Journal of Experimental Botany, Vol. 52, No. 360, pp. 1465-1472,
July 1, 2001
© 2001 Oxford University Press
Original Papers |
Diffusion pathway for oxygen into highly thermogenic florets of the arum lily Philodendron selloum
Department of Environmental Biology, University of Adelaide, Adelaide, SA 5005, Australia
Received 8 November 2000; Accepted 15 February 2001
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Abstract |
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Thermogenic inflorescences of some arum lilies have the highest rates of respiration known among plants. Peak rates of oxygen consumption in the sterile male florets of Philodendron selloum Koch exceed 0.3 µmol s-1 g-1 when the inflorescence warms to 38 °C. This study describes the morphology of the oxygen diffusion pathway between the atmosphere and the parenchymal cells of the florets. Dimensions of the florets, stomata, interstitial gas network, and cells provide data for diffusion models of the PO2 profiles at each level of the ‘oxygen cascade’. The lowest calculated PO2 of 4.7 kPa (35 mmHg) at the axis of the thickest part of the floret indicates that maximum respiration does not reach the point of diffusion-limitation, confirming earlier physiological measurements of the dependence of oxygen consumption rate on environmental PO2. Adequate aeration of all cells is achieved by appropriate floret size, despite a stomatal density less than 5%, and interstitial gas fraction less than 2%, of values commonly found in leaves.
Key words: Gas diffusion, flower, stomata, thermogenesis, respiration, Araceae.
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Introduction |
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Rates of oxygen consumption (M ·O2) by the inflorescences of arum lilies increase greatly during thermogenesis. Depending on the species and ambient temperature, mass-specific rates may reach 0.1–0.9 µmol s-1 g-1, which is equivalent to rates in the most active animals (Nagy et al., 1972
; Lance, 1972; Knutson, 1974; Seymour et al., 1983; Seymour, 1997; Seymour and Blaylock, 1999; Seymour and Schultze-Motel, 1999). In Philodendron selloum, about 70% of respiration occurs in a band of sterile male florets around the central spadix, between the fertile male florets at the top and the female florets at the base (Nagy et al., 1972) (Fig. 1A). At peak thermogenesis, these florets raise their temperature to about 40 °C and consume oxygen at rates over 0.3 µmol s-1 g-1 (Nagy et al., 1972; Seymour et al., 1983; Seymour, 1999).
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Oxygen presumably enters the florets by diffusion, and the rates are high enough to raise interest in the nature of the diffusion pathway and the question of diffusion-limitation of respiration. Previous experiments on P. selloum, involving respirometry in closed chambers with declining oxygen partial pressure (PO2), indicated that M ·O2 was not limited under atmospheric PO2 of about 20 kPa, but it began to decrease below 80% of maximum when PO2 decreased to about 10–15 kPa (Seymour et al., 1984
). These critical PO2 values increased at higher maximum M ·O2, as would be expected in a potentially diffusion-limited gas-transport system. With greatly simplified assumptions of floret anatomy, which considered them to be cylindrical and ignored diffusion resistances in the inter-floret gas spaces, the stomata and the tortuous intra-floret spaces, it was estimated that the fractional interstitial gas space within the florets was effectively 0.00018. This physiological estimate was one to two orders of magnitude smaller than the morphological volume of gas spaces in other bulky storage tissues of plants (Woolley, 1962), so its accuracy was doubtful. Consequently, the present morphological study was designed to describe the oxygen diffusion pathway in P. selloum, taking account of five levels in the ‘oxygen cascade’: atmosphere, inter-floret gas space, stomatal openings, intra-floret ( parenchymal) gas network, and the contents of cells. Direct anatomical measurements from complete florets and histological sections were coupled with gravimetric determinations of internal gas volumes to arrive at oxygen profiles of the diffusion pathway and to assess the question of diffusion-limitation.
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Materials and methods |
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All inflorescences were harvested from 17 plants on the University of Adelaide campus on the first day of heating, when the spathe had opened in the afternoon. This is ‘day 2’ of the flowering sequence, when thermogenesis is maximal, the female florets are receptive, but the fertile male florets have not yet released pollen (Seymour et al., 1983
; Seymour, 1999).
Gross floret morphology
Sterile male florets were cut from the top, middle and bottom of their band around eight spadices (Fig. 1A
, B, C). The total length (Ltot) and diameters at the tip (D1) and base (D2) were measured at three locations around the circumference of each floret. Measurements were made under a dissecting microscope with a machinist's micrometer, accurate to 0.01 mm. Surface area and volume of individual florets were calculated with appropriate geometric mensuration formulae for simple geometric solids. The florets were tapered, with tips that were only slightly domed, so they were best represented by frustra of right cones. Because it was necessary to model diffusion paths perpendicular to the surface of the floret, however, they were assumed to consist of three independent parts: two cylindrical segments of equal length and a hemisphere on the tip (see Fig. 3). The radii were ri=(3D2+D1)/8 for the inner segment, ro=(3D1+D2)/8 for the outer segment, and rt=D1/2 for the tip. Cylinder length was L=(Ltot-rt)/2. This three-segment model overestimated surface area by 4%, and underestimated volume by 1%, compared to a model of a frustrum of a right cone, differences that were considered negligible. Three sets of measurements were made on each of four florets from each of the three locations on the spadix. Thus each inflorescence is represented by 36 sets of measurements.
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Stomatal density
Florets from the three sections of the sterile male band were cut from nine spadices and kept in closed vials at room temperature for a few days after collection. This treatment caused the stomata to show up as individual brown spots in a creamy field of cuticle cells which facilitated counting (Fig. 1D). Each floret was cut with a razor longitudinally into three or four sections so that the entire surface could be clearly observed in a dissecting microscope, and the number of stomata was counted without confusion. Stoma numbers on each section were totalled for each floret, and the mean from 7–34 florets from each spadix was considered a single sample.
Stomatal and parenchymal morphology
Whole florets from 15 inflorescences were cut into three horizontal sections, fixed in 2.5% glutaraldehyde, dehydrated in a series of alcohol/water mixtures and then embedded in TAAB resin. To measure stomatal pore area, tangential serial sections of the cuticle were cut 1 µm thick with a Reichert OMU3 ultramicrotome and examined with light microscopy at 400x. The outline of the stomatal opening in each section was traced on heavy paper using a camera lucida, and the dimensions measured. The areas of the openings were determined by cutting the openings out and weighing them to 0.1 mg on a Mettler AE163 balance. The method was calibrated by weighing a square piece of paper traced from a precision 100 µm2 microscope scale. Pore area was measured on each of approximately 20 serial tangential sections from 31 stomata to arrive at the pore profile from the outside to inside surface of the cuticle. Pore depth was independently measured from radial sections of 68 stomata (Fig. 1E). The morphology of the interstitial gas spaces, and the dimensions of the largest sectioned cells, were similarly determined by tracing from both cross-sections and tangential sections. Transmission electron microscopic examination was also carried out on a few sections of parenchymal tissue (Fig. 1F).
Fractional interstitial gas space
Internal gas space of sterile male florets was measured by Archimedes’ principle. Florets were measured immediately after harvesting. A small section of about 10–60 sterile male florets (105–570 mg) was removed from the stalk, retaining a thin, transparent layer of stalk tissue to hold them together. The group was immediately weighed to 0.01 mg and then placed under about 100 ml of room-temperature water containing a drop of detergent to lower the surface tension. Bubbles between the florets were manually removed under a dissecting microscope, and then the sample was weighed underwater in a density measurement accessory for the balance. The weight of aerated samples never stabilized underwater, indicating that gas was decreasing slowly during the measurements, presumably because of respiratory gas exchange (see below). For uniformity, therefore, the weight was read after a few seconds, exactly when the instability indicator of the balance was extinguished. In all, the aerated floret was under water for about 30 s. The florets were then placed in a greased, 20 ml glass syringe with about 5 ml of detergent water. After expelling air from the syringe and closing it, the gas inside the florets was removed by pulling the plunger back and creating low pressure. It was estimated from the change in bubble size and continued production of water vapour bubbles during degassing, that the pressure decreased below 0.1 atmosphere. The bubbles that emerged from the florets were expelled from the syringe. After the first degassing, the florets sank, and the process was repeated several times to ensure that practically all gas in the florets was replaced by water. The radius of intercellular pores (c. 2 µm) would create a capillary tension of about 0.7 atm without detergent and 0.3 atm with it, so the invading water was not impeded by menisci. Then the florets were removed from the syringe, dipped in detergent water, freed from all bubbles, and weighed again underwater.
This technique underestimated the actual gas content in the florets because of respiration during the period underwater when the floret was cleared of external bubbles and weighed. The error is between 3% and 18%, as estimated from rates of floret oxygen consumption and CO2 production (Seymour et al., 1983, 1984). With a respiratory quotient of 0.83 and a rate of oxygen consumption at 20 °C of about 0.124 µmol s-1 g-1, the 8.27 mg floret would take up about 1.0 nmol O2 s-1 and produce 0.83 nmol CO2 s-1. With a fractional gas space of 0.0079 and a floret volume of 7.7 mm3 (Table 1 ), the total gas space in a floret is 61 nl. Assuming a mean PO2 of 18 kPa in the gas space, the volume of oxygen in a single floret becomes 10.8 nl. This amount of oxygen would be consumed in less than 1 s, so the 
30 s period underwater would have exhausted the oxygen and replaced it with 9.0 nl CO2. The immediate change in gas volume is 1.8 nl, or 3% of the total. Continued weight gain underwater may represent CO2 dissolving in the water, and if all of the CO2 were dissolved, the total gas lost would be 18%. It is not possible to evaluate the error with greater precision, because no record was made of the rate of weight increase. Therefore no correction has been made.
The fractional gas content of the florets (Fg) was calculated according to the equation: Fg=(B-C)/(A-B), where A is the weight of the florets in air; B is the weight of the aerated florets in water, and C is the weight of degassed florets in water. Three measurements were averaged from each of 12 spadices.
Statistics
Statistics are means and 95% confidence intervals. Comparisons involve ANOVAS or Student's t-tests, on arcsin transformed data in the case of percentages.
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Results |
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Floret morphology
Sterile male florets were about 7.30 mm in length and tapered from about 0.78 mm at the base to 1.49 mm near the top (Table 1
). Within the band of sterile male florets, the length increased slightly from about 6.41 mm at the top, near the fertile males, to 8.44 mm at the bottom, near the females, but the mean length (7.30 mm) was used to simplify further analysis. The florets touched each other at their tips, creating flattened sides and triangular openings between them (Fig. 1B). The tapering florets did not broadly touch below their tips and were surrounded by a continuous inter-floret gas space (Fig. 1C).
Stomata
The distribution of stomata on the florets appeared fairly uniform (Fig. 1D), so no statistical tests were performed. The average number per floret was 168. With a floret surface area of 26.8 mm2 (Table 1), the stomata were about 0.4 mm apart and the density was 6.28 per mm2. Pore area and depth were measured in stomata from three segments of the florets (Table 1). Mean pore area was significantly larger at the tip than at the outer or inner segments (ANOVA F15,2=4.7, P=0.03), but mean depth was slightly smaller at the tip than either segment (ANOVA F67,2=50, P<0.001). Pore areas were fairly uniform throughout the depth of tip stomata, but tended to constrict in the middle of inner and outer segment stomata (Figs 1E, 2).
Internal gas spaces
Fractional gas volume, determined by Archimedes' principle, averaged 0.0079, so the total floret gas space was calculated to be 0.061 mm3 (Table 1). This space comprised the atria beneath the stomata and a network of 4 µm diameter pores between the 33 µm diameter parenchyma cells (Fig. 1E, F). Atrial volume was estimated by measuring its cross-sectional area and converting it to an effective radius, assuming that the area was circular. The volume was assumed to be that of a sphere of the same radius. Thus the total atrial volume was estimated to be 3.4% of the total gas space in the floret (Table 1).
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Discussion |
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The point of this study is to assess the barriers to diffusion along the oxygen cascade and to determine whether the respiration of some cells is limited by diffusion. To model oxygen flux, it is assumed that it diffuses in turn through the inter-floret gas spaces, stomata, interstitial gas network and, finally, into the parenchyma cells. The mass-specific rate of oxygen consumption by sterile male florets during peak thermogenesis is about 0.31 µmol s-1 g-1 (25 ml h-1 g-1) (Nagy et al., 1972
; Seymour et al., 1983). It is assumed that the oxygen is consumed equally throughout the floret tissue, because thin sections showed a homogeneous distribution of similar parenchyma cells containing mitochondria.
Diffusion into the inter-floret gas space
The sterile male florets are tapered and touch each other at their distal ends, creating an air-space between them (Fig. 1C). The first step in the oxygen cascade is the diffusion from the atmosphere into this space. Gas samples (10 mm3) taken from this space revealed reciprocal changes in PO2 and PCO2 during episodes of heating that lasted about 2 h (Seymour et al., 1984). The deviation in gas pressures was directly related to the rate of thermogenesis, and the minimum PO2 was 17 kPa during peak heating.
It is of interest to assess the barrier to diffusion between the atmosphere and the inter-floret space to help explain the PO2 difference. The top of each floret is a hexagonal surface, surrounded by six small pores occurring at the intersections between three adjacent florets. (Figure 1A and B do not represent the appearance during maximal heating, because they show inflorescences that had completed flowering when larger gaps had opened between some florets.) Thus each floret is associated with the equivalent of two pores through which the oxygen diffuses. The volume of air in the inter-floret space is calculated from the total space under each hexagonal tip (9.44 mm3), minus the volume of the floret itself (Table 1). The air volume becomes 2.66 mm3 per floret, or 28% of the total space. There is a PO2 gradient in the inter-floret space, but gas samples from the space would mainly represent gas around the inner segments, because 89% of the gas is there. Therefore the PO2 of 17 kPa during peak heating is taken as the external PO2 around the inner segment (Seymour et al., 1984). It is further assumed that the outer segment is exposed to a PO2 of 18.4 kPa, half-way between the inner segment (17 kPa) and the free atmosphere (19.8 kPa) (Fig. 3). Assuming that the total oxygen uptake by a floret is 2.57x10-9 mol s-1, and the uptake by the three floral parts is proportional to their volumes (Table 1), then the tip consumes 2.85x10-10 mol s-1, and the outer and inner segments together consume 2.29x10-9 mol s-1 from the inter-floret gas space. Since the PO2 difference between the atmosphere and the inter-floret space is about 2.8 kPa, it follows from Fick's Law that the oxygen conductance of the inter-floret pores is about 8x10-10 mol s-1 kPa-1. Assuming that the length of each pore extends about 1 mm before opening into the inter-floret space, then the area of each pore would be about 0.05 mm2, equivalent to a round hole 250 µm in diameter. This diameter is about a sixth of the floret top diameter and appears reasonable.
Diffusion through the stomata
Each floret has about 168 stomata, distributed evenly over all surfaces at a density of 6.28 mm-2 (Table 1). This density is less than 5% of the average of 141 mm-2 (range=16–370 mm-2) given for the lower leaf surfaces of 27 species of plants (Meidner and Mansfield, 1968). The diffusion across Philodendron stomata is therefore calculated according to Fick's law, rather than Stefan's law. A comparison of the two models shows that a sparse stomatal distribution minimizes confluence of boundary air space between adjacent stomata, and the ratio of pore depth to radius (7.1) indicates that the boundary layer outside of an individual pore offers a small resistance to diffusion compared to the resistance of the pore itself; consequently Fick's law is the most appropriate (Rahn et al., 1987; Nobel, 1999). Counter-diffusion of water vapour and carbon dioxide are ignored, as is convection by internal pressurization, but the errors are a few percent (Leuning, 1983; Paganelli et al., 1987).
The PO2 profile along the stomatal pore is determined by calculating the PO2 drop across each of 20 tangential sections, using the equation:
 | (1) |
PO2 is the PO2 difference (kPa), M ·O2 is the total rate of oxygen uptake through all of the stomata in the floret part (mol s-1, calculated from the relative mass of the part and the total floret oxygen uptake), L is the length (m) of the diffusion path (i.e. the thickness of the sections), DO2 is the diffusivity of oxygen in air at 38 °C (2.164x10-5 m2 s-1), ßO2 is the oxygen capacitance of air (0.3867 mol m-3 kPa-1), and A is the total pore area (m2) of all of the stomata in the surface of the floret part. Because of different pore areas and depths, the total PO2 across the stomata varied between 0.9 kPa at the tip, 4.5 kPa at the outer segment, and 2.3 kPa at the inner segment (Fig. 3).
Of course stomatal conductance is variable, and it is uncertain how fixation may have altered the dimensions of the opening. However, the florets were fixed during maximal thermogenesis and they were placed individually in glutaraldehyde which would have quickly infiltrated the surface cells. That there were large, significant differences in pore area between the three parts of the floret (Table 1), suggests that fixation at least did not produce a uniform state of opening. Scanning electron micrographs of freeze-dried florets did not help answer this question, because, although the openings of the stomata were clearly visible, the area of deeper levels could not be quantified. The structure of the inflorescence, namely sequestering of most stomata in the inter-floret space, prevented indirect measurement of stomatal water vapour conductance in living florets. For the present, therefore, the morphological estimates of stomatal oxygen conductance are the only available data.
Diffusion in the interstitial air space
Once inside the stomata, the oxygen encounters the atria that distribute it to the network of tiny, tortuous interstitial gas spaces that invade the entire floret volume (Fig. 1F). Diffusion through this network is calculated according to analogous models for diffusion through porous media. Diffusion in dry soil, for example, has been shown theoretically and empirically to be proportional to fractional gas space (F) raised to the 1.5 power (Marshall, 1959). The diffusion coefficient is therefore the product of diffusivity, capacitance and corrected fractional gas space: DO2xßO2xF 1.5. The morphological gas fraction in floret parenchyma is quite small (0.0079), and when raised to the 1.5 power, the effective diffusion gas fraction becomes 0.0007. Thus the gas spaces in Philodendron florets are similar to those in potato tuber tissue which has a morphological gas fraction of 0.002–0.01 but an effective diffusion gas fraction of 0.001 (Woolley, 1962). By comparison, the morphological gas fraction in soybean nodules ranges from 0.003 to 0.03; much of this range is caused by large differences between fixed histological sections and frozen tissue (Thumfort et al., 1994). Similarly, the fraction in Philodendron florets calculated from histological sections was 0.04 (Table 1), or about five times higher than the measurements from fresh tissue. Because of this, the measurements from fresh tissue are accepted.
Diffusion into the interstitial gas network is modelled separately for the hemispherical tip and the outer and inner cylindrical segments. In all cases, diffusion is radial. For the hemisphere, the PO2 at a given radius (PO2(r)) is related to the PO2 at the surface (PO2(O)), the surface radius (ro), and the mass-specific oxygen uptake rate (M ·O2, taken here as 0.31 µmol s-1 g-1) according to the equation (Hill, 1929):
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For the outer and inner cylinders, the equation is:
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These models take into account the uptake of oxygen by cells along the diffusion pathway. According to the models, the PO2 distribution in the parenchyma is curved, reaching the lowest point at the centre (Fig. 3). During maximal respiration rates in air, the lowest gas-space PO2 is 8.7 kPa in the centre of the outer segment. The models are likely to underestimate the PO2 gradient slightly, because diffusion is assumed to be driven by a uniform PO2 under the entire surface of the floret. In fact, oxygen enters the floret through stomata that average 400 µm apart (Table 1), and some diffusion is tangential, rather than completely radial. The atria help distribute oxygen to the interstitial gas network, but their radii (14 µm) seem insignificant in relation to the distance between stomata.
Diffusion into parenchyma cells
Oxygen diffusion into parenchyma cells originates from the interstitial gas spaces that contact about 12% of the cell surface. Therefore it is invalid to use a spherical model that assumes a uniform surface PO2. To obtain the PO2 profile in individual parenchyma cells, therefore, a simplified cuboidal diffusion model is used (Thumfort et al., 1994). This model assumes that the gas spaces form a lattice around cuboidal cells and oxygen diffuses inward from the edges of each cube where the contact surface area is 12.8% of the total cell surface. The geometry of the model is modified as appropriate for Philodendron parenchyma cells with radii of 16.5 µm (Table 1). Eleven layers of known surface area (A) and thickness (L) are established, each of which consists of a volume of cell contents equidistant from the gas spaces. Oxygen diffuses through each layer in succession at a rate equal to the total oxygen uptake of that layer and all layers below it. The rate of oxygen uptake (M ·O2) of each layer is calculated from the volume-specific rate of 0.29 mol m-3 s-1 at 38 °C, and it is assumed to be independent of PO2 (Seymour et al., 1983, 1984). The value of diffusivity (DO2) in the cytosol of legume nodule cells is taken as 7.5x10-10 m2 s-1, presumably at 20 °C (Denison, 1992). For Philodendron, this is adjusted to 1.12x10-9 m2 s-1 at 38 °C with values for the temperature effect on DO2 in water (Himmelblau, 1964). Oxygen capacitance (ßO2) of the cytosol is assumed to be 1.042x10-2 mol m-3 kPa-1 at 38 °C (Dejours, 1981). Thus the PO2 difference across each layer is calculated from equation (1), and the PO2 profile is determined from successive values of PO2 along the diffusion path. According to this model, the PO2 at the centre of a parenchyma cell would be 4.0 kPa lower than at its surface.
The threshold of diffusion limitation
According to the models, the lowest PO2 occurs at the centre of the outer segment where it is estimated to be about 4.7 kPa, that is 15.1 kPa below the free atmosphere (Fig. 3). Therefore the ambient PO2 could drop to 15.1 kPa before anoxia would occur in the centre of the floret. Previous work shows that respiration of isolated Philodendron florets begins to decrease below 80% of the maximum rate (0.3 µmol s-1 g-1) at an ambient PO2 of 14.5 kPa (Seymour et al., 1984). The concordance between the earlier physiological study and present morphometric investigation is reassuring, given the number of assumptions of the latter.
In view of the prodigious rate of oxygen consumption by Philodendron florets, it was initially surprising to find that the density of stomata was less than 5%, and the interstitial gas fraction was less than 2%, of values commonly found in leaves (Meidner and Mansfield, 1968; Nobel, 1999). However, the PO2 difference between the atmosphere and the respiring floret cells is more than 200 times higher than the differences in PCO2 normally experienced by leaves. Consequently, the diffusion conductance in the florets may be much lower than in leaves without limiting respiration. It is interesting that conductance in florets is as low as it is—near the threshold of diffusion-limitation. It is tempting to speculate that this is a result of natural selection acting to reduce the rate of evaporative water loss from the inflorescence. In fact, evaporation is so low, that a 65 g spadix loses only 0.8% of its mass per hour while maintaining a temperature of 42.3 °C in dry air at 26.8 °C, a water vapour deficit of 8.3 kPa (Seymour et al., 1983). Under these conditions, the rate of evaporative heat loss from the spadix is less than 8% of the rate of metabolic heat production. Not only is Philodendron selloum a strongly thermogenic inflorescence, it is also thermoregulatory. The inflorescence maintains two levels of high stable temperatures that are practically independent of ambient temperature changes during about 22 h of the protogynous flowering sequence (Nagy et al., 1972; Seymour, 1999). It has been proposed that the provision of high floral temperature is a direct energy reward to insects that visit during this period of female receptivity (Seymour, 1997). Because evaporation is a powerful mechanism of heat dissipation, low rates of evaporation would conserve energy while the inflorescence maintains the high temperatures.
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Symbols, units and constants |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionSymbols, units and constantsReferences |
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PO2=oxygen partial pressure (kPa; 1 kPa=7.52 mmHg)
M ·O2=rate of oxygen consumption (mol g-1 s-1; 0.31 maximally at 38 °C) (Nagy et al., 1972; Seymour et al., 1983; Seymour, 1999)
DO2=oxygen diffusivity (m2 s-1. Air: 2.16x10-5. Cytosol: 1.12x10-9 at 38 °C) (Himmelblau, 1964; Denison, 1992)
ßO2=oxygen capacitance (mol m-3 kPa-1. Air: 0.387. Water: 1.042x10-2 at 38 °C) (Dejours, 1981)
Fg=fractional gas volume (dimensionless) r=radius (m) D=diameter (m) L=length (m) A=area (m2)
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Acknowledgments |
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This study was supported by the Australian Research Council and the University of Adelaide. I appreciate the technical assistance of Helen Vanderwoude, Heidi Walters, Sandi Poland, Phil Kempster, James Byles, Kate Rodda, and Chris Miller. The constructive comments and advice from three anonymous referees and the editors are gratefully received.
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Notes |
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1 Fax: +61 8 8303 4364. E-mail: roger.seymour{at}adelaide.edu.au
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References |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionSymbols, units and constantsReferences |
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