Aquatic Graminoids

Rushes (Juncus spp.), sedges (Carex spp.) and reeds (Phragmites, Scirpus, Bolboschoenus) are among the commonest groups of species to be found at the edges of streams and lakes. The rushes (Juncus spp.) are also prevalent in poorly drained pastures. Despite their common occurrence in wet soils, rushes (Juncus spp.) are generally not tolerant of prolonged anoxia and the rhizomes of all species of this genus so far tested die after a few days of being placed in an anaerobic incubator. A notable feature of overwintering rushes is the

Fig. 8.14 Scheuchzer's cotton grass (Eriophorum scheuchzeri) — an arctic and alpine wetland sedge with a disjunct distribution from the Alps to the Arctic. In this photograph it is growing in a bog at Mesters Vig, in north-east Greenland (73° N). Arctic populations of E. scheuchzeri have been found to be anoxia tolerant, a property which has not been detected in non-arctic populations of E. angustifolium and E. vaginatum (Crawford et al., 1994). These relatively anoxia- and flood-tolerant plants will have their rhizomes encased in ice throughout the many months ofthe arctic winter and have therefore to endure a prolonged period of oxygen deprivation until they are suddenly re-exposed to oxygen when the ice melts in early summer.

Fig. 8.14 Scheuchzer's cotton grass (Eriophorum scheuchzeri) — an arctic and alpine wetland sedge with a disjunct distribution from the Alps to the Arctic. In this photograph it is growing in a bog at Mesters Vig, in north-east Greenland (73° N). Arctic populations of E. scheuchzeri have been found to be anoxia tolerant, a property which has not been detected in non-arctic populations of E. angustifolium and E. vaginatum (Crawford et al., 1994). These relatively anoxia- and flood-tolerant plants will have their rhizomes encased in ice throughout the many months ofthe arctic winter and have therefore to endure a prolonged period of oxygen deprivation until they are suddenly re-exposed to oxygen when the ice melts in early summer.

persistence of green shoot bases throughout the winter. Aeration of the roots from the shoots, possibly assisted by some winter photosynthesis, can therefore play an important role in their survival. By contrast, the club-rushes and common reeds (Schoenoplectus spp. and

Phragmites australis), which inhabit areas that are frequently subject to prolonged and deep winter flooding in oxygen-deficient muds, have rhizomes which are capable of surviving lengthy periods of anoxia (Braendle & Crawford, 1999).

Oxygen Deprived Roots

Fig. 8.15 Population differences in leaf dissection in and near turloughs in creeping buttercup (Ranunculus repens). (Left) Leaves of R. repens cultivated for one year collected from the lowest elevation (left) and the highest elevation (right) from Hawkhill turlough, Co. Clare, Ireland. (Photo by courtesy of Dr D. Lynn.) (Right) Leaf dissection index of leaves derived from the field and cultivated plants in relation to elevation in the turlough. (Reproduced with permission from Lynn & Waldren, 2003.)

Fig. 8.15 Population differences in leaf dissection in and near turloughs in creeping buttercup (Ranunculus repens). (Left) Leaves of R. repens cultivated for one year collected from the lowest elevation (left) and the highest elevation (right) from Hawkhill turlough, Co. Clare, Ireland. (Photo by courtesy of Dr D. Lynn.) (Right) Leaf dissection index of leaves derived from the field and cultivated plants in relation to elevation in the turlough. (Reproduced with permission from Lynn & Waldren, 2003.)

Fig. 8.16 An alpine bog extensively colonized by the flood-tolerant form of the alpine krummholz pine (Pinus mugo ssp. pumilio). The bog lies just below the summit of Snizka, the highest mountain in the Czech Republic with an altitude of 1602 m (5300 feet) in the Krkonose range. The mountain range is also known as the Giant Mountains (German, Riesengebirge). The Czech name is ancient, appearing in the name of a people listed in Ptolemy as the Corconti. The mountains stretch from north-west to south-east and form the border between Poland and the Czech Republic. (Photo Dr Tomas Kucera.)

Fig. 8.16 An alpine bog extensively colonized by the flood-tolerant form of the alpine krummholz pine (Pinus mugo ssp. pumilio). The bog lies just below the summit of Snizka, the highest mountain in the Czech Republic with an altitude of 1602 m (5300 feet) in the Krkonose range. The mountain range is also known as the Giant Mountains (German, Riesengebirge). The Czech name is ancient, appearing in the name of a people listed in Ptolemy as the Corconti. The mountains stretch from north-west to south-east and form the border between Poland and the Czech Republic. (Photo Dr Tomas Kucera.)

Fig. 8.17 Reed canary grass (Phalaris arundinacea), a semi-aquatic marsh grass with rhizomes that are tolerant of long-term anoxia when overwintering. In the growing season, provided flooding is either shallow or well aerated as here in a moving stream, the species is capable of aerating its submerged organs.

Fig. 8.17 Reed canary grass (Phalaris arundinacea), a semi-aquatic marsh grass with rhizomes that are tolerant of long-term anoxia when overwintering. In the growing season, provided flooding is either shallow or well aerated as here in a moving stream, the species is capable of aerating its submerged organs.

Anoxia-tolerant species can therefore be further divided into two groups, namely those that can extend their shoots in the total absence of oxygen and those that are tolerant of prolonged anoxia but wait for the water table to fall and soil aeration to be restored before resuming growth in spring (see Table 8.1). There are many intermediates between these two extreme types of behaviour in relation to imposed oxygen deprivation. Plants that are tolerant of anoxia over winter can become susceptible to oxygen deprivation in early summer when their carbohydrate reserves have been reduced in the support of spring growth (see Phalaris arundinacea; Fig. 8.17). These variations illustrate the delicate ecological balance that exists between a phenology in which species maintain a prolonged tolerance of anoxia throughout the period of risk from flooding and a more opportunistic strategy which favours a rapid resumption of growth in spring, even if there is a risk of periodic growth checks due to late flooding.

8.7.1 Glyceria maxima versus Filipéndula ulmaria

Such a case can be seen in the competitive relationship between queen of the meadow (Filipendula ulmaria) and reed sweet grass (Glyceria maxima; Fig. 8.18). Successive mapping of the distribution of these two species over an interval of 24 years in a series of dune and slack communities in Tentsmuir National Nature Reserve, Scotland, that had suffered a change in their drainage regime was able to record the ecological consequences of the change that had taken place (Figs. 8.19, 8.20). The alterations in the flooding regime were particularly noticeable in spring when flooding was shallower and disappeared sooner than in the past. The effect on the vegetation was for G. maxima to expand its territory into areas that had formerly been dominated by F. ulmaria. Glyceria maxima is less tolerant of anoxia than F. ulmaria but, like many Juncus species referred to above, maintains green basal leaves during the winter and, provided the flooding is not deep, will resume growth in spring before F. ulmaria. The latter species relies on its anoxia tolerance for survival and does not extend its new season's shoots until the water level has fallen below the surface of the soil. Thus, when flooding is shallow the less-tolerant species has the competitive advantage due to a more precocious phenology. When flooding is more prolonged, maintaining a depth of 10 cm or more, Glyceria maxima cannot compete with the more anoxia-tolerant F. ulmaria (Studer-Ehrensberger et al, 1993; Figs. 8.21-8.22).

Overwintering in wetland habitats necessitates the ability to survive prolonged periods of inundation, which in some species may also include prolonged periods of anoxia. As is evident from much of the discussion above, it is not just the anoxia tolerance of the flooded part of the plant that is important for survival but its relationship to the plant as a whole. The presence or absence of ventilating stalks, or some residual activity in basal shoots, or even photosynthetic activity within the bark of wetland trees such as common alder, can all serve to mitigate the risks of oxygen deprivation in winter. The presence of potential competitors also has a bearing on whether or not flooding creates a marginal situation for the flood-tolerant species.

8.7.2 Sweet flag (Acorus calamus)

The sweet flag (Acorus calamus) is a non-fertile (n = 36, triploid) neophyte (Fig. 8.23), probably introduced from one plant that belonged in 1574 in Vienna to the famous herbalist Charles de L'Ecluse (Latinized as Clusius, 1525-1609; see Schröter, 1908). Nevertheless, despite this apparent lack of population heterozygosity this

Prairie Cordgrass
Fig. 8.18 Reed sweet grass (Glyceria maxima), an example of a semi-aquatic grass with numerous vegetative shoots and stout rhizomes spreading over wide areas in marshes and banks of slow running rivers.

Fig. 8.19 Aerial view of dune and slack system at Tentsmuir, Fife. Rapid accretion of sand has caused this coastline to advance rapidly seawards with the development of a series of dune and slack communities which show distinct boundaries controlled by topography, nutrients and water supply. The yellow box indicates the location of the transect shown in Fig. 8.20. (Photo Cambridge University Collection of Air Photographs: copyright reserved.)

Fig. 8.19 Aerial view of dune and slack system at Tentsmuir, Fife. Rapid accretion of sand has caused this coastline to advance rapidly seawards with the development of a series of dune and slack communities which show distinct boundaries controlled by topography, nutrients and water supply. The yellow box indicates the location of the transect shown in Fig. 8.20. (Photo Cambridge University Collection of Air Photographs: copyright reserved.)

species is a competitive and aggressive invader of heterotrophic European lake edges. This invasive success appears to stem in part from the extreme tolerance of anoxia found in the rhizomes of this species. The rhizomes have high carbohydrate reserves throughout the year which are more than sufficient to sustain etha-nolic fermentation for several months. Furthermore, ATP production is considerably greater than in potato (1.55-2.33 imol ATP g_1fr.wt. h_1) and adenylate pools and energy charge levels remain stable and high throughout prolonged periods of anoxia (Sieber & Braendle, 1991). These figures indicate a state of equilibrium between ATP production and consumption coupled with metabolic rates that are high enough to allow an extended viability for tissues under anoxia. In addition, the porous nature of the rhizomes and their position on the surface of lake muds allows excess ethanol to diffuse out into the lake water and avoids the dangers of post-anoxic conversion to acetaldehyde discussed above (Studer & Braendle, 1984). Messenger RNAs for glycolytic and glycolysis related enzymes are induced anaerobically under artificial anoxia as well as in the natural habitat during winter (Bucher et al., 1996). The proteins formed under anoxia in the laboratory and the field have been shown to be highly active. Moreover, in contrast to non-tolerant species, many additional proteins other than those involved directly in anaerobic metabolism are also synthesized under field and laboratory anoxia and clearly indicate that oxygen depletion is less of a metabolic perturbation and less likely to lead to cellular dysfunction in this species than in potato (Armstrong et al., 1994). In addition, rhizomes of A. calamus are able to store and detoxify nitrogen that has been taken up as ammonium by the roots by transfer into alanine. The main nitrogen storage compound, however, in winter rhizomes is the nitrogen-rich amino acid arginine (Haldemann & Braendle, 1986, 1988). Arginine is readily converted into transport amino acids in spring when growth starts (Weber & Braendle, 1994). Nitrogen recycling and continuous uptake favours growth and development and protein synthesis in this species in comparison with other marsh plants. A similar strategy is used for the detoxification and utilization of sulphide formed in anaerobic soils. It is stored in the rhizomes as glutathione (Weber & Braendle, 1996). Glutathione is used as a sulphur source, but can also serve in the antioxidative defence mechanisms, in addition to tocopherol and phenolics (Larson, 1988). The most outstanding strategy with regard to anoxia tolerance in this species is probably the stability of membrane lipids under anoxia and their protection against peroxidation damage when the tissues are re-aerated (Henzi & Brandle, 1993). After 70 days of anoxia, lipids show only minimal alterations to the saturation level, with the principal change being a shift in fatty acid saturation from 18:3 linolenic acid to 18:2 linoleic acid. Furthermore, free fatty acids in the tissues are minimal and there is little evidence of membrane breakdown.

By comparison, in the anoxia-tolerant common club-rush (Schoenoplectus lacustris) rhizomes begin to show some signs of injury only after 35 days of anoxia. Moreover, in the rhizomes there is only a minor production of the peroxidation products malonedialdehyde and ethane. The membranes of this species are clearly

Ecological Limits

Fig. 8.20 Relationship between vegetation and relief along a dune and slack transect at Tentsmuir National Nature Reserve as recorded over 24 years from (a) 1964 to (b) 1988. For approximate location see Fig. 8.19. The main change between 1964 and 1988 was the advance of the less anoxia-tolerant Glyceria maxima displacing the highly anoxia-tolerant Filipendula ulmaria as a result of a new drain reducing flooding levels. (Reproduced with permission from Studer-Ehrensberger et al., 1993.)

Fig. 8.20 Relationship between vegetation and relief along a dune and slack transect at Tentsmuir National Nature Reserve as recorded over 24 years from (a) 1964 to (b) 1988. For approximate location see Fig. 8.19. The main change between 1964 and 1988 was the advance of the less anoxia-tolerant Glyceria maxima displacing the highly anoxia-tolerant Filipendula ulmaria as a result of a new drain reducing flooding levels. (Reproduced with permission from Studer-Ehrensberger et al., 1993.)

well adapted to withstand prolonged periods of oxygen deprivation. Lipid metabolism under anoxia differs from that of proteins in that lipids are preserved while proteins can be synthesized de novo. This distinction is not unexpected given that lipids will require desaturases and molecular oxygen for their synthesis. Acorus calamus is therefore particularly well defended against the dangers of anoxia, both in terms of internal resistance to anoxia and resistance to externally generated anaerobic products in the soil solution, and can be considered better adapted than even such anoxia-tolerant species as Phragmites australis and Spartina alterniflora where high sulphide concentration can be damaging (see below).

8.7.3 Reed sweet grass (Glyceria maxima)

Among amphibious plant species, reed sweet grass (Glyceria maxima) represents an important example of an ecological strategy for wetland survival, namely seasonal tolerance of anoxia in early spring. Despite this seasonal variation in anoxia tolerance, G. maxima is able to outcompete the more anoxia-tolerant species such as Filipendula ulmaria (Studer-Ehrensberger et al., 1993) due to its capacity for early spring growth enabling it to pre-empt the occupation of sites by other later developing species. In summer G. maxima rhizomes are not as tolerant of anoxia as some other wetland species and cannot survive prolonged deep flooding. When

Scheuchzer Cottongrass Diagram

Care* community Filipéndula community Glyceria community

Fig. 8.21 Interface between retreating patch of Filipéndula ulmaria and an advancing stand of Glyceria maxima. Note the gradual changes in soil pH, conductivity, and organic matter. Despite the gradual change in properties along this section of the transect there is nevertheless an abrupt boundary between the dominant plant species. Compare this with Fig. 8.22 (see text). (Reproduced with permission from Studer-Ehrensberger et al., 1993.)

Care* community Filipéndula community Glyceria community

Fig. 8.21 Interface between retreating patch of Filipéndula ulmaria and an advancing stand of Glyceria maxima. Note the gradual changes in soil pH, conductivity, and organic matter. Despite the gradual change in properties along this section of the transect there is nevertheless an abrupt boundary between the dominant plant species. Compare this with Fig. 8.22 (see text). (Reproduced with permission from Studer-Ehrensberger et al., 1993.)

deprived of oxygen at high summer temperatures (22 °C) the rhizomes can lose 50% of their total nonstructural carbohydrate reserves in 4 days (Barclay & Crawford, 1983). In this case, the underlying cause of anoxia intolerance is energy starvation.

By contrast overwintering rhizomes survive up to three weeks at 22 ° C in the laboratory and probably survive even longer under field conditions. The physiological basis for this seasonal dependence ofanoxia tolerance is not fully understood, but may be due in part to high carbohydrate reserves in winter coupled with a less active metabolism of the overwintering organs. In sites where reed dieback is associated with abnormally high mineral nutrient concentrations, Glyceria maxima can be used as a successful replacement species. Planted into such seemingly phytotoxic sites, as seen from the decline of Phragmites australis, cuttings of Glyceria maxima are able to produce new roots within a few days. The survival strategy of G. maxima in wetland sites is that of a stress avoider rather than a stress tolerator. The

Glyceria community Carex nigra community

Fig. 8.22 Interface between Glyceria maxima and Carex nigra. Note the minimal changes in soil pH, conductivity, and organic matter along this section of the transect and the absence of an abrupt boundary between the dominant plant species and compare this with Fig. 8.21 (see text). (Reproduced with permission from Studer-Ehrensberger et al., 1993.)

Glyceria community Carex nigra community

Fig. 8.22 Interface between Glyceria maxima and Carex nigra. Note the minimal changes in soil pH, conductivity, and organic matter along this section of the transect and the absence of an abrupt boundary between the dominant plant species and compare this with Fig. 8.21 (see text). (Reproduced with permission from Studer-Ehrensberger et al., 1993.)

Planting Reflection Water
Fig. 8.23 The sweet flag (Acorus calamus) invading a lake margin in Switzerland where it has replaced former vigorous stands of the common reed (Phragmites australis).

species has a powerful capacity for oxygen transfer from shoots to roots and the well-developed aerenchyma is protected against accidental flooding by the presence of subdivisions of longitudinally arranged cells. This arrangement prevents inundation of the whole gas lacunae in event of any accidental physical damage and, therefore, reduces the risk of a sudden anoxic stress developing in the underground organs (Armstrong et al., 1994). The capacity for flooding tolerance in this species, however, is strictly limited and the species is not a suitable replacement for Phragmites in areas with large fluctuations in the levels of the water table. The short and soft leaves of Glyceria maxima decay readily and thus fail to provide a snorkel for prolonged periods of submergence.

8.7.4 The common reed (Phragmites australis)

The common reed (Phragmites australis), in common with Acorus calamus and Spartina alterniflora (also wetland geophytes), combines all year round anoxia tolerance with a high capacity for oxygen transport from shoots to roots during the growing season. These species can therefore be considered as both avoiders and tolerators of the anoxic stress condition of wetland sites. Nevertheless, despite this two-pronged tolerance of inundation stress both Phragmites australis and Spartina alterniflora can suffer from elevated levels of sulphide (Bradley & Morris, 1990). High sulphide concentrations, above about 1 mM, occur frequently in reduced sediments of eutrophic lakes, polluted areas and in estuarine muds. An extensive study of sulphide tolerance in Phragmites australis showed that sulphide applied under hypoxic conditions (<0.6 ppm oxygen) severely affects root energy metabolism of reed plants with weakly developed shoots mainly by inactivation of metalo-enzymes. Normally sulphide has no direct access to rhizome tissues because of the thickened rhizome surface. However, grazing by the larvae of the reed beetle (Donacia claviceps) can create lesions which cause flooding of the rhizome air spaces with sulphide-rich water (Ostendorp, 1993). Sulphide can be translocated into the rhizome where it is partially detoxified by the formation of glutathione. The intermediate compounds are cysteine and glutamylcysteine with O-acetylserine acting as the sulphide acceptor. Rhizomes are less sensitive to sulphide poisoning than roots, but the detoxification capacity is limited and sulphide accumulates. The following phenomena have been observed in roots suffering from sulphide poisoning: (1) a decrease in adenylate energy charge and total adenylates, (2) a decrease of alcohol dehy-drogenase activity, and (3) a decrease in post-hypoxic respiratory capacity (Fiirtig et al., 1996).

8.7.5 Amphibious trees

Trees with large trunks and deep anchoring roots represent the ultimate challenge in withstanding oxygen deprivation in wetland habitats. It is therefore surprising that in many parts of the world flooding is no detriment to tree growth. The forested bottomlands of the Mississippi Basin, the swamps of Louisiana and South Carolina, and the mangrove forests of tropical coastal regions, are all testimony to the ability of trees to grow, even where prolonged inundation is inevitable. In common with all other higher plant species the trees of swamp forests have an upper limit for the length of time that they can endure constant inundation, which is determined by the need for access to oxygen for tissue renewal.

The trees of bottomland forests in North America are also dependent on intermittent periods of low water levels for regeneration. For swamp cypress trees it can take four or more years of continuous inundation before many trees are killed (Ewel & Odum, 1984). In the past it was sufficient for this to take place once every 20-30 years. However, improved river level regulation has removed the amount of occasional drawdown of river levels with the result that the regeneration of these forests in several areas such as the Mississippi Basin and the swamp forests of Louisiana is seriously threatened. Even the recruitment of such flood-tolerant trees as the swamp cypress (Taxodium distichum) and the water tupelo (Nyssa sylvatica) is prevented when there is no relief from constant flooding (Conner et al., 1981). Similarly, it is predicted that higher flood levels on the Rhine will reduce the establishment of hardwood tree species in the low-lying sites in this river's flood-plain forests (Siebel et al., 1998).

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