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- Materials and Methods
Internal pressurization and convective gas flow in aerenchyma are now well established as important for aeration adaptation for many emergent and floating-leaved aquatic plants growing in waterlogged, anoxic soils (Brix et al., 1992; Colmer, 2003; Armstrong & Armstrong, 2009). This mechanism achieves much greater rates of internal oxygen transport than does simple diffusion, the sole gas transport mechanism for most wetland plants, increasing internal oxygen concentrations in underground rhizomes, as well as root oxygen release and rhizosphere oxidation (Armstrong et al., 1996b; Brix et al., 1996). This allows greater rhizome and root growth, especially in strongly reducing soils, and permits growth in deeper water (Strand, 2002; Sorrell & Hawes, 2010).
Crucial to the ability of convective flow to improve plant aeration are the environmental factors governing pressurization, the driving force behind the flow. Pressurization is a purely physical process based predominantly on differences in water vapor pressure between the aerenchyma and external atmosphere. Much of the early literature on shoot pressurization focused on distinguishing between the contributions of humidity and temperature in generating pressures, ultimately confirming humidity as the dominant pressurizing factor (Armstrong et al., 1992; Bendix et al., 1994). This raises questions about the ability of plants to generate internal pressures and flows in environments in which atmospheric humidity may be high, particularly the tropics. Almost all previous studies have been carried out on species from temperate latitudes under temperate climatic conditions (Raven, 2009). Tropical environments not only have higher atmospheric humidity during some parts of the year, but also have consistently high temperatures, increasing the oxygen demand of the rhizome and root respiration. An efficient oxygen supply to below-ground tissues is therefore likely to be even more important in tropical than temperate wetlands, yet atmospheric conditions may not be conducive for convective through-flows, the most efficient oxygen transport mechanism identified so far in plants. The absence of data from the tropics is therefore a major gap in our understanding of the importance of convective flows for wetland plant aeration.
In addition to the environmental conditions necessary for pressurization, internal pressures will only be developed in plants with the appropriate morphological and physiological adaptations for generating pressures. The fact that the large majority of emergent wetland plants do not pressurize, despite their almost ubiquitous possession of porous aerenchyma, is a result of the need for restricted stomatal apertures and narrow, tortuous airspaces between the substomatal cavity and cortical lacunae in order to sustain a pressure differential between plant and atmosphere that can be vented through the rhizome (Dacey, 1980; Armstrong & Armstrong, 1990; Armstrong et al., 1996a,b; Steinberg, 1996). Whether there are tropical emergent species with these features that are capable of generating pressures when atmospheric conditions allow is largely unknown. Furthermore, even when pressures are generated, the flows that they support are a function of the gas flow resistance through the aerenchyma pathway, which is often high, given that resistances to fluid flow are a fourth-power function of the airspace radius (Sorrell et al., 1997). The ability of pressures to generate significant flows varies widely in temperate species, and differences in their flow development are related to species’ distribution in nature (Strand, 2002; Sorrell & Hawes, 2010), but there are currently no field data available to assess whether this might also apply in tropical environments.
In this article, we therefore present the first ever measurements of internal pressurization and convective gas flow from a range of tropical wetland plants under field conditions. The first objective of this study was to assess whether internal pressurization is widespread as an aeration mechanism for tropical wetland plants. We studied 20 common wetland plants from flooded habitats in South-East Asia, where the climate is characterized as tropical with a dry season from December to May and a rainy season for the rest of the year. A second aim was to investigate the ability of convection to improve below-ground aeration for three emergent species with different gas flow rates.
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This study shows that pressurization and convective gas flow are widespread mechanisms for aerating the below-ground parts of wetland plants in tropical climates. Previous claims of pressurized gas transport in tropical trees (Graffmann et al., 2008) are unreliable, as they are based on indirect oxygen exchange and tracer gas methods that ignore the non-through-flow nature of the gas pathway in roots, leading to the false identification of pressurized gas flow in trees (Armstrong & Armstrong, 2005). Our measurements were restricted for logistic reasons to the dry season when atmospheric temperature and humidity are similar to those of temperate climates, and therefore optimal for pressurization and convective flow. Although conditions will be less favorable for pressurization in the wet season, the ability to pressurize for much of the year may be ecologically significant. Even in the wet season, there are likely to be periods when flow is possible, as the rain is usually limited to brief showers during the day, and humidity can fluctuate between 60% and 95% in a short time (H. Brix et al., unpublished). Nine of the 20 species were able to build up a substantial static pressure of > 50 Pa and eight species had convective flow rates higher than 1 ml min−1. However, even low flow rates can greatly increase the O2 supply into rhizomes compared with that available to plants lacking convection, which rely solely on diffusion for O2 transport (Armstrong & Armstrong, 1990). Convective flow rates measured from cut culms are potential flow rates rather than the actual flow rates that occur from influx culms to below-ground plant parts. Some species have very high resistances to gas flow in the junction between culm and rhizome, which means that high flow rates from cut culms might not correspond to high flow rates in intact plants (Brix et al., 1992). However, species which are able to pressurize are likely to be able to produce some convective flow, although the rate depends on the resistance, and species with nondetectable flow rates from cut culms definitely cannot produce any convective through-flow ventilation in intact plants. The highest flow rates were achieved in N. nucifera with a mean of 288 ml min−1; one specimen reached > 500 ml min−1, which is the highest flow rate ever recorded in any plant species, with the nearest values of ≤ 120 ml min−1 recently reported for Equisetum telmateia (Armstrong & Armstrong, 2009). Nelumbo nucifera has an unusual through-flow system in which both influx and efflux flows occur in individual leaves in intact plants (Mevi-Schutz & Grosse, 1988; Matthews & Seymour, 2006). It may be that the unusual long, multi-internode flow pathways documented in N. nucifera by Matthews & Seymour (2006) require considerably higher flows to achieve aeration than the simpler pathways of most other species. In all other plants with convective flow, the pathway of flow is from young influx leaves, capable of generating pressure, to old, leaky, efflux leaves or stubble attached to the same rhizome (Dacey, 1981; Armstrong & Armstrong, 1991; Tornbjerg et al., 1994; Sorrell & Tanner, 2000).
In this study, the monitoring of gas flow from cut stubble showed diel variations, with flow increasing rapidly after sunrise and a sudden change in gas composition of the efflux air as a result of the ventilation in E. dulcis and P. vallatoria. CO2, which had accumulated in the rhizome during the night, was flushed out in the morning, giving a peak emission when the flow started. At the same time, the O2 concentration showed an opposite pattern, with O2-depleted air being flushed out of the rhizomes in the morning and the concentration thereafter reaching almost atmospheric levels during the day at 16–20%. Brix et al. (1996) found similar changes in the gas composition of air from efflux culms in Phragmites australis stands in a temperate climate, although it took longer to flush out CO2 from the night from the rhizomes, and CO2 concentrations were in the range 1–3%, which are comparable with those in this study. The CO2 in rhizomes is a result of the plant’s respiration, but also CO2 produced by soil microorganisms entering the roots and rhizomes. Hence, CO2 concentrations in rhizomes may vary depending on the respiration rates of the below-ground plant parts and the microorganisms in the rhizosphere, which, in turn, depend on factors such as temperature, pH, redox potential and the content of organic matter (Greenway et al., 2006).
The O2 and CO2 concentrations measured during the night are influenced by the back-diffusion of atmospheric air into the system, as convective flow rates were close to zero. Hence, the actual concentrations of O2 and CO2 in the rhizomes during the night were probably lower and higher, respectively, than the values measured. For H. acutigluma, the flow rates were sufficiently low for atmospheric air to affect the values of O2 and CO2 both day and night, giving quite constant measurements with O2 at c. 15–18% and CO2 at c. 2%. However, during the day, there was a slight decrease in O2 concentration and an increase in CO2, probably because O2-depleted air was convected from the rhizomes, although the flow rate was low and not sufficiently high to give an efficient flush of the rhizomes as in E. dulcis and P. vallatoria. The flow from H. acutigluma stubble also showed sudden dips, which may be because of the lower pressurization and flow, and therefore the tube could more easily be blocked by condensed water. It should be emphasized that the curves for the shoot systems depend on how many shoots are attached to the efflux culm and whether there are other leakages in the shoot system. Hence, in the field, there is probably large variation in convective gas flow from different stubbles within the same species.
For E. dulcis and P. vallatoria, there was a linear relationship between flow and pressure, but the slopes may vary depending on the shoot system, as the flow rate is a result of how many shoots contribute to the efflux. Furthermore, Brix et al. (1992) showed that the resistance of the different plant parts and, in particular, the junction between culm and rhizome determines to what degree the plant is able to convert pressure to convective flow.
The sudden decrease in pressure and flow for E. dulcis and P. vallatoria at sunset, even though humidity was still suitable for pressurization, could indicate that factors other than ambient atmospheric humidity are also important. One possible explanation is the presence of thermal transpiration, which occurs in parallel with humidity-driven pressurization and can also contribute to pressurization. However, experimental and modeling evidence has shown that thermal transpiration is a minor contributor relative to humidity-driven pressurization in emergent plants, and may even counteract pressurization (Armstrong et al., 1992; Bendix et al., 1994; Afreen et al., 2007). The decrease in pressure and flow at sunset follows the light intensity very closely, and effects of solar radiation on shoot microclimate, internal humidity and stomatal conductance are likely to be involved (Sorrell & Brix, 2003). Armstrong & Armstrong (1990) also reported that in P. australis, pressures and flows are greatly reduced at light intensities of less than 100 μmol m−2 s−1 when RH is < 40%. On the other hand, it has been reported that, in E. sphacelata, static pressures up to 300 Pa can develop at night in arid climates during the summer, showing that nocturnal convection is possible, although with lower flow rates than during the daytime (Sorrell et al., 1994). However, in our study, we did not observe substantial pressures and flow at night, although our measurements were conducted in the dry season. Hence, the climate in southern Vietnam with high RH in the night throughout the year is not likely to facilitate nocturnal pressurization and flow.
The ability to pressurize and produce convective flow can determine the distribution of species in relation to water depth (Brix et al., 1992; Strand, 2002; Sorrell & Hawes, 2010). In our study, we did not make a detailed survey of the plant distributions, but it was observed that the four floating-leaved plants, which also had the highest flow rates, were able to grow at several meters of water depth, and E. dulcis formed dense vegetation in water up to 1.4 m depth, indicating that this species may have an advantage in deep water related to its high convective flow. By contrast, species such as U. mutica and I. aquatica apparently have a different growth strategy, where they are rooted on land and cover the water surface with creeping, floating stems. Species such as L. hexandra and E. crassipes form free-floating mats, which allow them to invade deeper waters using a strategy without having high convective flow rates.
In conclusion, this study shows, for the first time, that pressurization and convective through-flow are common aeration mechanisms in tropical wetland plants. Although there are different growth strategies to cope with flooding in this area, it is apparently an advantage for plants to have convective flow, especially when growing in deep water.