leaf in
Corypha umbraculifera L. at 8m in leaf diameter (Tomlinson, 2006). Also, because tall
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height have a lower margin of safety against mechanical failure than shorter palms.
Younger palms are also overbuilt for mechanical safety with respect to diameter while
older palms are underbuilt with respect to diameter when compared to both younger
palms and with angiosperm and conifer species (Rich, 1987a). However, instead of
exhibiting large increases in diameter, palms increase the stiffness and strength of their
stem tissues in order to make themselves more mechanically stable (Rich, 1987a). The
upper region of palm stems also becomes increasingly flexible (Rich, 1987a) and the
crown becomes narrower (Rich et al., 1986) in order to make tall palms less susceptible
to wind damage. However, Gale and Barfod (1999) found that manyIriartea deltoidea
palms (47%) died standing, while 45% died from being snapped and 8% were uprooted
(although all of the palms that were snapped or uprooted were pushed over by other
trees). Palms also appear to exhibit decreases in height growth as they get older/taller.
Homeier et al. (2002) found thatIriartea deltoidea reaches its maximum height growth
rates at about 10-12m when the palm reaches reproductive age, at which point vertical
growth rates decrease. Lugo and Rivera Batlle (1987) also found that dominantPrestoea
montana palms grew fast in height when they are small, but height growth slowed once
they reached the canopy.
Palms also provide a unique opportunity to study vulnerability to embolism and
embolism repair because they lack the capacity to make new conducting tissues.
Therefore, their vascular conduits either need to efficiently avoid embolisms or
efficiently reverse embolisms that were to occur in their vascular tissues if they are to
remain functional over a lifetime. Few studies have looked at the rate of embolism
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formation and reversal in palm species. A study done by Drake and Franks (2003) found
that vascular conductivity was significantly decreased in the dry season compared to the
wet season in two species ofCalamus, a rattan in the Palmae. A study done by Sperry
(1986) onRhapis excelsa, found that large tensions were required to induce xylem
embolisms and when embolisms did occur, they were confined to conduits in the petiole
with conduits in the bole remaining intact. Bole conduits were protected by the hydraulic
architecture of the palm, with most of the resistance to water flow located at the stem to
leaf connection and in the leaf itself (Sperry, 1985). If embolisms do occur in palms,
then some mechanism of refilling would be necessary, given that palms cannot replace
embolized vessels. It also seems plausible that the phloem tissue could be involved in
vessel refilling because of its proximity to the xylem vessels in the vascular bundle.
Phloem carries sugars from their origins to locations throughout the plant. When sugars
transported through the phloem exit, the osmotic potential of the phloem drops and the
surplus water that originally transported the sugars also exits and is recycled by the xylem
(Milburn, 1996; Patrick et al., 2001). This surplus phloem water makes up 1 to 3% of
xylem transport and could make up much of the water used to refill embolized vessels
(Milburn, 1996). Measurements of xylem tensions and changes in phloem turgor suggest
that there is a close association of radial water movement from the phloem to the xylem
(Sovonick-Dunford et al., 1981). Several studies have found that inactivating the phloem
by girdling significantly impairs embolism repair (Salleo et al., 1996; Zwieniecki et al.,
2000; Salleo et al., 2004).
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1.3 DISSERTATION STRUCTURE
Chapter 2 describes a test of the hydraulic limitation hypothesis in Washingtonia
robusta palms growing in Southern California. Relationships of sapflux per unit leaf
area, stomatal conductance, maximum photosynthetic rates, leaf water potentials,
stomatal densities, guard cell lengths, leaf dry mass per unit area were evaluated with
palm height to determine whether photosynthesis in taller palms was more hydraulically
limited. As well bole water storage and leaf epidermal cell sizes, and total leaf areas
were compared in palms of differing heights to determine whether any physiological
compensations were occurring to overcome hydraulic limitations.
Chapter 3 describes a study comparing wet season and dry season transpiration in
a tropical rainforest palm,Iriartea deltoidea. Atmospheric data, soil moisture data and
sapfluxes were compared in order to determine if transpiration was more stomatally
limited in the dry season compared to the wet season and if so, was that driven more by
atmospheric vapor pressure deficits or soil moisture availability. Additionally, based on
published tree abundances in this area, measured sap fluxes inIriartea deltoidea were
scaled up to the hectare level.
Chapter 4 tests the hydraulic limitation hypothesis in two species of tropical
rainforest palms,Iriartea deltoidea andMauritia flexuosa. Height growth rates,
sapfluxes per unit leaf area and total leaf areas were compared within species across
palms of differing heights to determine if hydraulic limitations were occurring.
Additionally, physiological comparisons were made betweenIriartea deltoidea and
Mauritia flexuosa because all though they experience similar atmospheric conditions,
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they differ markedly in edaphic conditions (terra firme vs swamp), leaf type (pinnate vs.
palmate) and ontogenetic bole development. This comparison led to speculation as to
whether sustained stem lengthening can occur inIriartea deltoidea.
Chapter 5 focuses specifically on comparing the hydraulic characteristics of
petioles from these three palm species (Washingtonia robusta,Iriartea deltoidea and
Mauritia flexuosa) across an ontogenetic gradient as well as across an atmospheric
moisture gradient. Comparison of leaf area to conducting area ratios, petiole
conductivity, anatomic properties, and vulnerability to embolism shed light on any
hydraulic compensations to increased height that were occurring at the petiole level. As
well, comparison of P50 values (point at which 50% of hydraulic conductivity is lost) with
measurements of midday leaf water potentials, as well as a double-dye staining
experiment, allowed for estimation of the magnitude of daily embolism formation in
these palm petioles. This led to speculation about whether palms avoid embolisms
through tight stomatal control, or refill embolisms that occur on a daily basis.
1.4 LITERATURE CITED
Barnard, H.R., and M.G. Ryan. 2003. A test of the hydraulic limitation hypothesis in
fast-growingEucalyptus saligna. Plant, Cell and Environment 26: 1235-1245.
Becker, P., Gribben, R.J., and C.M. Lim. 2000. Tapered conduits can buffer hydraulic
conductance from path-length effects. Tree Physiology 20: 965-967.
Bond-Lamberty, B., Wang, C., and S.T. Gower. 2004. Net primary production and net
ecosystem production of a boreal black spruce wildfire chronosequence. Global
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Bucci, S.J., Scholz, F.G., Goldstein, G., Meinzer, F.C. and L. da S.L. Sternberg. 2003.
Dynamic changes in hydraulic conductivity in petioles of two savanna tree
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vessels. Plant, Cell and Environment 26: 1633-1645.
Buckley, T.N. and D.W. Roberts. 2006. How should leaf area, sapwood area and
stomatal conductance vary with tree height to maximize growth? Tree
Physiology 26: 145-157.
Burgess, S.S.O., Pittermann, J. and T.E. Dawson. 2006. Hydraulic efficiency and safety
of branch xylem increases with height in Sequoia sempervirens (D.Don) crowns.
Plant, Cell and Environment 29: 229-239.
Domec, J.C., and B.L. Gartner. 2003. Relationship between growth rates and xylem
hydraulic characteristics in young, mature and old-growth ponderosa pine trees.
Plant, Cell and Environment 26: 471-483.
Domec, J.C., Lachenbruch, B., Meinzer, F.C., Woodruff, D.R., Warren, J.M. and K.A.
McCulloh. 2008. Maximum height in a conifer is associated with conflicting
requirements for xylem design. PNAS 105: 12069-12074.
Drake P.L. and P.J. Franks. 2003. Water resource partitioning, stem xylem hydraulic
properties, and plant water use strategies in a seasonally dry riparian tropical
rainforest. Oecologia 137: 321-329.
Dransfield, J. 1978. Growth form of rain forest palms. In Tropical Trees as Living
Systems, ed P.B. Tomlinson, M.H. Zimmermann, pp. 247-268. NY: Cambridge
University Press.
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Gale, N., and A.S. Barfod. 1999. Canopy tree mode of death in a western Ecuadorian
rain forest. Journal of Tropical Ecology 15: 415-436.
Goldstein, G., Andrade, J.L., Meinzer, F.C., Holbrook, N.M., Cavelier, J., Jackson, P.,
and A. Celis. 1998. Stem water storage and diurnal patterns of water use in
tropical forest canopy trees. Plant, Cell and Environment 21: 397-406.
Hacke, U.G., Sperry, J.S., Wheeler, J.K. and L. Castro. 2006. Scaling of angiosperm
xylem structure with safety and efficiency. Tree Physiology 26: 689-701.
Henderson, A., Galeano, G., and R. Bernal. 1995. Field Guide to the Palms of the
Americas. Princeton University Press. Princeton, New Jersey
Homeier, J., Breckle, S.W., Dalitz, H., Leyers, C., and R. Ortiz. 2002. Demography,
spatial distribution, and growth of three arborescent palm species in a tropical
premontane rain forest in Costa Rica. Ecotropica 8: 239-247.
Hubbard, R.M., Bond, B.J., and M.G. Ryan. 1999. Evidence that hydraulic conductance
limits photosynthesis in oldPinus ponderosa trees. Tree Physiology 19: 165-
172.
Hubbard, R.M., Ryan, M.G., Stiller, V. and J.S. Sperry. 2001. Stomatal conductance and
photosynthesis vary linearly with plant hydraulic conductance in ponderosa pine.
Plant, Cell and Environment 24: 113-121.
Koch, G.W., Sillett, S.C., Jennings, G.M., and S.D. Davis. 2004. The limits to tree
height. Nature 428(22): 851-854.
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Mencuccini, M., Martinez-Vilalta, J., Vanderklein, D., Hamid, H.A., Korakaki, E., Lee,
S., and B. Michiels. 2005. Size-mediated ageing reduces vigour in trees.
Ecology Letters 8: 1183-1190.
Meng, S.X., Lieffers, V.J., Reid, D.E.B., Rudnicki, M., Sillins, U., and M. Jin. 2006.
Reducing stem bending increases the height growth of tall pines. Journal of
Experimental Botany 57(12): 3175-3182.
Milburn, J.A. 1996. Sap ascent in vascular plants: challengers to the cohesion theory
ignore the significance of immature xylem and the recycling of Mnch water.
Annals of Botany 78: 399-407.
Patrick, J.W., Zhang, W., Tyerman, S.D., Offler, C.E. and N.A. Walker. 2001. Role of
membrane transport in phloem translocation of assimilates and water. Australian
Journal of Plant Physiology 28: 695-707.
Phillips, N., Bond, B.J., McDowell, N.G., Ryan, M.G., and A. Schauer. 2003a. Leaf area
compounds height-related hydraulic costs of water transport in Oregon white oak
trees. Functional Ecology 17: 832-840.
Phillips, N., Bond, B.J., and M.G. Ryan. 2001. Gas exchange and hydraulic properties in
the crowns of two tree species in a Panamanian moist forest. Trees 15: 123-130.
Phillips, N.G., Ryan, M.G., Bond, B.J., McDowell, N.G., Hinckley, T.M., and J. Cermak.
2003b. Reliance on stored water increases with tree size in three species in the
Pacific Northwest. Tree Physiology 23: 237-245.
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Pothier, D., Margolis, H.A. and R.H. Waring. 1989. Patterns of change of saturated
sapwood permeability and sapwood conductance with stand development.
Canadian Journal of Forest Research 19: 432-439.
Protz, C.G., Sillins, U., and V.J. Lieffers. 2000. Reduction in branch sapwood hydraulic
permeability as a factor limiting survival of lower branches of lodgepole pine.
Canadian Journal of Forest Research 30: 1088-1095.
Rich, P.M. 1987a. Mechanical structue of the stem of arborescent palms. Botanical
Gazette 148(1): 42-50.
Rich, P.M. 1987b. Developmental anatomy of the stem ofWelfia georgii,Iriartea
gigantea, and other arborescent palms: implications for mechanical support.
American Journal of Botany 74(6): 792-802.
Rich, P.M., Helenurm, K., Kearns, D., Morse, S.R., Palmer, M.W., and L. Short. 1986.
Height and stem diameter relationships for dicotyledonous trees and arborescent
palms of Costa Rican tropical wet forest. Bulletin of the Torrey Botanical Club
113(3): 241-246.
Ryan, M.G., Binkley, D., Fownes, J.H., Giardina, C.P. and R.S. Senock. 2004. An
experimental test of the causes of forest growth decline with stand age.
Ecological Monographs 74: 393-414.
Ryan, M.G., Bond, B.J., Law, B.E., Hubbard, R.M., Woodruff, D., Cienciala, E., and J.
Kucera. 2000. Transpiration and whole-tree conductance in ponderosa pine trees
of differing heights. Oecologia 124: 553-560.
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Ryan, M.G., and R.H. Waring. 1992. Maintenance respiration and stand development in
a subalpine lodgepole pine forest. Ecology 73(6): 2100-2108.
Ryan, M.G., and B.J. Yoder. 1997. Hydraulic limits to tree height and tree growth.
Bioscience 47(4): 235-242.
Salleo, S., Lo Gullo, M.A., De Paoli, D., and M. Zippo. 1996. Xylem recovery from
cavitation-induced embolism in young plants ofLaurus nobilis: a possible
mechanism. New Phytologist 132: 47-56.
Salleo, S., Lo Gullo, M.A., Trifilo, P., and A. Nardini. 2004. New evidence for a role of
vessel-associated cells and phloem in the rapid xylem refilling of cavitated stems
ofLaurus nobilis L. Plant, Cell and Environment 27: 1065-1076.
Schfer, K.V., Oren, R., and J.D. Tenhunen. 2000. The effect of tree height on crown
level stomatal conductance. Plant, Cell and Environment 23: 365-375.
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growth and stand yield by thinning. Pp. 69-98, In: The Practice of Silviculture
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measurements of phloem turgor pressure in white ash. Plant Physiology 68: 121-
126.
Sperry, J.S. 1985. Xylem embolism in the palmRhapis excelsa. IAWA Bulletin n.s. 6:
283-292.
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Sperry, J.S. 1986. Relationship of xylem embolism to xylem pressure potential, stomatal
closure, and shoot morphology in the palmRhapis excelsa. Plant Physiology 80:
110-116.
Sperry, J.S., Alder, N.N. and S.E. Eastlack. 1993. The effect of reduced hydraulic
conductance on stomatal conductance and xylem cavitation. Journal of
Experimental Botany 44(263): 1075-1082.
Sterck, F.J. and F. Bongers. 2001. Crown development in tropical rain forest trees:
patterns with tree height and light availability. Journal of Ecology 89: 1-13.
Stiller,V., Sperry, J.S., and R. Lafitte. 2005. Embolized conduits of rice (Oryza sativa,
Poaceae) refill despite negative xylem pressure. American Journal of Botany
92(12): 1970-1974.
Tomlinson, P.B. 1979. Systematics and ecology of the palmae. Ann. Rev. Ecol. Syst.
10: 85-107.
Tomlinson, P.B. 1987. Architecture of tropical plants. Annual Review of Ecology and
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Tomlinson, P.B. 2006. The uniqueness of palms. Botanical Journal of the Linnean
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Tyree, M.T., and J.S. Sperry. 1989. Vulnerability of xylem to cavitation and embolism.
Annual Review of Plant Physiology and Molecular Biology 40: 19-38.
Waterhouse, J.T, Quinn, F.L.S., and C.J. Quinn. 1978. Growth patterns in the stem of
the palmArchontophoenix cunninghamiana. Botanical Journal of the Linnean
Society 77: 73-93.
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West, G.B., Brown, J.H. and B.J. Enquist. 1999. A general model for the structure and
allometry of plant vascular systems. Nature 400: 664-667.
Woodruff, D.R., Bond, B.J., and F.C. Meinzer. 2004. Does turgor limit growth in tall
trees? Plant, Cell and Environment 27: 229-236.
Woodruff, D.R., McCulloh, K.A., Warren, J.M., Meinzer, F.C., and B. Lachenbruch.
2007. Impacts of tree height on leaf hydraulic architecture and stomatal control in
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biology IV. Transport problems in arborescent monocotyledons. The Quarterly
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Zimmermann, M.H. 1983. Xylem structure and the ascent of sap. Springer-Verlag. New
York.
Zimmermann, M.H., McCue, K.F. and J.S. Sperry. 1982. Anatomy of the palmRhapis
excelsa, VIII. Vessel network and vessel-length distribution in the stem. Journal
of the Arnold Arboretum 63: 83-95.
Zwieniecki, M.A., and N.M. Holbrook. 1998. Diurnal variation in xylem hydraulic
conductivity in white ash (Fraxinus americana L.), red maple (Acer rubrum L.)
and red spruce (Picea rubens Sarg.). Plant, Cell and Environment 21: 1173-
1180.
Zwieniecki, M.A., Hutyra, L., Thompson, M.V., and N.M. Holbrook. 2000. Dynamic
changes in petiole specific conductivity in red maple (Acer rubrum L.), tulip tree
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(Liriodendron tulipifera L.) and northern fox grape (Vitis labrusca L.). Plant,
Cell and Environment 23: 407-414.
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CHAPTER 2
COMPARATIVE HYDRAULIC AND ANATOMIC PROPERTIES IN PALMTREES (WASHINGTONIA ROBUSTA) OF VARYING HEIGHTS:
IMPLICATIONS FOR HYDRAULIC LIMITATION TO INCREASED
HEIGHT GROWTH
2.1 INTRODUCTION
It has been frequently observed that as trees mature, height growth reaches a peak,
at which point rates begin to decrease (Barnes et al. 1998; McDowell et al. 2002a; Litvak
et al. 2003; Bond-Lamberty et al. 2004; Koch et al. 2004). There have been several
proposed hypotheses regarding forest growth decline and, in particular, why tree height
growth may begin to decline as trees get older and taller, including increased respiration
(Ryan and Waring, 1992), differences in the vigor of older tissues relative to younger
ones (Mencuccini et al. 2005; Bond et al. 2007; Vanderklein et al. 2007) and increased
mechanical stresses (Meng et al. 2006). However, there are several promising studies that
suggest that hydraulic limitation may not only explain why height growth in tall trees is
limited (Ryan and Yoder 1997) but could be used to predict maximum heights of a given
tree species growing under given environmental conditions (Koch et al. 2004; Burgess
and Dawson 2007). The hydraulic limitation hypothesis is built upon the idea that as trees
get taller, not only does the hydrostatic gradient due to gravity increase, but the path
length of water travel increases, with taller trees overcoming more friction in water
transport than shorter trees. This means that taller trees are, by virtue of their height, less
efficient at transporting water to their leaves relative to shorter trees. This lower
efficiency could lead to lower stomatal conductance and, therefore, reduced
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photosynthesis and carbon gain (Ryan and Yoder 1997). Additionally, the turgor
pressure at the tops of these trees will decrease, unless osmotic adjustment occurs,
making cell expansion more difficult in developing leaves (Koch et al. 2004; Woodruff et
al. 2004). Decreased turgor at the tops of the largest palms could therefore lead to
decreases in leaf cell sizes and increases in leaf mass per unit area (LMA).
Studies in species ranging from ponderosa pine (Pinus ponderosaDougl.ex C.
Lawson) (Hubbard et al. 1999; Ryan et al. 2000), European beech (Fagus sylvatica L.)
(Schfer et al. 2000), eucalyptus (Eucalyptus saligna Sm.) (Barnard and Ryan 2003),
Oregon white oak (Quercus garryana Dougl.) (Phillips et al. 2003a) and the tallest trees
in the world, coastal redwoods (Sequoia sempervirens(D. Don) Endl.) (Koch et al. 2004)
have found evidence that the hydraulic cost of increased frictional resistance reduced
stomatal conductance in tall trees relative to shorter ones (reviewed in Ryan et al. 2006).
However, there are other studies that suggest that the hydraulic costs that taller trees face
can be offset by alterations in their architecture (Becker et al. 2000a). Also, theoretical
models (West et al. 1999; Becker et al. 2000b) as well as empirical measurements show
that hydraulic resistance due to path length can be significantly reduced (Weitz et al.
2006, Coomes et al. 2007), but in very tall trees not completely overcome (Anfodillo et
al. 2006; Petit et al. 2008), by the tapering of vascular conduits along the length of trees.
However, these compensatory features of taller trees are, in fact, consistent with the
presence of hydraulic constraints to water transport in taller trees.
About 60 to 70% of studies that have measured one or more of the components of
the hydraulic limitation hypothesis have found results that were consistent (Ryan et al.
http://en.wikipedia.org/wiki/David_Donhttp://en.wikipedia.org/wiki/Stephan_Ladislaus_Endlicherhttp://en.wikipedia.org/wiki/David_Donhttp://en.wikipedia.org/wiki/Stephan_Ladislaus_Endlicher -
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2006), although several studies have provided some contradictory data (McDowell et al.
2002a; Barnard and Ryan 2003). One reason for the conflicting information could be the
complexity of most tree systems. Their complicated branching patterns mean that each
leaf on the tree will have a different path length from the ground. Also, the hydraulic
architecture has been shown to be designed in such a way that branches receiving more
sunlight are hydraulically favored over lower branches (Protz et al. 2000). Much of this
complexity could be avoided if a simpler tree species such as palms were used to study
hydraulic limitation. Palms represent a desirable tree form to use because, unlike most
trees, they lack complex branching patterns and exhibit relatively fixed crown sizes
(Zimmermann et al. 1982; Tomlinson 1990) making the path length of water flow as well
as leaf area easily measurable. Additionally, hydraulic limitations in palms become
especially important considering they lack secondary growth and may exhibit decreased
functioning of xylem and phloem tissues with age (Zimmermann, 1973). This is
especially relevant for a palm species such as Washingtonia robusta where older, taller
palms are likely to have experienced more frost episodes over their lifetime than younger,
shorter palms and may not be able to refill embolized conduits (Sperry, 1986). If vessels
are able to refill, multiple freeze-thaw episodes have been shown to negatively affect the
functioning of xylem tissues through cavitation fatigue, which may or may not be
reversible (Hacke et al. 2001; Stiller and Sperry, 2002).
We studied hydraulic limitation in Mexican fan palms, Washingtonia robusta (H.
Wendl.), a species that is naturally distributed throughout southern and central Baja
California and western Sonora, Mexico along streams and canyons or near springs (Uhl
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and Dransfield 1987; Bullock and Heath 2006). Bullock and Heath (2006) studied
Washingtonia robusta in the Baja California desert and estimate that they reach
reproductive maturation at approximately 8 m tall with the tallest palms in their study
being 32 m. They also estimate the potential longevity of these palms to exceed 500
years. We hypothesize that hydraulic constraints on leaf gas exchange will increase with
height in Washingtonia robusta with taller palms having lower sap flux per unit leaf area
and lower stomatal conductance than shorter palms. Additionally, we are interested in
any alterations in physiology or hydraulic architecture that tall palms exhibit in order to
compensate for an increased path length of water flow relative to shorter palms; including
changes in minimum leaf water potential, maximum photosynthetic rates, and leaf area to
conducting area ratios. Not only could this research shed light on the physiological costs
of increasing size in palms, but, because the biophysical variables we studied are also
shared by woody plants, it may shed light on the physiological costs and compensations
in tree species, in general, as they grow taller.
2.2 MATERIALS AND METHODS
2.2.1 SITE DESCRIPTION
This study was performed from July 23 to August 3, 2007 on 10 individuals of
Washingtonia robusta (H. Wendl.) growing at the Los Angeles County Arboretum &
Botanic Garden (34 8' 29.43"N, 118 3' 15.15"W) in Arcadia, California. The site
contained several open-grown palm individuals scattered throughout a lawn with palms
varying in height from 1 m tall to approximately 35 m tall. The site is adjacent to a
natural aquifer; therefore, the water table is elevated in this location. Also, the area was
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sprinkler irrigated approximately three times per week for one to two hours at each
interval, and plants, therefore, should not have experienced soil moisture stress during the
experimental period. Measurements of solar radiation were made using a pyranometer
(Apogee Instruments, Roseville, CA, USA) located on an open lawn. Diurnal measures
of temperature and relative humidity were made using a Campbell Scientific (CS215)
temperature and relative humidity sensor (Campbell Scientific Inc., Logan UT, USA)
located approximately 5 m above the ground in an exposed area. Atmospheric and
radiation data were captured at intervals of 30 sec and logged every 2 min using a CR10X
datalogger and an associated AM16/32A multiplexer (Campbell Scientific Inc., Logan,
UT, USA). For the 10 day measurement period, daily maximum temperatures ranged
from 29 to 34oC and nightly minimum temperature ranged from 17 to 20 oC. Daily
minimum humidity ranged from 21 to 50% and nightly maximum humidity ranged from
82 to 90%. Daily maximum vapor pressure deficits (VPD) ranged from 2 to 4 kPa.
Maximum daily solar radiative flux densities ranged from 850 to 1060 W m-2.
2.2.2 PALM HEIGHT ESTIMATION
Palm heights were estimated, with the aid of a tape measure, from the ground to
the point at which the lowest leaves of the crown attached to the bole. Tall palms were
accessed using a bucket lift. For shorter palms, height was estimated by making a mark
on the bole 1 m above the ground, then estimating height by eye based on this mark.
Because shorter palms tended to have more leaves, height was measured from the ground
to the midpoint of the crown of leaves. The palm reported to be 2 m tall was a juvenile
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that did not possess a trunk; therefore its height was measured from the top of its leaves
to the ground.
2.2.3 SAP FLUX MEASUREMENT
Sap flux was measured in a total of 10 palms in this study, ranging in height from
2 m to 34 m. Sap flux sensors were distributed as follows: Sap flux sensors were
installed in the boles of eight palms ranging from 7 m to 34 m tall using 2 cm long
Granier heat dissipation sensors (Granier 1987). Sap flux was also measured in the
petioles in five palms ranging from 2 m tall to 34 m tall, in each of which two sap flux
sensors were installed in two separate petioles. Table 2.1 summarizes tree data and
sampling details.
In boles, the leaf bases (if any) were removed from the base of the palm and two
sensors were installed on either side of the bole directly beneath the pseudobark, with this
position indicated by a color change that was indicative of wet, conductive bole material.
An additional sensor was also installed at a depth of 2 cm below the pseudobark, giving a
total of three sensors per palm bole. Sensors were connected to a CR10X datalogger and
an associated AM16/32A multiplexer that captured data at intervals of 30 sec and logged
every 2 min (Campbell Scientific Inc., Logan, UT, USA). The boles were wrapped with
reflective insulation to prevent external temperature fluctuations. Data from outer bole
sensors and the 2 cm depth sensor were pooled because statistical analysis indicated that
they were not significantly different (p-value = 0.25). Sap flux data (g m-2 s-1) were
scaled up to the whole tree level by multiplying by the cross-sectional area of the bole
minus the area of the pseudobark (approximated to be 1 cm thick) giving sap flux units of
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kg day-1 and then divided by total palm leaf area to give units of kg day-1 m-2 leaf area.
We are assuming that sap flux is more or less constant across the radius of the bole (and
indeed we found no significant differences between outer bole and 2 cm depth sensors).
This assumption is also validated by work done by Roupsard et al. (2006) who found a
constant pattern of sap flux throughout the stem of coconut palms (Cocos nucifera L.) up
to a 12 cm radius. Likewise, Sellami and Sifaoui (2003) found that the sap flow in date
palms (Phoenix dactylifera L.) did not differ significantly between the 3 cm and 6 cm
depth sensors.
For the petiole sap flux, 1 cm long Granier sensors were only used in the petioles
of the 2 m tall palm. All other petioles had 2 cm long Granier sensors. The shape of the
petiole cross-section is approximately a semi-circle and sensors were inserted in the flat
portion of the petiole (adaxial side). Petioles were then wrapped with reflective
insulation to minimize external temperature fluctuations. Sap flux data (g m-2 s-1) were
scaled-up by multiplying by the cross-sectional area of the petiole, giving sap flux units
of kg day-1 and then divided by individual frond leaf area to give units of kg day-1 m-2 leaf
area.
Stem water storage was also investigated in order to ascertain contributions of
stored water in the bole to overall sap flux. Palms that are more reliant on stored bole
water will tend to lag behind palms that have less stored bole water. To evaluate this,
diurnal time courses of bole sap fluxes (g m-2 s-1) in two short palms (7 m and 8 m) were
compared with diurnal time courses of bole sap fluxes (g m -2 s-1) in three tall palms (28 m
to 34 m) using cross-correlation analysis. In addition, two of the ten palms (8 m and 28
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m tall) had simultaneous bole and petiole sap flow data. In these individuals, stem water
storage was estimated by pairing diurnal time courses of sap flux made in the bole with
that of corresponding petioles using cross-correlation analysis. The time lag
corresponding to the maximum degree of correlation between the petiole sap flux and the
bole sap flux represented the approximate amount of water storage in the bole of the
palm.
2.2.4 STOMATAL CONDUCTANCE AND PHOTOSYNTHESIS
Stomatal conductance and photosynthetic assimilation were measured diurnally
on five palms ranging from 8 m to 34 m tall using a LiCor 6400 photosynthesis system
(Licor, Lincoln, NE, USA) fitted with a red-blue LED light source. Five palms were
chosen from among the 10 total palms to span a large range in height of reproductively
mature individuals, and to maintain reasonable sampling time intervals throughout the
day. Measurements were made over a four day period at intervals of approximately 1.5 h
(from approx. 7 am to 5 pm) with a light level of 1500 mol m-2 s-1 and a CO2 level of
400 mol mol-1. Two leaf segments from different fronds were measured per palm during
each time period. Measurements were taken when both stomatal conductance and
photosynthetic assimilation had stabilized. Measurements from the two leaf segments
were averaged per time period. Polynomial equations were then fit to the diurnal stomatal
conductance and photosynthetic assimilation data and were used to calculate maximum
daily stomatal conductance and maximum daily photosynthetic assimilation rate (both
calculated by setting the first derivative equal to zero) for each palm measured.
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Equations and r2 values are presented in Table 2.2. With few exceptions, the rankings of
maximum photosynthetic assimilation and maximum stomatal conductance across tree
height were the same whether values were obtained from the polynomial equations or
from the raw data.
2.2.5 WATERPOTENTIAL MEASUREMENT
Diurnal measures of leaf water potential were made on five palms ranging from 2
m to 28 m tall using a Scholander type pressure chamber (Soil Moisture Equipment
Corp., Santa Barbara, CA, USA)(Scholander et al. 1965). These individuals were selected
from among the ten total palms to cover a large range in palm height but to maintain a
manageable diurnal sampling schedule. Leaf water potentials were measured over a four
day period at intervals of approximately 1.5 h (from approximately 6 am to 5 pm). Water
potential measurements were made by removing two individual segments from the leaf.
Leaf segments were immediately placed in a plastic bag and covered in order to promote
stomatal closure and prevent further leaf dehydration. An approximately 1 cm length of
leaf tissue was removed from either side of the midrib, and the remainder of the segment
was placed in the pressure chamber with the midrib exposed to the outside environment.
Measurements from the two leaf segments were averaged to give one measurement per
palm at a given time period. Polynomial equations were then fit to the diurnal leaf water
potential data and were used to calculate minimum leaf water potential and the time of
minimum leaf water potential (both calculated by setting the first derivative equal to
zero) for each palm. Equations and r2 values are presented in Table 2.2. The rankings of
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minimum leaf water potential across tree height were the same whether values were
obtained from the polynomial equations or from the raw data.
2.2.6 LEAF CHARACTERISTICS
Leaf areas were estimated for the same two leaves used to measure petiole sap
flux in four of the ten study palms ranging from 8 m to 34 m tall. These palms
represented a range of heights and could be accessed using the bucket lift or ladder.
Leaves were harvested after sap flux measurement had been completed and an overhead
digital photo was taken of each leaf with a known scaling factor. Image analysis software
(Image J, Scion Image, Frederick, MD, USA) was then used to measure leaf area.
Measurements of the two leaves were pooled to give an average leaf area for each palm.
In order to measure leaf dry mass per unit area (LMA), three leaf segments from each
leaf were removed and their individual areas measured. These leaf segments were
allowed to air dry for one week, then their dry weight was obtained. Additionally, live
leaf counts were made on each individual.
Leaf epidermal cell sizes, stomatal density and guard cell length were measured
by making hand sections of leaf material. To begin, individual leaf segments were
gathered from palms 2 m to 34 m tall, and then thin sections were cut with a razor blade
from the adaxial side of two individual leaf segments tangential to the midrib. Sections
were then stained with a solution of 1% Toluidine Blue O and mounted on slides using
Permount. The slides were viewed at 200X magnification using a compound light
microscope (Nikon Alphaphot-2, Melville, NY, USA) and photographs were taken with
digital camera (Fuji FinePix F700 Valhalla, NY, USA). These photographs were
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imported into image analysis software (Image J, Scion Image, Frederick, MD, USA) for
measurement. Leaf epidermal cell areas were measured by tracing around the perimeter
of approximately 20 to 30 cells per photograph and calculating the area of this traced
section. Approximately 2 to 5 photographs per palm were used for this measurement
giving a total of approximately 50 to 150 cells measured per palm. Stomatal densities
were calculated by counting the number of stomata within a field of view, then
calculating the area of that field of view. Approximately 15 to 20 different fields of view
were used per palm. Guard cell lengths were calculated by measuring the distance
between the two points where the guard cells meet. Approximately 50 and 100 stomata
were measured per palm in order to calculate average guard cell length.
2.2.7 STATISTICAL ANALYSES
Means, standard errors and Tukey HSD tests were calculated using JMP 7.0
statistical software (SAS Institute, Cary, NC, USA). All linear and polynomial
regressions were fitted using SigmaPlot 2000 Version 6.1 (SPSS Inc. Chicago, IL, USA)
software. R2 and p-values for all regressions were also calculated using SigmaPlot 2000.
2.3 RESULTS
Palms were found to range in height from 2 m tall to 34 m tall. Due to its
significant lean, the crown of one of the palms reported to be 34 m tall was only 27 m
about the ground. However, because hydraulic limitation is concerned with friction
imposed on water travel as well as hydrostatic gradients in water potential, trunk length is
as important in this study as actual crown height above the ground. All other palms did
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not possess a significant lean. The palm reported to be 2 m tall was a juvenile that did
not possess a trunk therefore, because this individual differed so greatly in development
from the other individuals, only petiole sap flux, water potentials and leaf epidermal cell
areas were compared with taller palms, and only to make limited inferences (in
discussion).
Representative diurnal time courses of bole sap flux (g m-2 s-1) in palms ranging in
height from 7 m to 34 m tall are presented in Fig. 2.1 with corresponding VPD and solar
radiation time data. Daily minimums, maximums, means and standard errors for the
palms studied are presented in Table 2.3. There is a slight positive relationship between
palm height and daily bole sap flux per unit leaf area (Fig. 2.2a; p=0.06, r2 = 0.46) due to
the decrease in leaf area with increases in palm height, but no relationship between palm
height and daily petiolar sap flux per unit leaf area (Fig 2.2b; p-value= 0.54). Variability
in Washingtonia robusta sap flux both within and between palms was considerable with
bole sap flux per unit leaf area differing by up to a factor of about 3 and petiole sap flux
per unit leaf area differing by almost a factor of about 6. Roupsard et al. (2006) also
found large variability in coconut palms with sap flow varying by up to a factor of 3
between palms.
Investigation of stem water storage using between-palm cross-correlation analysis
indicated that bole sap flux in large palms lagged behind bole sap flux of small palms by
30 min (n= 4 palms; maximum r2 = 0.68). Similarly, within-palm cross-correlation
analysis indicated a larger petiole-bole time lag in a larger palm (44 min lag in a 28m tall
palm; maximum r2 = 0.87) than a shorter palm (28 min lag in an 8 m tall palm; maximum
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r2 = 0.8). These lags correspond to approximately 16 and 22% of daily water use
respectively according to procedures and assumptions described in Phillips et al (2003b).
Daily maximum stomatal conductances and photosynthetic assimilation rates
were calculated from the curves shown in Figs. 2.3a and b and equations with r2 values
are presented in Table 2.2. Maximum daily stomatal conductance showed no discernable
relationship with tree height (Fig. 2.4a; p-value = 0.36). Additionally, there was no
observable relationship between tree height and either stomatal density (p-value = 0.82)
or guard cell length (p-value = 0.86)(data not shown). Maximum daily photosynthetic
assimilation rate exhibited a positive linear correlation with tree height (Fig. 2.4b;
r2=0.80, p-value=0.041) with taller palms exhibiting higher photosynthetic rates than
shorter palms. There was no observable relationship between LMA and tree height (Fig
2.4c; p-value = 0.19) and individuals did not differ significantly from one another.
Minimum leaf water potentials and the timing of minimum leaf water potentials
were calculated from the curves shown in Fig. 2.3c and equations with r2 values are
presented in Table 2.2. Minimum leaf water potentials were significantly and non-
linearly correlated with tree height (Fig. 2.5a; r2=0.97, p-value=0.0234) with taller palms
generally having more negative minimum leaf water potentials than shorter palms;
although the slope of the curve decreases with increasing height. Also, the time of
minimum leaf water potential was negatively correlated with tree height (Fig 2.5b;
r2=0.61, p-value=0.12) with taller palms reaching a minimum leaf water potential earlier
in the day than shorter palms. Because all individuals were open grown, it is unlikely
that differences in the timing of minimum leaf water potential were the result of
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differences in solar radiation throughout the day. The earliest minimum leaf water
potential (in the tallest palm) was reached at approximately 13:42 PDT and the latest
minimum leaf water potential (in the shortest palm) was reached at 16:36 PDT (mean =
14:42 PDT, SE = 29 min). Although the 2 m tall palm was still a juvenile and therefore
differed developmentally from the other individuals, we feel that comparisons of leaf
water potential are still valid.
Leaf areas were significantly and negatively correlated with tree height. Taller
palms had fewer leaves (Fig. 2.6a; r2=0.6, p-value=0.026) and leaves with smaller areas
(Fig. 2.6b; r2=0.99, p-value = 0.058) than shorter palms; although both of these
relationships were non-linear with the slope of the curve decreasing as tree height
increased. Leaf epidermal cell sizes were found to remain constant in palms 2 m tall to
22 m tall with Tukey HSD tests confirming that cell sizes in these palms did not differ
significantly from one another at a 95% confidence level (Fig. 2.6c). On the other hand,
leaf epidermal cell sizes in both 28 m tall palms and 34 m tall palms were found to be
significantly smaller (p-values < 0.05) than in palms 2 m to 22 m tall. Additionally, leaf
epidermal cells from the 34 m tall palm were found to be significantly smaller than cells
from the 28 m tall palm (Fig. 2.6c; p-value < 0.001).
2.4 DISCUSSION
The hydraulic limitation hypothesis states that as trees grow taller, greater friction
to water flow causes taller trees to reach minimum leaf water potentials sooner in the day
than shorter trees causing stomatal closure that decreases carbon gain (Yoder et al. 1994;
Ryan and Yoder 1997). However, Washingtonia robusta palms showed no discernable
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decrease in daily bole sap flux per unit leaf area, daily petiolar sap flux per unit leaf area,
maximum stomatal conductance, stomatal densities or stomatal sizes with an increase in
tree height suggest that taller palms are not experiencing the effects of hydraulic
limitation. Barnard and Ryan (2003) also found that tallerEucalyptus trees had similar
sap flux per unit leaf area and whole tree stomatal conductance compared to their shorter
counterparts. McDowell et al. (2002a) found similar results in old-growth Douglas-fir
trees, in that stomatal conductance, photosynthetic assimilation and leaf-specific
hydraulic conductance were not significantly different among trees of different heights.
Although hydraulic limitation was not observed in Washingtonia robusta in terms
of lower stomatal conductance in taller palms, we found several alterations in physiology
with height including decreasing leaf area, decreasing leaf cell sizes and more negative
midday leaf water potentials suggesting that tall palms face, and in turn compensate for,
some degree of hydraulic path length constraint. For example, taller palms reached a
minimum leaf water potential sooner in the day than shorter palms. Because all
individuals were open grown, it is unlikely that differences in the timing of minimum leaf
water potential were the result of differences in solar radiation throughout the day. The
timing of minimum leaf water potential may have been even more disparate had all palms
exhibited the same minimum leaf water potential. However, as with many other studies
of trees across a height gradient (McDowell et al. 2002a; Barnard and Ryan 2003;
Woodruff et al. 2007), taller palms also exhibited more negative minimum leaf water
potentials than shorter trees. It is interesting that taller palms would be able to withstand
more negative water potentials than shorter palms and it begs the question; Why dont
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shorter palms keep their stomata open longer and reach the minimum water potentials
that tall palms do? One reason could be that the petiole xylem of taller palms is more
resistant to cavitation than petioles of shorter palms. Woodruff et al. (2007) found
minimum leaf water potentials were highly correlated with the water potential at which
leaves lost hydraulic conductance along a height gradient. Their finding implies that not
only do the leaves at the top of tall trees keep their stomata open at more negative leaf
water potentials, but stomatal closure could be correlated to a loss of leaf hydraulic
conductance.
Lower leaf water potentials were one way in which taller palms compensate for
a longer path length of water travel. However, in order to sustain these more negative
water potentials, leaf cells in taller trees may have had to increase their osmotic potential
in order to maintain turgor (Meinzer et al., 2008). This additional carbon requirement in
taller palms could negatively affect increased height growth. It is also interesting to note
that differences in minimum leaf water potential between the 8 m tall palm and the 28 m
tall palm are approximately 0.4 MPa, and we would expect the taller palm to exhibit, at
minimum, a decrease of 0.2 MPa, simply due to the hydrostatic gradientalone (i.e. ifthere were zero frictional resistance). Therefore, about half of the difference in leaf water
potential between the 8 m tall palm and the 28 m tall palm is a consequence of moving
water against gravity with the other half likely resulting from the added friction to the
water column given the increased path length.
Another compensation that trees can make to offset hydraulic limitation is to alter
their hydraulic architecture so that they have less leaf area for a given unit of sapwood
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area that needs to be supplied with water. For many palm species including Washingtonia
robusta,bole diameters remain more or less constant across various heights once their
stems reach maximum diameter and begin to elongate vertically. Likewise, palm species
do not lose conducting area of their boles through the formation of heartwood. Therefore,
any changes in hydraulic architecture in this and many other palm species occur mainly
through changes in leaf area. In our study, not only did taller palms have fewer leaves
than shorter palms, but the leaves they had were smaller in area. This is unlikely to be
influenced by light environment since all individuals were open-grown.Decreases in leaf
area to sapwood area ratios across height has been seen in several other studies (Schfer
et al. 2000; Phillips et al. 2001; McDowell et al. 2002b; Barnard and Ryan 2003),
although there are some exceptions to this trend (Phillips et al., 2003a). Specifically,
Buckley and Roberts (2006) predict that leaf area to sapwood area ratios should increase
with height growth (until height growth tapers off) in order to maximize carbon gain. Of
course, thes