JXB Advance Access originally published online on March 9, 2007
Journal of Experimental Botany 2007 58(7):1651-1662; doi:10.1093/jxb/erm017
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© 2007 The Author(s).
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.This paper is available online free of all access charges (see http://jxb.oxfordjournals.org/open_access.html for further details)
RESEARCH PAPER |
Pressure gradients along whole culms and leaf sheaths, and other aspects of humidity-induced gas transport in Phragmites australis
Department of Biological Sciences, University of Hull, Hull HU6 7RX, UK
* Present address and to whom correspondence should be sent: Department of Bioproduction, Faculty of Horticulture; Chiba University, Matsudo, Chiba 271-8510, Japan. E-mail: afreen{at}restaff.chiba-u.jp
Received 30 June 2006; Revised 24 December 2006 Accepted 18 January 2007
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Abstract |
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Emergent aquatic macrophytes growing in waterlogged anaerobic sediments overlain by deep water require particularly efficient ventilating systems. In Phragmites australis (Cav.) Trin. ex Steud, pressurized gas flows, generated by humidity-induced diffusion of air into leaf sheaths, enhance oxygen transport to below-ground parts and aid in the removal of respiratory CO2 and sediment-generated CO2 and methane. Although modelling and flow measurements have pointed to the probable involvement of all leaf sheaths in the flow process and the development of pressure gradients along the whole lengths of living culm and leaf sheaths, direct measurements of pressure gradients have never been reported. The aim of this study was to search for pressure gradient development in Phragmites culms and leaf sheaths and to determine their magnitudes and distribution. In addition, dynamic (with gas flow) and static pressures (no flow condition) and their relationship to flows, leaf sheath areas, and living-to-dead culm ratios were further investigated. Dynamic pressures (
Pd) recorded in the pith cavities of intact (non-excised) leafy culms, pneumatically isolated from the below-ground parts and venting through an artificial bore-hole near the base, revealed a curvilinear gradient of pressure ‘asymptoting’ towards the tips of the culms. Similarly, Pd in upper and lower parts of leaf sheaths increased with distance from the base of the culm, with values in the upper parts always being greater. Curvilinear gradients of pressure were also found along pneumatically isolated individual leaf sheaths, but radial channels linking the leaf sheath aerenchyma with the pith cavity of the culm appeared to offer little resistance to flow. In keeping with predictions, static pressure differentials (Ps) achieved in intact and excised culms and single leaf sheaths on intact culms proved to be relatively independent of leaf sheath area, whereas the potential for developing convective flows (pressure-driven flows) increased with increasing leaf sheath area. As measured by the ventilating coefficient [1–(Pd/(Ps)] the old dead (efflux) to living (influx) culm ratio of 1:12 compared with 1:25 raised ventilating efficiency from 31% to 71%, giving flows per tall culm into the rhizome system of c. 2.8 cm3 and 6.5 cm3 min–1, respectively. It was concluded that dynamic pressure gradients probably extend along the whole length of the leafy culms and leaf sheaths of Phragmites and that all leaf sheaths and all exposed points along the leaf sheaths can contribute convective gas-flow to the rhizome system. Key words: Aeration, convective flow, diffusion, humidity-induced convection, oxygen, Phragmites australis, pressurized gas flow, pressure-flow resistance, ventilating efficiency
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Introduction |
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TopAbstractIntroductionMaterials and methodsResults and discussionFinal commentsReferences |
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Phragmites australis (Cav.) Trin. ex Steud., a rhizomatous plant of the family Poaceae which can thrive in shallow, deep, and almost stagnant water, has recently become a focal point of renewed interest because of its use in water purification. Reed beds form natural phytodepuration systems, and artificially constructed Phragmites beds are currently used extensively for the purposes of treating domestic, agricultural, and industrial effluent (Lawson, 1985; Athie and Cerri, 1987; Cooper and Findlater, 1990; Mandi et al., 1996; Davies et al., 2005). An important part of the purification process is the oxidation of ammonium compounds to nitrite and nitrate (Kirk and Kronzucker, 2005); for this, the efflux of oxygen from the plant's roots promotes the growth of aerobic nitrifying bacteria (Hansen and Andersen, 1981). The reed–periphyton complex also plays an important biofilter role in the adsorption and retention of cations, especially of heavy metals (Lakatos et al., 1999).
Phragmites, in common with other emergent macrophytes, depends upon the passage of atmospheric oxygen through an internal gas transport system of low resistance to gas flow, to supply the respiratory needs of rhizomes and roots buried in anoxic sediment. Moreover, the efflux of oxygen from the permeable root apices and fine laterals protects these parts against phytotoxins such as compounds of FeII, MnII, sulphides, and organic acids that commonly exist in waterlogged soils (Mendelssohn and Postek, 1982; Begg et al., 1994; Lee et al., 1999; Pedersen et al., 2004).
For quite a long time it was generally assumed that the only ventilating mechanism in P. australis and other wetland plants involved the reciprocating gas-phase diffusion of oxygen and carbon dioxide through the well-developed, interconnecting aerenchymatous and non-aerenchymatous cortical gas-spaces of the submerged and non-submerged parts. However, in wetland species such as Phragmites, Nuphar, Eleocharis, Nelumbo, and Typha, and some others, where the roots arise from rhizomes which may be more than 0.5 m below the surface of the sediment, and where the shoot system may also be partially submerged, aeration can be enhanced during the growing season by pressurized (convective) internal gas flows (‘winds’) and oxygen is transported much more quickly than by diffusion alone (Dacey, 1980; Dacey and Klug, 1982; Schröder et al., 1986; Grosse and Mevi-Schutz, 1987; Mevi-Schutz and Grosse, 1988; Armstrong and Armstrong, 1990a, b, 1991; Brix et al., 1992; Sorrell and Boon, 1994; Tornbjerg et al., 1994; White and Ganf, 2000).
The discovery of pressurized (convective) gas flow in plants appears to have originated with Dufour (1874a, b), who noted the bubbling of gases from wetted water lily leaves in bright light. Dufour was probably the first to study humidity-induced convection (HIC) and the diffusion process leading to it, namely ‘diffusion hygrometrique’ (Dufour, 1875). The process of HIC depends upon (i) a diffusion of air into the plant under the influence of concentration gradients caused by the humidity differential which exists between the humid gases within the internal gas spaces and the comparatively dry atmosphere outside and (ii) the presence of microporous partitions or surfaces in which the pores offer a more significant resistance to pressure flow than to diffusion. The mechanism is described in detail and modelled in Armstrong et al. (1996a, b). In P. australis the HIC is driven by a diffusion of ‘dry’ air through the stomata of living leaf sheaths and, to a smaller extent, of culm nodes, into the humid atmosphere of the substomatal cavities (Armstrong and Armstrong, 1991). The constant humidification of the atmosphere within the leaf sheath creates and maintains high water vapour levels and thus dilutes the internal concentrations of oxygen and nitrogen so that they are significantly less than in the drier external atmosphere (in saturated air at 20–30 °C the water vapour content is 2–3% by volume). Since the depths of the stomatal pores are relatively short, 
15 µm, a rapid diffusive inflow of O2 and N2 is promoted under the humidity-induced diffusion (HID) gradient. Also, because of the narrowness of the pores (c. 0.2 µm) there is significant stomatal resistance to Poiseuille (pressure flow) from leaf sheath to atmosphere (Armstrong et al., 1996a, b), resulting in pressurization of the substomatal atmosphere as the O2 and N2 concentrations within the plant rise in a tendency to equalize with those outside. Thus the total pressure within the leaf sheath gas space becomes greater than atmospheric by an amount numerically equal to the water vapour partial pressure beneath the stomata and, if there is no other path for gases to escape, the pressure will equilibrate to give what is known as the static (no flow) pressure, Ps. In P. australis, this tendency to pressurize usually drives a convective flow (pressurized, bulk flow) of gases through the path of least resistance, i.e. via the gas space system of the culm into the underground parts, from where they are vented back to the atmosphere through the snapped-off ends of old, dead, flowering culms (Armstrong and Armstrong, 1990a, b). The pressures developed in this condition have been termed dynamic (with flow) pressures (Pd). The energy maintaining HIC convection is the latent heat necessary to evaporate water from the cells walls lining the gas spaces in the leaf sheaths, particularly the substomatal cavities. Convective flow directly enhances rhizome aeration and hence increases the diffusive aeration of the roots by increasing the oxygen concentrations and decreasing the CO2 at the root–rhizome junction (Armstrong and Armstrong, 1990b). Because of stomatal closure and reduced energy inputs in darkness, flows are much greater during the day than at night (Armstrong and Armstrong, 1990a, b) and some hypoxia may occur in the more remote tissues of the root–rhizome system at night. However, any hypoxic stress should be short-lived and Phragmites is also moderately tolerant of anoxia (Brändle and Crawford, 1987). Rhizosphere oxidation by radial oxygen loss (ROL) from the roots will also be diminished at night, but re-reduction of oxidized rhizospheres is a much slower process than the initial oxidation (Jensen et al., 2005) and hence the effects of a short-term interruption in pressurized gas-flow should be outweighed by the advantages of the long periods during which flows operate.
Previous reports of HIC in P. australis showed that convective flow and static pressure increased linearly with decreasing external humidity and, while the removal of leaf sheaths from culms markedly reduced the flow rate, the removal of leaf laminae had no appreciable effect (Armstrong and Armstrong, 1990b). The lamina–leaf sheath junction has an extremely low porosity and it was concluded that it was this that prevented the laminae from contributing to, or leaking, the convective flow. The leaf sheaths contain parallel aerenchyma channels which lead into aerenchyma pockets at the nodes of the culm. These, in turn, connect with the pith cavity of the culm via radial channels of high porosity across the vascular cylinder just above the nodal diaphragm (Afreen, 1998; Armstrong et al., 1996c). The major convective flow path is described briefly in Fig. 1.
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Despite the extensive nature of this earlier work, some important aspects of the convection in P. australis still remain unexplored. Since flows, and static and dynamic pressure measurements have only been obtained for whole culms and do not focus on individual parts, they tell us little of the pressure–flow relationships or pressure gradients in particular regions of the aerial culm or leaf sheaths of P. australis. Microscopic studies of the leaf sheath revealed that it consists of narrow, longitudinally running, aerenchyma channels each of which is interrupted by a number of partitions or diaphragms (trabeculae) (Afreen, 1998). The pith cavity nodal diaphragms of rhizome and culms offer significant resistance to the ventilating pressure flows induced by HID (Armstrong et al., 1988) and the same must be true of the narrow leaf sheath aerenchyma channels and their diaphragms, and possibly also of the radial channels which connect the leaf sheath aerenchyma to the pith cavity of the culm. The Poiseuille equation (flow=
Pd/R) demonstrates that any flow requires that there should be a pressure differential, and if gas flows from all the leaf sheaths into the culm, one could expect that the presence of all these resistances would produce a series of pressure drops along each leaf sheath and along the culm itself, and a significantly higher pressure will develop towards the apex of the culm than at the base. Mathematical modelling has suggested that this should be so and that counter pressures between culms and leaf sheaths help determine flows (Beckett et al., 2001). The main objectives of this study were (i) to establish whether gradients of the type suggested do indeed occur in Phragmites culms and leaf sheaths, and if so what form and magnitude they might have, and (ii) using non-excised culms, as well as excised ones, to investigate further the potential of whole culms and leaf sheaths to generate pressures and convective flow. To this end, novel procedures were devised for pneumatically isolating and sampling non-excised culms and individual leaf sheaths, and static and dynamic pressures and flows measured in whole culms and individual leaf sheaths in relation to leaf sheath area and dead (efflux) to living (influx) culm ratios.
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Materials and methods |
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The experiments were performed in summer in the field on the banks of the River Hull, near Beverly, UK (map ref. TA 057407) using intact (non-excised) or excised leafy culms of Phragmites australis (Cav.) Trin. ex Steud. Culm height often exceeded 2 m but excised culms were sometimes shortened to vary the leaf sheath areas.
Convective flows and static pressures of excised culms in relation to leaf sheath areas
Static (no flow) pressures (the maximum pressure developed by the plant in the non-throughflow condition, i.e. when the convective flow is blocked, Ps), and convective flow rates from healthy culms, were measured in the field on cloudless August days [photosynthetically active radiation (PAR) top: c. 1500 µmol m–2 s–1; bottom: c. 400 µmol m–2 s–1; relative humidity (RH), 35–47%; temperature, 25–36 °C]. A healthy leafy culm was excised at the base and immediately connected by means of rubber tubing and two 3-way taps (Fisons, UK) to a custom-made, glass, soap-film flow-meter for measuring flows, and a portable pressure transducer (Furness Controls, Bexhill, UK) for measuring Ps (Fig. 2a). Static pressure was measured first, followed by the flow. Measurements were done as quickly as possible to minimize any effects from dehydration of the culm, but HID equilibration is rapid and readings were usually reproducible for about 5–10 min following excision. Since the porosity of the stem cortex is extremely low except at the nodes (Armstrong et al., 1996c), the flow from the base of the culm occurs chiefly via the pith cavity; similarly the static pressure is sampled from the pith cavity.
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The total length of living leaf sheath (L) was recorded and, using digital callipers (Mitutoyo Components Ltd, Kawasaki, Japan), the top diameter of the apical leaf sheath (Da) and the bottom diameter of the basal one (Db) were measured. The leaf sheath area for each culm was then calculated from the expression, 0.5L
(Da+Db) and static pressures and convective flows were plotted against corresponding leaf sheath areas.
Non-excised culms venting to the rhizome: measurement of static and dynamic pressures in relation to leaf sheath area and incidence of old, dead culms
Dynamic (with gas flow) pressures, Pd, and the corresponding static pressures, Ps, of single non-excised leafy culms of various lengths and diameters were measured in the field in the months of July and August in bright sunshine (PAR, top: c. 1410 µmol m–2 s–1 and bottom: c. 363 µmol m–2 s–1; temperature, 25–34 °C; RH, 33–55%). The culms were venting into the rhizome system and the pressures were monitored by tapping into an internodal pith cavity near the base of the culm. The procedure was as follows.
The dynamic pressure differential (Pd), in this case the pressure above atmospheric developed within the intact culm during convection into the rhizome system (Fig. 2b), was measured through a hypodermic needle inserted and sealed into the pith cavity of the third internode from the bottom. This was connected via plastic tubing and a 3-way tap to the portable pressure transducer. For the measurement of static pressures (Ps), the intact culms were subsequently flooded internally above the lowermost node by inserting a hypodermic needle and injecting water into the pith cavity. The needle was then withdrawn and the wound sealed with silicone rubber and tape. Since the stem cortex has extremely low porosities, this prevented venting via the rhizome system. The Ps was then recorded, equilibration taking only about a minute or so. Leaf sheath areas were determined as described in the previous experiment.
The measurements were carried out at two sites, one having a lower incidence of old dead culms than the other, and were plotted against leaf sheath area.
The relationship between leaf sheath area, Ps, and convective flow through the aerenchyma channels of single pneumatically isolated leaf sheaths on non-excised culms
Single pneumatically isolated leaf sheaths, 15–20 cm in length, on intact non-excised aerial culms, were used to determine Ps and convective flow rate in relation to leaf sheath area. Leaf sheaths from the lower halves of the culms were chosen. The pith cavity above the next node up from the base of the selected sheath was flooded carefully and the wound sealed as described in the previous section. Similarly, the pith cavity below the leaf sheath's nodal insertion point was flooded and resealed. Thus, in terms of ventilation, the leaf sheath was isolated from the rest of the culm (Fig. 3a).
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A hypodermic needle was now inserted and sealed into the pith cavity of the culm internode near the top of the leaf sheath to avoid damage to the leaf sheath. The needle was connected by tubing and 3-way taps to either a pressure transducer, for measuring
Ps, or to a soap-film flow-meter for measuring flows.
Dynamic pressure gradients along non-excised pneumatically isolated leafy culms; pith cavity sampling points
The pith cavity above the lowermost (basal) node of the intact culm was blocked by flooding to prevent venting to the rhizome system as mentioned earlier. Subsequently, a venting hole (an artificial outflow) was made by drilling the culm wall with a needle in the next internode up (internode 2) and venting of the culm was via this artificial bore-hole. Care was taken to avoid damage to any leaf sheath. The dynamic pressure gradient down the culm was then measured by inserting a hypodermic needle connected to the pressure transducer into the top of each internodal region avoiding the leaf sheath, and starting from internode 8 above the venting hole, namely internode 11 (Fig. 4a). After each measurement of Pd the needle was removed and the wound sealed with silicone rubber and tape. Five to six culms of similar heights (190±23 cm), under fairly uniform conditions (PAR, top: c. 1213 µmol m–2 s–1 and bottom: c. 188 µmol m–2 s–1; RH, 49±11%; temperature, 24±4 °C) were sampled in this way and dynamic pressures were plotted against internodal position.
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Dynamic pressure differences between upper and lower parts of leaf sheaths on non-excised pneumatically isolated leafy culms
Dynamic pressures in the upper and lower parts of leaf sheaths on nodes 3–12 above an artificial bore-hole (Fig. 4b) were sampled on non-excised pneumatically isolated leafy culms of similar heights (c. 2.1–2.3 m) in dry sunny conditions (PAR, top: c. 1221 µmol m–2 s–1; bottom: c. 159 µmol m–2 s–1; RH, 40±3%; temperature, 30±4 °C). The venting of gases to the rhizome was prevented by flooding the lowermost internode, and venting was via an artificial bore-hole above this, near the culm base, as described in the previous section. Access to the aerenchyma channels in the sheaths was achieved by slivering away a small portion (c. 5 mm2) of the abaxial surface of the leaf sheath, and connection to the pressure transducer was by means of a specially designed peg which clamped onto a ring of Terostat (blue tack) to create a sealed junction over the slivered portion (Fig. 5). The peg had a small hole on one side from which a narrow plastic tube emerged and was connected with the pressure transducer via a 3-way tap.
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The mean
Pd values of upper and lower parts of the sheaths were plotted against leaf sheath position on the culm.
Dynamic pressure gradients along the aerenchyma channels of individual pneumatically isolated leaf sheaths on non-excised pneumatically isolated leafy culms
For more detailed measurement of dynamic pressure gradients along leaf sheaths, leaf sheaths similar to those used for the previous experiment were selected and the upper and lower internodal regions were flooded and an artificial vent created as described earlier; in this case, however, the bore-hole vented directly to the atmosphere (Fig. 3b). The Pd was determined at intervals along sheaths (Fig. 3b) by slivering away the leaf sheath and attaching pegs (Fig. 5) as described earlier in the previous section.
It should be noted that since HID is very much influenced by atmospheric conditions, and the data were collected under field conditions where RH, PAR, and temperature are constantly varying, considerable scatter of data points might be expected. This will be in addition to the potential for variation due to structural and physiological differences between culms.
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Results and discussion |
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Convective flows and static pressures of excised culms in relation to leaf sheath areas
The static (no flow) pressures (
Ps) did not vary greatly with increasing leaf sheath area (Fig. 6a) and this accords with the mathematical modelling of the HID and HIC processes (Armstrong et al., 1996a, b). The explanation lies in the dependence of Ps upon the degree of stomatal opening, RH, PAR, and temperature rather than leaf sheath area; one other similar result has been reported elsewhere (Armstrong et al., 1996c).
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Earlier studies showed that stomata occur over the full length of the leaf sheath with frequencies ranging from 270–400 mm–2 (Armstrong, 1992). In the present study the potential for developing convective flows increased with increasing leaf sheath area (Fig. 6b) and hence with the increasing numbers of stomata involved in the HID. This strongly suggests that most of the leaf sheath area on a culm must be implicated in generating the flows. The potential consequences for the plant of increasing flow rates are improved ability to support rhizome growth deeper into flooded sediments (Vretare and Weisner, 2000) and improved potential for ROL and rhizosphere oxidation. Again it should be noted that it is only leaf sheaths that are involved in generating the convections since the porosity of the sheath–leaf lamina junction is too low to support significant pressure flow.
In this experiment only the living portions of the culm were taken into consideration. The reason why the senesced portions were not included is because although stomata and aerenchyma channels do exist in these portions, the aerenchyma channels of senesced leaf sheaths are usually blocked by callus in the basal (nodal) region; also, it is only the living leaf sheaths that can maintain the humidity gradients necessary for HIC.
Non-excised culms venting to the rhizome: measurement of static and dynamic pressures in relation to leaf sheath area and incidence of old, dead culms
As with the excised culm the results indicated that the level of Ps achieved was relatively independent of leaf sheath area (Fig. 7a) and it is almost certainly open to the same explanation discussed in the previous section. So far as the authors are aware this is the first time that such a relationship has been demonstrated for culms still connected to the rhizome system. A possible explanation for the slightly positive correlation seen here and in Fig. 6a is that tall culms, which have the largest leaf sheath areas, may have had their apical regions in conditions of comparatively lower RH and greater PAR than shorter culms. Also, the boundary layer resistance around the sheaths is likely to be narrower higher in the canopy where wind speed is greatest, and this also will contribute to steeper humidity gradients across the leaf sheath stomata, thus creating higher internal pressures. The new:old culm ratio also had no effect on the level of Ps (Fig. 7a).
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The dynamic pressure differentials (
Pd) (Fig. 7b) revealed that mature, green healthy culms having broken or old dead culms as neighbours at an old:new culm ratio of 1:12 gave dynamic pressures of 100–300 Pa. In contrast, healthy culms with fewer dead, persistent culms as neighbours (old:new culm ratio <1:25) exhibited greater values for Pd (400–600 Pa). Both sets of Pd values are relatively high, but the result does indicate that increasing numbers of old, dead culms will provide a venting (efflux) pathway of lower resistance. These Pd and Ps data for non-excised culms, together with the flow values from the excised culms (Fig. 6b) can be used to predict the probable flows to the rhizome from the non-excised culms. It has been shown elsewhere (Beckett et al., 2001) that the expression [1–(Pd/Ps)], the ventilating coefficient, provides a means of predicting the deliverable gas flows to the underground parts. A ventilating coefficient approaching 1.0 would indicate that almost the full potential for flow from a culm was being realized; a coefficient of zero (i.e. where Pd/Ps=1) would correspond to there being no flow. The results presented here reveal ventilating coefficient means (±SE) of 0.71±0.02 for the 1:12 old:new culm ratio and 0.31±0.04 for the 1:25 ratio. In other words 71% of the potential flow from the culm would be entering the rhizome system at the higher ratio and only 31% at the lower one. For the tallest culms in this study this would translate into flows of c. 100–117 nm3 s–1 (6–7 cm3 min–1) and 43–48 nm3 s–1 (2.6–3.1 cm3 min–1), respectively. High dynamic pressures and low ventilating coefficients are characteristic of die-back sites (Beckett et al., 2001) or sites that have been mown (Rolletschek et al., 1999). Although mowing will initially raise ventilating coefficients by removing some efflux resistance, if this is followed by a flooding of the stubble and wetting of exposed nodal diaphragms, callusing will be induced, resulting in a blocking of the venting pathway (Armstrong et al., 1996d). The study site had been heavily trampled in the preceding winter during river-bank maintenance work and it is possible that, in ventilation terms, because of unseen callusing, the effective efflux to influx culm ratio might have been even lower than recorded.
The plots show a small positive correlation between Pd and leaf sheath area (Fig. 7b); the explanation for this could be 2-fold: (i) culms with larger leaf sheath areas and hence potentially greater flow potential will induce higher pressures at their bases and (ii) the reasons given in the previous section in relation to Ps.
The relationship between leaf sheath area, Ps and convective flow through the aerenchyma channels of single pneumatically isolated leaf sheaths on non-excised culms
The results indicated a slight positive correlation between Ps and leaf sheath area (Fig. 8a). Although this accords with the previous findings (Fig. 7a), the values of Ps are somewhat lower. The explanation for this may lie in the positioning of the sheaths examined: choice was influenced by the ease with which the sheaths could be sampled and this meant assaying only sheaths at 1–1.5 m from the ground where humidity levels are higher, and wind speed and light flux lower than nearer the culm apices.
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In contrast, the potential for HIC strongly increased with leaf sheath area (Fig. 8b): the flow rate was highest (33 nm3 s–1) for the leaf sheath area of c. 30 cm2, and lowest (6.7 nm3 s–1) when the leaf sheath area was only c. 6 cm2. Flows from single leaf sheaths have never before been reported but, as might be expected, the form of the relationship between flows and leaf sheath area is similar to those observed for the whole excised culms (Fig. 6b). The positive correlation between flow and sheath area can again be explained in terms of the greater the leaf sheath area the greater are the numbers of stomata for the entrance of atmospheric gases during HIC. Despite their lower overall positions in the canopy, however, the flow rate per unit area of leaf sheath was greater for the single sheaths compared with those observed for excised culms (Fig. 6b). The most likely reasons for this are that (i) in the case of the whole culms the flows have to traverse the nodal diaphragms, which lie as a series of resistances in the flow path and (ii) the sheaths also have to overcome the counter-pressures generated by one another, and this lowers the overall flow rates (Beckett et al., 2001).
Dynamic pressure gradients along non-excised pneumatically isolated leafy culms; pith cavity sampling points
Moving up the culm, dynamic pressures increased with increasing distance from the outflow vent: Pd increased from c. 5 Pa at internode 4 (the first above the outflow) to c. 26 Pa at internode 11 (the eighth above the outflow) (Fig. 9). This is as anticipated since the greater the distance from the venting point, the higher will be the resistance, and a higher pressure must develop to deliver the flow. This result is in keeping with mathematical modelling predictions (Beckett et al., 2001) and, although it has been shown that pressure drops from the leaf periphery towards the petiole in the influx leaves of water lilies (Schröder et al., 1986), the authors believe that this is the first time that pressure gradients have been directly measured in an emergent macrophyte.
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The shape of the plot in Fig. 9 is also of some interest. Given the variation observed and the approximately linear relationship shown, it might seem reasonable to apply a linear regression to the data. However, a better fit is obtained by a second order polynomial, and there are good justifications for supposing that the data will follow a curvilinear relationship (Beckett et al., 2001). Such an effect is likely to be obtained wherever similar lateral in-flows occur along a set of regularly spaced resistances in series. The latter are represented here by the nodal diaphragm resistances that range in value from 20 to 80 MPa s m–3 depending upon culm diameter (Afreen, 1998). In this context, however, it may be that lower relative humidities and higher wind speeds and insolation towards the top of the canopy could contribute to the development of potentially higher static and dynamic pressures in the upper parts of the culms. This could reduce the expression of the curvilinear effect. However, the curve would be expected to flatten out in the topmost internodes, but no measurements of this were possible; access to the internodes could not be achieved without collateral damage to the subtending leaf sheaths.
Finally, the existence of a pressure gradient along the culm confirmed that gases are transported into the underground parts, perhaps from all parts of the culm, but certainly up to and beyond node 11.
Dynamic pressure differences between upper and lower parts of leaf sheaths on non-excised pneumatically isolated leafy culms
Obvious differences in dynamic pressures between the upper and lower parts of leaf sheaths along culms were noted. When plotted against position on the culm, the pressures followed curvilinear gradients (Fig. 10), similar in form to those observed for the intact culms themselves (Fig. 9). Again this is the expected outcome wherever similar lateral in-flows occur into channels interrupted by a set of regularly spaced resistances in series (in this case the sheath aerenchyma diaphragms), and where the outflow is at one end of the system. However, the mean values were higher overall than in Fig. 9; this may have been due to a variety of factors such as smaller venting holes, lower relative humidity, higher ambient temperatures and wind speeds, and, to some extent the resistance between the lower sampling point on each sheath and the culm pith cavity from where the Fig. 9 data points were collected.
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It is interesting that the curvilinear relationship discussed in the previous section is even more apparent and this would accord with the longer length of culm sampled. It is also interesting that even leaf sheaths as high as node 13 still appeared to contribute to the overall convective gas flow, although the flattening of the gradients suggested that their contributions were diminished compared with those lower down the culm.
Dynamic pressure gradients along the aerenchyma channels of individual pneumatically isolated leaf sheaths on non-excised pneumatically isolated leafy culms
In each leaf sheath tested, dynamic pressures increased with distance up the sheath; the individual gradients for five leaf sheaths are shown in Fig. 11a–e. The gradients varied in shape: three had a convex shape, the other two were concave, but in each the slope was still positive in the upper parts. Thus, the dynamic pressure was highest in the upper part of the leaf sheath and lowest at the bottom close to where it connects with the culm. This is in keeping with the importance of higher pressure development to drive the flows as distance, and resistance, from the venting point increases. Convective flow resistances longitudinally through the leaf sheaths range from approximately 1000 to 2500 MPa s m–3 cm–1 (Afreen, 1998). The results indicate that all points along the leaf sheath potentially can contribute convective flow to the culm. Further, if the gradients are extrapolated to estimate the pressures at the bottom of each sheath it will be noticed that the values would be close to zero, and this is indicative of a relatively low resistance for the radial channels through the culm vascular cylinder that connect the leaf sheath aerenchyma with the pith cavity of the culm. Only convex profiles have been predicted by mathematical modelling (Beckett et al., 2001) and there can only be speculation about the reason for the two concave profiles. It is possible that they reflect some unnoticed senescence or ‘leakiness’ near the bottom of these sheaths.
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Final comments |
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HIC is an important mechanism for augmenting oxygen transport to the below-ground system of P. australis; it is usually much more effective than passive diffusion for supplying oxygen (Armstrong and Armstrong, 1990b) and removing respiratory CO2 and sediment-generated CO2 and methane (Brix et al., 1996: Chanton et al., 2002). The present study has confirmed experimentally what has only previously been mathematically demonstrated, namely, that pressure gradients in the culms of Phragmites should extend for the full length of the living culm. In addition, pressures in the sheaths increased with increasing distance up the culm, while pressure differences between upper and lower parts of the sheaths were maintained. It is deduced from this and from the increased flows with increasing leaf sheath area that most, if not all, leaf sheaths contribute to the convective flow. Furthermore, since gradients within individual sheaths appear to extend over the full length of the sheath, it is also concluded that the whole leaf sheath length is involved in the process. Only leaf sheaths that were free from sleeving by other sheaths were tested during this study; where partial sleeving occurs, as in immature culms and near the tips of mature culms, only the exposed portions of sheath will be involved in pressure generation and the sleeved portions might act as minor efflux sites.
Pressure gradients in culms and sheaths are the consequences of the pressure-generating mechanism and the resistances to flow through the system. The primary resistances in the culm are the nodal pith diaphragms; in the leaf sheaths they are the trabeculae partitioning and supporting the aerenchyma channels. The greater the distance from the venting point, the higher will be the resistance, and the development of a higher pressure will be necessary to deliver a flow. Upper leaf sheaths will only contribute significantly to flow if the stomatal aperture and density, coupled with the efficiency of internal humidification, are such as to provide the necessary pressurization. Clearly, in the present study, this was so, but the convex shape of the curves for culm and leaf sheath pressurization versus nodal position (Fig. 10) might indicate that contributions per sheath are diminishing with distance from the base; the same might apply to contributions along individual leaf sheaths (Fig. 11a, b, d). Both have been predicted by mathematical modelling, and the extent to which nodal diaphragms and leaf sheath diaphragms resistances affect pressure flows will be addressed in a subsequent paper.
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Abbreviations |
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, convective flow
pressure-driven flow; HIC, humidity-induced convection; HID, humidity-induced diffusion; Pd, dynamic (with flow) pressure; Ps, static (no flow) pressure; Pa, Pascal; R, resistance; ROL, radial oxygen loss. |
References |
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