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Anatomy and Morphology |
2Fairchild Tropical Garden, 11935 Old Cutler Road, Coral Gables (Miami), Florida 33156 USA; 3Department of Biological Sciences, Florida International University, Miami, Florida 33199 USA; 4Department of Biological Sciences, The National University of Singapore, 117543 Singapore
Received for publication May 10, 2001. Accepted for publication August 23, 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMaterials and MethodsResultsDiscussionLITERATURE CITED |
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1200 vessel elements (cells). The widest vessel in that same stem was 532 µm in diameter. Long, wide vessels decrease resistance and increase water transport efficiency. In addition, we suggest that wide metaxylem vessels may have an important function in water storage.
Key Words: Arecaceae • Calamoideae • Calamus • Daemonorops • Korthalsia • Palmae • Plectocomia • vessels • xylem
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMaterials and MethodsResultsDiscussionLITERATURE CITED |
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; Tomlinson, 1990
). These climbing species also have the widest xylem vessels among palms (Klotz, 1978a
) and thus follow the widespread trend of climbers in having wider vessels than do related nonclimbing species (Ewers and Fisher, 1989b
; Ewers, Fisher, and Chiu, 1990
; Gartner, 1995
). Although rattan stems are often coiled on the forest floor or loop through the rain forest canopy, they rarely root and thus represent a very long pathway for water transport from roots to the leaf crown. In addition, all vascular tissues are primary and thus must function for the entire life of the stem. To better relate and understand these unique structural and physiological attributes, we determined the size and structure of the vessels in a variety of rattan palms growing under natural conditions.
Vascular features and details of vascular architecture were described in qualitative and quantitative terms for the first time by Tomlinson and Fisher (2000)
and Tomlinson et al. (2001)
. The present study extends these descriptions and further supports the original conclusions about the special vascular arrangement in rattans relative to other palms.
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Materials and Methods |
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TOPABSTRACTINTRODUCTIONMaterials and MethodsResultsDiscussionLITERATURE CITED |
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. Herbarium vouchers are deposited in FTG (Fairchild Tropical Garden herbarium) and SINU (National University of Singapore herbarium).
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). We used two methodologies for paint infusion into large stems. In method 1, stems were cut (with a long-handled pruner) underwater at their bases (water was taken from either a clear stream or a tap) in a plastic basin and then recut several times underwater. The surface was then carefully shaved with a razor blade. The stem was transferred to a container of the diluted latex paint, keeping the cut surface flooded at all times to prevent introduction of air into the xylem. Paint uptake was driven by transpiration of the attached leaves. After there was no observable uptake of paint (usually a few days, depending upon weather conditions), the shoot was pulled from its supporting trees and transported to the laboratory.
In method 2, shoots were first pulled from the supporting trees. If the stem was undamaged, its base was cut (with a long-handled pruner) underwater as in method 1, and a container of water was taped to the stem to keep the cut end submerged in the water while the shoot was transported to the laboratory. All lower leaves were cut off to leave a small crown of 6–10 terminal leaves. In the laboratory, the stem was recut, shaved with a razor blade, and a plastic tube was tightly fitted over the cut end while it remained underwater. Diluted latex paint was fed into the stem through the plastic tube with a 2.5-m column of paint (pressure = 25 kPa). Paint uptake was driven by the pressure applied by the paint column and transpiration of the few attached leaves. Some stems were similarly supplied with diluted latex paint via plastic tubing in the field immediately after pulling the stem from its supporting tree. After paint flow stopped (usually after a few days), the stem was harvested. For both methods, stems were cut longer than 10 m, which was longer than the longest vessels, as indicated in preliminary studies.
Harvested stems treated by either method were cut into uniform lengths, carefully labelled, and the basal end of each segment was observed under a stereozoom microscope. The number of paint-filled (or paint-lined) vessels were counted as described in Ewers and Fisher (1989a)
. The raw counts of paint-filled vessels were used for calculating the frequency distributions of different vessel lengths according to the procedures of Ewers and Fisher (1989a)
and Zimmermann (1983)
.
General histological observations were made on hand sections of stem stained with aqueous toluidine blue O. Slivers of stem were macerated in Jeffrey's solution (chromic acid + nitric acid) for several days (Ruzin, 1999
), washed, stained with safranin, and mounted on slides in corn syrup or glycerine beneath a cover glass for light microscope observations. Photomicrographs were made of cut surfaces and hand sections of stems. Vessel diameter was measured directly with the ocular scale of a compound light microscope.
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Results |
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TOPABSTRACTINTRODUCTIONMaterials and MethodsResultsDiscussionLITERATURE CITED |
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. Within one transverse section, all the variations in the anatomy of a single large vascular bundle (as illustrated in Tomlinson et al., 2001
) could be observed in different bundles. The structure of a large vascular bundle changes from its origin until it departs the stem as a leaf trace. This change has the following three phases: (a) the basal end is narrow with little to no protoxylem; (b) along most of the length is wide, with one large metaxylem vessel and two regions of phloem (Fig. 2, right side with one phloem area only partially seen, and Fig. 5); and (c) the distal region where the bundle migrates to the stem periphery to become a leaf trace and has narrow metaxylem vessels and an increased area of protoxylem (Fig. 2, left side, and Fig. 3, upper side).
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and often long narrow tails extending beyond the transverse perforation (Fig. 6). The wide metaxylem vessel elements of Korthalsia rigida ranged in cell length from 2.65 to 4.55 mm. Narrow metaxylem vessel elements have either scalariform (Fig. 7) or simple (Fig. 8) perforation plates. In K. rigida, intervascular pitting is alternate. Short vessels elements that form the connection between longitudinal bundles via transverse commissural bundles were very irregular in outline, often many armed, and with more than two simple or scalariform perforations. In one irregular element, up to five separate scalariform perforation plates were observed. Protoxylem elements rarely had intact cell ends due to ripping of the thin primary wall during maceration and processing. Early-formed elements had annular thickenings and late-formed elements had helical wall thickenings with progressively tighter coils of wall thickening (Fig. 9). A few helical elements with tight coils were nearly entire, and most had long tapered ends, although two were observed with simple perforations in K. rigida (collection VR9) on their tapering ends.
Functional vessels and vascular bundles per stem stained with dye
The majority of vascular bundles in stems that were cut and supplied with paint had at least one element filled with paint at the cut end. This was evident when the cut end was viewed after the painted surface was shaved with a razor thus removing 1–2 mm from the original proximal end, the point of paint introduction (Fig. 1). In large stems, painted bundles numbered 270 (C. insignis, collection VR2), 500 (D. hystrix, collection VR12), and 430 (P. elongata, collection VR27).
Two stems were cut underwater and placed in aqueous safranin stain while still attached to their supporting trees. Essentially all vascular bundles were colored and assumed to be functional in these transpiring plants. At 5 mm from the cut surface of D. hystrix (collection VR36), 1194 bundles were stained, and 44 bundles (8 wide bundles and 36 narrow bundles or leaf traces) were unstained (3.6% of the total number). These unstained bundles were presumably nonfunctional in water trasnport. In D. grandis (collection VR35), there were a total of 815 bundles, and of these, 2.0% were unstained at 5 mm from the cut surface.
Frequency distribution of vessel lengths
The calculated distributions of vessel lengths by the latex paint method showed many short vessels and a decreasing percentage of long vessels (Figs. 10 and 11). In a few stems (Figs. 12–14), additional counts were made to distinguish between paint-filled metaxylem (Figs. 3 and 4) and protoxylem vessels (Fig. 5). The paint-filled protoxylem elements were clearly defined by their position within the vascular bundle. In a few leaf traces, protoxylem is particularly obvious since the large metaxylem vessel(s) became progressively smaller and the protoxylem vessels increased in number and size. The absence of metaxylem vessels between 0.8 and 1.8 m long (Fig. 12) was an artifact of the technique. Many vessels that were between 0.6 and 2.0 m in length had only traces of paint lining the vessel lumen. Presumably, these long vessels were completely filled with paint at their distal ends and basal ends but not in their central regions. Thus, many vessels were not counted at these intermediate lengths and consequently distorted the frequency calculations. Protoxylem vessels (Figs. 13 and 14) followed a similar frequency distribution as metaxylem (Fig. 12) and all vessels (Figs. 10 and 11), but protoxylem vessels were shorter.
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). There was a general linear relationship between the length of the longest vessel of a stem and the widest vessel in that same stem (Fig. 15); however, the correlation was not very strong (R2 = 0.416, N = 17). When a similar data set was plotted (data not shown) using the diameter of the longest vessels measured when their bundles were still in the central region of the stem and therefore with a wide metaxylem vessel, diameter and length had a weaker correlation (R2 = 0.316, N = 32).
To estimate the number of cells that form a single long vessel, we examined two species (one stem each) and used macerations to measure length of the wide metaxylem vessel elements. In K. rigida (collection VR9), the maximum vessel length was 3.96 m and its wide vessel element length was 3.276 mm (mean for N = 10). Thus, this longest vessel is constructed of 1208 cells. In D. grandis (collection VR13), the maximum vessel length was 2.7 m, vessel element length was 2.236 mm (mean for N = 10), and therefore, the longest vessel was 1207 vessel elements.
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Discussion |
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TOPABSTRACTINTRODUCTIONMaterials and MethodsResultsDiscussionLITERATURE CITED |
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. Narrow commissural bundles form transverse connections between large longitudinal vascular bundles. The narrow and highly contorted metaxylem elements of commissural bundles are clearly vessel elements, as shown in macerations (Fig. 8). We did not observe whether perforations were present at the connection of commissural elements with wide vessel elements of the large vascular bundles. Furthermore, as we did not observe paint-filled commissural bundles, such perforations are unlikely.
Dye ascents demonstrated that >95% of vascular bundles are functional in water transport in long mature stems. Functional vessels were similarly demonstrated by paint movement both under pressure and tension using paint columns or paint uptake by intact shoots, respectively. Many short and a few long vessels occur in metaxylem and protoxylem. Although the technique may not be precise (i.e., when vessels fail to fill completely with latex particles), paint did travel the length of the longest vessels into the leaf traces.
Long vessels are correlated with wide vessels, a trend found in other climbers (Ewers and Fisher, 1989a, b
; Ewers, Fisher, and Chiu, 1990
; Fisher and Ewers, 1995
). Vessel element diameter is correlated to vessel element length and to the climbing (or scandent) habit in palms (Klotz, 1978a, b
). Thus, the generalization that climbing plants (e.g., dicots, monocots, and Gnetum) have wider vessels than related nonclimbing species continues to be supported. The longest metaxylem vessels (four species with a vessel longer than 3 m) can be compared to the length of internodes in these species. When the maximum length for each species (Table 2) is divided by the internode length for that same stem (Table 1), we find that the mean number of internodes included by this longest vessel was 13.25 (N = 8, range = 8–18). While there is considerable quantitative variation among stems of the same species and replicate sizes are small, there appears to be a general range in the absolute maximum length possible for a wide vessel, namely the total length of a large vascular bundle. This upper limit to vessel length equals the maximum length of a single large vascular bundle. This finding is in accord with the those of Tomlinson et al. (2001)
who determined that large vascular bundles were continuous through 3 m or 15 internodes of Calamus longipinna.
Protoxylem vessels attained maximum lengths of 20–60 cm and were frequently observed in many individual vascular bundles. Yet the observed lengths of 2 and 3 m in Korthalsia rigida were unexpected and far greater than other maximum protoxylem vessel lengths (Table 2). This species should be reexamined to confirm this extraordinary finding and eliminate the possibility of some artifact of the technique. There is little or no published information on the lengths of vessels in other palms, so we cannot contrast vessel lengths in palms with different growth forms.
In functional terms, we conclude that xylem water in rattan stems has the following potential pathway. Water enters the stem base from connections between adventitious roots and longitudinal stem vascular bundles. Details of initiation and structure of these root/stem vascular connections are poorly described for palms (Tomlinson, 1990
). Water travels along both wide and narrow wide vascular bundles located both in the stem center and periphery, respectively. At least 95% of all bundles in the base of a mature stem are functional in transport of aqueous dye solution. In many of these bundles, both proto- and metaxylem elements are functional. In fact, surveys of old stems of climbing palms (Fisher and Ewers, 1991
) found little evidence of tyloses or deposits (gums or mucilage) within vessels, which would be expected in nonfunctional vessels.
Water can pass from one wide vascular bundle to another by the interconnecting vessels of commissural bundles. These commissural bundles are scattered irregularly along the length of the stem (Tomlinson et al., 2001
). There is no pattern of vascular connections or plexi associated with the nodes. However, the structural changes in the xylem of leaf traces means that water must move increasingly through the protoxylem since the metaxylem of each vascular bundle decreases as the bundle approaches the stem periphery. At nodes with attached live leaves, all water enters the leaf base via the protoxylem of the major leaf traces. The peripheral small bundles that lack protoxylem also enter the leaf sheath and may contribute to water flow as a result of commissural interconnections, but we did not study this. Presumably, the protoxylem should experience the extreme in low water potentials. Thus, the protoxylem of leaf traces in the leaf sheath should cavitate before the metaxylem of the leaf trace in the stem.
Within the stem, proto- and metaxylem vessels are separated by at least one layer of live parenchyma cells, which form a living barrier to possible transfer of gas bubbles between proto- and metaxylem vessels (Tomlinson et al., 2001
). In other palms, the vessels of these two xylem regions may touch directly, presumably offering less resistance to gas movement via pit membranes or pores (Tomlinson and Fisher, 2000
).
Water loss by foliar transpiration in palms appears to be similar to other plants and under expected stomatal control (Zobel and Liu, 1980
; Sperry, 1986
; Holbrook and Sinclair, 1992a, b
), although we have no information for rattans. The large-trunked palm tree, Sabal palmetto, was shown to be capable of stopping essentially all transpiration when water stress occurred after digging it from the ground (Holbrook and Sinclair, 1992a, b
). In this palm, water stored in the trunk (in cells of living tissues and in free space within vessels) was critical to survival during prolonged water stress. It may be possible that the volume of water stored in wide and long vessels of rattans may have a similar function, in addition to efficient water transport, as suggested in other lianas (Ewers, Fisher, and Chiu, 1990
). Like other lianas of tropical rainforests, the leafy crown of a rattan is eventually exposed to full sun conditions when it reaches the top of the forest canopy. When rattans grow above the forest canopy, they produce shorter internodes (Putz, 1990
), a possible indication of reduced growth rate caused by increase light, transpiration, and other environmental factors. During periods of limited rainfall, rattans and other lianas can experience severe water stress. At such times, both stomatal closure and stem water storage would aid survival. In other lianas, water-storing tubers or succulence of stems and leaves are common (Fisher and Ewers, 1991
). Rattans lack tuberous roots and their narrow stems have a small proportion of parenchyma that could function in water storage. However, their long stems with a relatively large volume of water in wide vessels represent a significant water reservoir that would become available if cavitation of vessels occurred during periods of extreme water stress (Holbrook, 1995
). If cavitation of wide vessels does play a role in water supply during draught periods, then the question of vessel refilling must be addressed. Further studies should also focus on the water capacity of rattan stems compared to nearby nonclimbing palms, as well as their relative degrees of stomatal control.
At present, we have no information on production of embolisms in rattan xylem. Yet the low percentage of nonfunctional vascular bundles in old stems suggests either a lack of vessel cavitation or a mechanism for refilling vessels (and tracheids). Other lianas have root pressure that is sufficient to refill air-filled xylem, as in Vitis (Sperry et al., 1987
), or to decrease xylem tension and thus assist in removal of embolisms (Fisher et al., 1997
). In a nonclimbing palm, Sperry (1986)
found that embolisms were dissolved when xylem pressure potential approached that of the atmosphere during periods of rain. When stem bases of cultivated species of Calamus, Daemonorops, and Desmoncus (a climbing nonrattan palm) were cut at dawn during rainy periods, no exudation appeared, thus indicating no root pressure (Fisher et al., 1997
); however, there was an indication of root pressure in one species of Calamus cultivated in a mountainous rainforest. We suggest that future measurements for possible root pressure are needed to better understand water conduction for rattans growing in natural environments.
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FOOTNOTES |
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5 Author for correspondence (jfisher{at}fairchildgarden.org
).
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMaterials and MethodsResultsDiscussionLITERATURE CITED |
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Ewers F. W. J. B. Fisher 1989a Techniques for measuring vessel lengths and diameters in stems of woody plants. American Journal of Botany 76: 645-656[CrossRef][ISI]
Ewers F. W. J. B. Fisher 1989b Variation in vessel length and diameter in stems of six tropical and subtropical lianas. American Journal of Botany 76: 1452-1459[CrossRef][ISI]
Ewers F. W. J. B. Fisher S.-T. Chiu 1990 A survey of vessel dimensions in stems of tropical lianas and other growth forms. Oecologia 84: 544-552[CrossRef][ISI]
Fisher J. B. F. W. Ewers 1991 Structural responses to stem injury in vines. In F. E. Putz and H. A. Mooney [eds.], The biology of vines, 99–124. Cambridge University Press, New York, New York, USA
Fisher J. B. F. W. Ewers 1995 Vessel dimensions in liana and tree species of Gnetum (Gnetales). American Journal of Botany 82: 1350-1357[CrossRef][ISI]
Fisher J. B. G. Angeles A. F. W. Ewers J. López-Portillo 1997 Survey of root pressure in tropical vines and woody species. International Journal of Plant Sciences 158: 44-50[CrossRef]
Gartner B. L. 1995 Patterns of xylem variation within a tree and their hydraulic and mechanical consequences. In B. L. Gartner [ed.], Plant stems: physiology and functional morphology, 125–149. Academic Press, San Diego, California, USA
Holbrook N. M. 1995 Stem water storage. In B. L. Gartner [ed.]), Plant stems: physiology and functional morphology, 151–174. Academic Press, San Diego, California, USA
Holbrook N. M. T. R. Sinclair 1992a Water balance in the arborescent palm, Sabal palmetto. I. Stem structure, tissue water release properties and leaf epidermal conductance. Plant, Cell and Environment 15: 393-399[CrossRef]
Holbrook N. M. T. R. Sinclair 1992b Water balance in the arborescent palm, Sabal palmetto. II. Transpiration and stem water storage. Plant, Cell and Environment 15: 401-409[CrossRef]
Klotz L. H. 1978a Observations on diameter of vessels in stems of palms. Principes 22: 99-106
Klotz L. H. 1978b Form of the perforation plates in the wide vessels of metaxylem in palms. Journal of the Arnold Arboretum 59: 105-128[ISI]
Putz F. E. 1990 Growth habits and trellis requirements of climbing palms (Calamus spp.) in north-eastern Queensland. Australian Journal of Botany 38: 603-608[CrossRef]
Ruzin S. E. 1999 Plant microtechnique and microscopy. Oxford University Press, New York, New York, USA
Sperry J. S. 1986 Relationship of xylem embolism to xylem pressure potential, stomatal closure and shoot morphology in the palm Rhapis excelsa. Plant Physiology 80: 110-116
Sperry J. S. N. M. Holbrook M. H. Zimmermann M. T. Tyree 1987 Spring filling of xylem vessels in wild grape. Plant Physiology 83: 414-417
Tomlinson P. B. 1990 The structural biology of palms. Oxford University Press, Oxford, UK
Tomlinson P. B. J. B. Fisher 2000 Stem vasculature in climbing monocotyledons: a comparative approach. In K. L.Wilson and D. A. Morrison [eds.], Monocotyledons: systematics and evolution, 89–97. CSIRO, Collingwood, Victoria, Australia
Tomlinson P. B. J. B. Fisher R. E. Spangler R. A. Richer 2001 Stem vascular architecture in the rattan palm Calamus (Arecaceae–Calamoideae–Calaminae). American Journal of Botany 88: 797-809
Zimmermann M. H. 1983 Xylem structure and the ascent of sap. Springer Verlag, Berlin, Germany
Zobel D. B. V. T. Liu 1980 Leaf-conductance patterns of seven palms in a common environment. Botanical Gazette 141: 283-289
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