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Anatomy and Morphology |
Fairchild Tropical Botanic Garden, 11935 Old Cutler Rd, Coral Gables, Florida 33156 USA; Department of Biology, University of Miami, Coral Gables, Florida 33124 USA; USDA Forest Service, 60 Nowelo Street, Hilo, Hawaii 96720 USA
Received for publication October 16, 2006. Accepted for publication April 5, 2007.
ABSTRACT
We tested the hypothesis that trees growing at high elevations with occasional freezing temperatures have smaller diameter xylem vessels than trees of the same species growing at lower and warmer elevations. The young branch wood of the wide-ranging Hawaiian tree species Metrosideros polymorpha (Myrtaceae) was examined in three natural field populations (high, middle, and low elevations: 2469, 1280, and 107 m a.s.l., respectively) and contrasted with seedlings from these populations that were grown in a common garden at middle elevation (1190 m). Previous studies showed that these populations have some genetic differences and have distinctive leaf structure and ecophysiological traits. Vessel diameter was significantly smaller in the high elevation field and common garden plants than in middle elevation plants. However, high elevation vessels were wider in common garden plants compared to field plants, indicating that vessel diameter is determined both by genotype (parental populations) and environment (growing conditions different from those of parents). Reduced vessel diameter has implications for resistance to cavitation induced by freezing and/or drought in plants growing near tree line in Hawaii.
Key Words: altitude • cold tolerance • ecological wood anatomy • elevation • Metrosideros • Myrtaceae • xylem vessel diameter
An active area of ecophysiological investigation is the relationship between xylem conduit size and long-distance water transport. Conduit diameter affects flow resistance, flux rate, susceptibility to cavitation, and cavitation repair in both tracheids and vessels (Hacke et al., 2005
). A body of physiological and experimental literature now supports the view that wider conduits increase the probability of conduit cavitation caused by low xylem water potential or freezing, most likely due to pit membrane features or ice crystal formation within the conduit, respectively (Davis et al., 1999
; Hacke and Sperry, 2001
; Martínez-Vilalta and Pockman, 2002
; Pitterman and Sperry, 2003; Cavender-Bares, 2005
; Hacke et al., 2005
). In general, species native to colder habitats had narrower xylem conduits that those from warmer habitats.
In parallel to these physiological and experimental findings, comparative wood anatomists found that some variable anatomical characters can be correlated to the local environment of the species (e.g., temperature, soil moisture) or its biogeographic range (e.g., latitude, elevation) as reviewed by Carlquist (1975)
, Baas et al. (1983)
, and more recently Anguilar-Rodríguez et al. (2006)
. Because the earlier broad surveys used wood collections (xylaria), they could only relate wood anatomy to the limited habitat and location information recorded for each specimen (these limitations were stressed by Carlquist [2001]
). Van der Graaff and Baas (1974)
surveyed 52 species in 17 genera and suggested that, among other wood features, average vessel diameter and vessel member length tended to decrease with increasing latitude of the natural range of a species. However, when they examined multiple specimens of six species collected over a range of elevations, no relationship between vessel diameter and elevation was found. Other studies focused on a genus with species growing in different habitats. Noshiro and Baas (2000)
found that vessel diameters in two of three species of Cornus were negatively correlated with altitude (wood samples from higher elevations had narrower vessels). Among 31 species of Symplocos, there was a similar but weaker negative correlation between a specimen's altitude and its vessel diameter (van den Oever et al., 1981
). The relationship between vessel diameter and elevation in these multiple species surveys was not definitive.
To reduce the effects of phylogenetic variability (both intergeneric and interspecific), investigators have examined variation in wood anatomy in a single species growing over a range of habitats. Metrosideros polymorpha Gaud. (Myrtaceae), growing at many sites in Hawaii, was examined by Sastrapradja and Lamoureux (1969)
, who tried to correlate variations in stem wood structure with taxonomy, ecology, and within-plant variation. No correlations could be made between anatomical features (including vessel diameter) and rainfall or elevation, which was used as a substitute for temperature. Unfortunately, at the time of their study, the taxonomy of M. polymorpha was still confused and statistical methodology was limited. In another study on a single widespread species (Dodonaea viscoa, Sapindaceae), Liu and Noshiro (2003)
found no relation between vessel diameter and latitude or elevation. On the other hand, Anguilar-Rodríguez et al. (2006)
examined the wood of Buddleja cordata (Buddlejaceae) over a wide geographical range in Mexico. They related wood samples with more precise measures of environmental variables such as soil type, temperature, seasonal rainfall, etc. A canonical correlation analysis indicated that temperature and rainfall were associated with latitude and also with presence of ring porosity. We re-examined their published data and found no correlation between the diameter of wide vessels and either minimum temperature or elevation. Buddleja cordata, however is basically a mountain species with a limited altitudinal range (1350–3040 m a.s.l.), and elevation in their study was not strongly correlated with minimum temperature or other climate parameters. Five subspecies of Eriastrum densifolium (Polemoniaceae) that grow in dry habitats of southern California were examined by Patterson and Tanowitz (1989)
. The average vessel diameter in these subspecies suggested that the widest vessels are found in plants growing in "dry river beds" and in one chaparral site that may have had more available moisture than other sites, but the correlation was unclear because it lacked statistical analysis.
A weakness in the comparisons cited is the imprecise use of elevation, latitude, or habitat as indicators of environmental differences. Latitude and elevation only suggest possible differences in winter minimum temperature, precipitation, or average temperature. Carlquist (2001)
noted that although we assume that moisture availability and freezing affect xylem anatomy, geographical location of a wood sample tells us little about a species' habitat, structure, or phenology, e.g., slope exposure, rainfall, deciduous nature of plant, leaf size, or seasonal stem dieback. Nevertheless, environmental factors clearly do affect some aspects of xylem structure, as shown for soil fertility and wood density (Muller-Landau, 2004
), soil water and vessel diameter (Stevenson and Mauseth, 2004
), climate and growth rings (Wang et al., 2005
), and temperature and vessel diameter (Thomas et al., 2007
).
Ideally, to clarify the influence of elevation on vessel diameter, wood from the same species should be compared using field-collected material from different elevations where climate and environment are well documented. To distinguish which anatomical characteristics are determined by environment and which are determined by genetics and are unmodified by environment, we grew plants in a common garden to find whether anatomical differences persist. We applied these two approaches to the widespread native Hawaiian tree, M. polymorpha. As its epithet indicates, the species has highly variable morphology. It has a great altitudinal range encompassing a variety of habitats, yet the soils in which it grows are similar because they are derived from similar lava substrates. Distinctive ecotypes are found at different elevations of its wide natural distribution. Previous ecophysiological studies used trees from three elevations and seedlings derived from these trees grown in a common garden (Cordell et al., 1998
; Melcher et al., 2000
). Moreover, the high elevation plants experience occasional freezing at their tree line location, and their resistance to freezing has been studied (Melcher et al., 2000
). Thus, we were able to use equivalent trees at field sites and in the same common garden that were used in the earlier physiological research. The wood of small branches (twigs with terminal leaves) was sampled because their vessels are more likely to be affected by short-term freezing events than are vessels in the more massive xylem of tree trunks used previously by Sastraprdja and Lamoureux (1969). In fact, most if not all previous studies of the relation between xylem structure and environment have used wood samples from tree trunks or the larger stems of shrubs. The mature secondary xylem structure in those studies was purposely collected to avoid anatomical variation in "immature" wood near the central pith.
We tested the hypothesis that populations of M. polymorpha at high elevations would have relatively narrow vessels as part of a syndrome of features that help trees to avoid damage caused by freeze- or drought-induced cavitation. Other physiological and structural variations in M. polymorpha were previously correlated to the periodic exposure of these high elevation plants to freezing temperatures (Melcher et al., 2000
). By comparing trees growing at different natural field sites with their seedlings growing in a common garden, we also determined whether variations in vessel diameter were stable for a genotype or influenced by the environment
MATERIALS AND METHODS
Natural habitats
Wild trees used for measurements and as the source of seeds of Ohia (Metrosideros polymorpha Gaud.; Myrtaceae) were growing in natural habitats at three elevations on the island of Hawaii (Table 1). Frost never occurs at low and middle elevations, but occasionally occurs at high elevation near tree line where there have been records of frost on vegetation and freezing temperatures at dawn. Four branches or twigs located 1.5–2 m above ground were randomly collected from each of four trees at each elevation. Diameters of branch axes ranged from 3 to 6 mm.
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and Melcher et al. (2000)
. They were then planted outdoors in a common garden at the Hawaii Volcano Experimental Station, Volcano, Hawaii (elevation = 1190 m a.s.l.). The trees grew in the ground for at least 3 yr and were regularly fertilized and irrigated before branches were harvested. Five branches or twigs located 1.5–2 m above ground were randomly collected from each of five trees (= siblings) from each of the three populations. Diameters of branch axes ranged from 3 to 6 mm. Trees were 3–5 m tall, were growing in full sun on old substrate, and all had the pubescent leaf form.
Anatomical measurements
Branches were fixed in 70% ethanol. Transverse sections were cut with a sliding microtome at 40–90 µm depending on wood properties. Sections were then stained with aqueous toluidine blue and mounted in glycerin for microscopic studies. One section from each twig was photographed at 40x magnification with a digital camera connected to a microscope and a computer, and xylem dimensions were measured with image analysis software (Scion Image, Scion Corp., Frederick, Maryland, USA). Because vessels were not exactly circular, diameter was calculated as the mean of maximum and minimum inside (lumen) diameters. Outer xylem adjacent to the vascular cambium was sampled to compare the most recently formed vessels in the narrow branches of trees of differing age and stem diameters. Four images per section were taken for each section at four arbitrary quadrats positioned alternately with the pith arms (Fig. 1). All vessels positioned completely within the image (dimensions = 190 x 140 µm) were measured. For each elevation, four branches were collected from each of four wild trees and five branches from each of five common garden trees, giving 16 and 25 branch means for wild and common garden trees, respectively. The total number of vessels measured in all samples was 825 in wild trees and 2203 in common garden trees.
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RESULTS
Branch anatomy
The central pith region was roughly cross-shaped and related to the decussate phyllotaxy (Fig. 1). As in other Myrtaceae, internal phloem occurred between the pith periphery and the primary xylem in vaguely delimited regions of primary xylem. The early secondary xylem formed a ring around the pith and was a distinct zone of inner xylem with narrow vessels and thicker-walled fibers. The remaining outer xylem tended to have wider vessels and thinner-walled fibers, sometimes with tangential growth regions or arcs of wood with fibers and few vessels. These areas were not well defined and cannot be considered growth rings. At the departure of leaf traces near the node, the ends of the pith arms had few vessels and were avoided by sampling at the four sites that alternated with the pith arms.
Vessels in the outer secondary xylem tended to be slightly elliptical and radially elongated (Fig. 2) and were surrounded by fibers, vasicentric tracheids, narrow rays, and scattered paratracheal parenchyma. Most vessels were clearly defined and distinguishable from fibers and parenchyma in the captured images. In the few cases in which cells had no visible cytoplasm and could not be distinguished as either large xylem parenchyma or narrow xylem tracheid, the cells were not measured as vessels.
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), was calculated for naturally growing trees at each elevation using the formula: 
d5/ d4. For the plants at natural sites, the means and standard errors were: high = 31.1 µm (±2.05); middle = 41.7 µm (±3.04); and low = 40.0 µm (±0.83). The high elevation mean is significantly different from both the middle and low elevation means (ANOVA with SS = 1.532 x 1013, F2,15 = 7.074, P = 0.003). These values have a similar relationship as the mean diameters in Table 3. DISCUSSION
Elevation correlations
The first attempt to relate variations in wood anatomy of M. polymorpha (at that time still considered different species or subspecies) to environment was made by Sastrapradja and Lamoureux (1969)
. They sampled trunk wood at different heights of the main stem (trunk) from a wide diversity of sites that included different tree morphologies, elevations, and rainfalls. They found no clear correlation between xylem characters (including vessel diameter) and elevation or other site-specific variables. The xylem from all trunks they sampled had a mean tangential vessel diameter of 80.1 µm, more than twice the average diameter of vessels in the small branches used in our study. In trunk wood, vessel diameters gradually increase from near the pith to the vascular cambium, a trend of increasing vessel diameter from juvenile to adult wood found in many dicotyledons. We found a similar trend in large branches of M. polymorpha (data not shown). The juvenile wood adjacent to the pith (marked as "inner xylem" in Fig. 1) and the outer xylem (region of vessel measurements) in branches had narrower vessels than in the trunk.
Narrow vessels (and tracheids) are presumed to be more resistant to embolisms caused by freezing and by very low xylem water potentials (
) during drought. In pine, tracheids of trees growing in dry, warm sites were wider and had greater hydraulic conductivity than those of trees growing in wetter, cooler, montane sites (Maherali and DeLucia, 2000
). Using both comparative and experimental techniques, Pittermann and Sperry (2003)
showed that narrow tracheid diameters are associated with species growing in freeze-prone habitats and that narrow tracheids are more resistant to freeze-induced cavitation. They found that tracheids wider than 30 µm have a greater chance of cavitation upon freezing. The critical conduit diameter, above which tracheids will embolize at a water potential of –0.5 MPa, was about 43 µm. This value is similar to the critical diameter (44 µm) calculated for angiosperms by Davis et al. (1999)
and indicates that susceptibility to freezing-induced cavitation, being dependent upon conduit diameter, is similar in tracheids and vessels. Distribution of freeze-tolerant chaparral shrubs was further correlated with smaller maximum vessel diameters, as seen with a hydraulic mean value of 43–44 µm (Davis et al., 2005
). In evergreen trees growing with a severe dry season, Kondoh et al. (2006)
found that hydraulic conductivity increased with increasing vessel diameter and that drought-induced dieback was also positively correlated with vessel diameter. Presumably, this was due to increased cavitation of wider vessels during periods of severe water stress.
However, there is a relationship between freeze–thaw embolisms and xylem that may complicate interpretations of vessel diameters in M. polymorpha. Davis et al. (2005)
cited their and other studies to show that as xylem becomes more negative, freeze–thaw induced embolisms increase. In Hawaii, freezing temperatures occur at the driest site (= high elevation), where water stress could enhance formation of embolisms. Unfortunately, we have no information on at times of freezing temperatures, but one of us (S. Cordell, unpublished observations) never observed leaf xylem less than –1.5 MPa at any natural site, including wet and dry sites and during periods of water stress (drought). In any case, both drought and freezing would seem to impact wide vessels more than narrow vessels.
The effect of low on vessel cavitation was studied indirectly in M. polymorpha by Santiago et al. (in press
). They measured the percent loss of hydraulic conductivity (PLC) in excised branches taken from natural populations at different elevations. The most negative that caused 50% loss of hydraulic conductivity (PLC50) occurred in high elevation plants ( = –3.3 MPa) (Fig. 1 and Table 2 in Santiago et al., in press
). Trees at wetter and warmer middle and low elevations had PLC50 at less negative water potentials ( = –2.2 and –2.7 MPa, respectively). These values for PLC50 have the same relative relationship as the theoretical hydraulic losses from cavitation in Table 6, mean vessel diameters (Table 3) and mean hydraulic diameters (noted in Results earlier).
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). On clear nights, ice forms in foliage tissue and presumably in small, exposed branches. We found that branches from high elevation trees had significantly narrower vessels than those from lower elevation trees (Table 3). If we assume that vessels in M. polymorpha behave similarly to those of other dicotyledons with respect to freezing-induced cavitation, we can predict that vessels wider than the critical diameter of 44 µm (Davis et al., 1999
) or 43 µm (Pittermann and Sperry, 2003
) will be susceptible to embolism. These widest vessels also transport the bulk of water, as determined theoretically by the Hagen–Poiseuille relationship for capillary conduits: hydraulic conductance is proportional to vessel inside diameter raised to the fourth power (d4). Using a critical diameter value of 40 µm, we calculated the theoretical hydraulic loss from cavitation based on trees of M. polymorpha growing in the natural parent population (Table 6). Thus, in high elevation trees, 3.7% of vessels are wider than 40 µm, and in functional terms, these same vessels contribute 20.1% to the total theoretical hydraulic conductance. In middle elevation trees, 24% of vessels are wider than 40 µm, yet they contribute 63.7% to total theoretical conductivity. If the findings of freeze-induced cavitation from other species are extrapolated to M. polymorpha, cavitation of wide vessels would have a far smaller effect on high elevation trees than on middle and low elevation trees (Table 6).
Fewer wide vessels will reduce freeze damage to the branch xylem in theory, but this assumption must still be supported by direct measurement of xylem dysfunction caused by freezing as was done in other species (Davis et al., 1999
; Cordero and Nilsen, 2002
; Martínez-Vilalta and Pockman, 2002
; Pittermann and Sperry, 2003
; Cavender-Bares et al., 2005
). This relation between greater PLC and wider conduits (tracheids and vessels) was shown clearly in a survey of 12 gymnosperms and dicots by Feild and Brodribb (2001)
. Unfortunately, Melcher et al. (2000)
did not measure ice formation within branch vessels of M. polymorpha or the direct effect of a freeze–thaw cycle on branch conductivity in the field. If supported by additional data, the protective effect of fewer wide vessels would be another in the list of structural feature that helps high elevation trees survive near tree line, namely, smaller and thicker leaf blades; increased pubescence; and increased capacity of leaves to supercool (smaller intercellular spaces, lower apoplastic water content, and increased osmolarity) (Cordell et al., 1998
; Melcher et al., 2000
).
The high elevation site is the driest site as well as the coldest (Table 1). Precipitation is one-half to almost one-third that of the middle and low elevation sites. We can assume that dry periods might occur more frequently at the high site, causing relatively low xylem , although we did not measure minimum . The observed values of PLC50 (Santiago et al. [in press]
noted earlier) suggested that high elevation plants could tolerate the very negative . Regardless of whether cavitation would be caused by drought or freezing, the fewer wide vessels would reduce hydraulic failure in high elevation plants.
Common garden implications
By comparing trees grown in the common garden with those grown in the natural sites, we could estimate the relative effects of environment and genetics on vessel diameter. We found that vessels were narrower in trees derived from high elevation than from middle elevation trees, although at a lower level of significance than found among naturally growing trees (Table 3). High elevation vessels did not differ from low elevation vessels in the common garden. When the differences between field collected and common garden material were compared for the same elevation, there was a significant difference between high elevation trees but not between middle or low elevation trees. These findings show that in the common garden, vessels were wider in trees derived from high elevation than in parental field trees, but were narrower than in trees derived from middle elevation. It follows that vessel diameter has both a genetic component that distinguishes high elevation trees from low and middle elevation trees, and an environmental component by which trees derived from high elevation respond to the common garden environment to produce slightly wider vessels. The low and middle elevation trees show no change when grown in the common garden, which is essentially at middle elevation. Vessel size in high elevation trees may be genetically fixed, i.e., all seedlings have narrower vessels, or seedlings at high elevation sites may have been selected during freezing events because those with wider vessels died.
If vessel size is genetically fixed, what is the evidence for possible gene flow between populations? The five or six recognized varieties of M. polymorpha often have distinct morphological and physiological differences, but overlap in both types of characteristics is also common (James et al., 2004
and papers reviewed therein). James et al. (2004)
reported on combinations of the extremes in morphological character states that indicate genetic mixing of local populations in wet and dry habitats and at different elevations. Evidence for interbreeding between dry high and moist middle elevation populations (similar to our high and middle elevations) was seen in results of random amplified polymorphic DNA (RAPD) analysis (James et al., 2004
). Thus, there appeared to exist a balance between gene flow (facilitated by wind-dispersed, small seeds) and specific selective pressures, resulting in genotype differences but not distinct species.
In a relevant common garden study the hydraulic properties of clones of hybrid Eucalyptus, also in the Myrtaceae, were examined (vander Willigend and Pammenter, 1998
). Four clones were grown at two sites: mesic and dry. Hydraulic conductivities were relatively constant within a clone at both sites. Therefore, the clone most vulnerable to cavitation had the least growth and the greatest dieback during a severe draught. Unfortunately, vessel diameters were not examined so that the structural basis for cavitation differences among clones was unclear. Vulnerability to cavitation was genetically determined. This conclusion was later supported in a survey of five tree species grown in a common garden (vander Willigen et al., 2000
). Mean conduit diameter was correlated to vulnerability to cavitation, while hydraulic conductivity did not differ among species. On the other hand, a greater effect of environment on wood structure was suggested when 17 clones of Eucalyptus globulus were grown at two sites by Leal et al. (2003)
. They measured vessel area (a proxy for diameter) and found vessel size varied by clone and that all vessels tended to be larger at one site, but they did not statistically analyze their vessel size data.
In parallel studies of physiological and morphological features, Cordell et al. (1998)
found that leaf size, petiole length, and internode length maintained their correspondence with elevation in the common garden, and the authors considered these characteristics to be strongly genetically based. Character differences such as leaf thickness and pubescence (although the trend of increased pubescence with higher elevations remained), some leaf anatomy traits, and various physiological parameters related to photosynthesis showed more change. Differences that declined or disappeared in the common garden were considered as more environmentally induced. Melcher et al. (2000)
found that both field and common garden leaves had the same response to freezing (i.e., they had the same temperature of ice formation) and that this response seemed to be correlated with other stable or genetically fixed characters (e.g., high leaf mass per unit area, cell density, and small extracellular spaces). Other features showed some variability in the common garden and indicated a combination of genetic and ecological determination. A large change in a feature in the common garden indicated greater phenotypic variability and relatively less genetic determination.
Conclusions
In this study, we hypothesized that high elevation plants, which are more resistant to freeze damage than lower elevation plants, also have significantly narrower vessels than lower elevation plants. That hypothesis was supported by our data and is consistent with other ecophysiological studies. The difference in vessel diameter persisted in common garden plants, indicating a strong genetic basis for vessel diameter. We suggest that branch wood with smaller vessel diameters is better able to survive freezing or periodic drought because narrow vessels are less likely to cavitate.
FOOTNOTES
1 The authors thank C. Goldstein and S. Atwater for technical assistance, L. Santiago and J. Sah for statistical advice, and C. Lewis for discussions on phenotypic plasticity. 
5 Author for correspondence (jfisher{at}fairchildgarden.org
; phone: +1 (305) 665-2844, ext. 3412, fax: +1 (305) 665-8032
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