Habitat characteristics of FVTs in relation to nutrient limitation
Most vegetation in this study was subject to some form of inferred nutrient limitation, generally by N, as appears to be the norm in temperate ecosystems (Aerts & Chapin, 2000; Van Duren & Pegtel, 2000). Different forms of nutrient limitation were not distributed randomly between FVTs partly because to some extent these occupied hydrochemical environments that posed different nutritional challenges (Fig. 1). However, in line with previous studies (e.g. Hayati & Proctor, 1990; Wheeler et al., 1992) soil extractable concentrations of nutrients on their own were not an adequate reflection of bioavailability.
In riverine wetlands the narrow growth window between exposure of alluvial sediment and its re-flooding, erosion or burial precludes the development of slower growing, longer-lived stress tolerators. Similarly, regular mowing, poaching or grazing suppresses the development of strongly competitive species. Species with strongly or partially ruderal strategies are therefore typically well represented in habitats ranging from river gravels and temporary floodplain water bodies to river forelands and traditionally managed floodplain meadows (Menges & Waller, 1983; Rodwell, 1992, 2000; Abernethy & Willby, 1999). In such situations the soil nutrient pool is small due to organic impoverishment or export of biomass and vegetation was frequently subject to N-limitation, as predicted for early successional environments by Vitousek & Walker (1987). However, nutrient availability, particularly of P, may be relatively high due to inputs of P adsorbed to riverine sediment and the limited opportunity for immobilization of phosphorus by iron or organic matter complexes. The low N : P supply ratio is liable to accentuate N-limitation. In open, damp, alluvial habitats, with high surface irradiance conditions should favour mineralization of integrated organic matter and nutrient uptake, as well as rapid germination of seeds. Superficial detritus associated with flood strand lines or exported from adjacent riparian forest and beds of emergent monocots must act as an important supplementary source of nutrients in these habitats in the same way that strandline deposits nurture the vegetation of coastal foredunes (Davy & Figueroa, 1993).
The stress tolerator FVT was characterized by low productivity vegetation in peaty, waterlogged sites in acid mires and calcareous spring fed rich fens. S stands had lower concentrations of all nutrients and relatively high N : P and N : K ratios. Critical nutrient contents implied frequent P limitation or colimitation (usually with K) as often previously observed in these habitats (e.g. Boyer & Wheeler, 1989; Hayati & Proctor, 1991; Boeye et al., 1997; Shaver et al., 1998). Phosphorus limitation operates by dual mechanisms in habitats of contrasting pH. In discharge fens at high pH phosphorus is often immobilized by coprecipitation as forms of calcium phosphate (Boyer & Wheeler, 1989). At low pH organic P is reversibly bound to amorphous iron-organic matter complexes, while inorganic P is commonly immobilized as insoluble iron or aluminium phosphates (Shuman, 1991; Kooijman et al., 1998). High concentrations of Fe, Mn and Al often coincide with low soil fertility (assessed phytometrically) although they may be largely independent of extractable concentrations of principal plant nutrients (this study (Fig. 1), Wheeler et al. (1992). Adaptations to mitigate metal ion stress may pose a further constraint on the availability of P relative to other nutrients in S stands (see below). Several S stands were also situated on East Anglian fens located in intensely agricultural catchments, where export of nutrients following reinstatement of hay-making on hydrologically intact sites has restored species-rich spring-fed fen communities associated with P limitation (Koerselman et al., 1990; Fojt & Harding, 1995). Although P limitation is commonly emphasized in small sedge mires it should be stressed that N or NK limitation still accounted for almost half of the inferred limitation of the stress tolerator FVT in the present study. Mineralization of N is generally inhibited in waterlogged, acid soils (De Laune et al., 1981), which also promote leaching of soluble K due to desorption from the cation exchange complex (Bolt & Bruggewert, 1976). Sites subject to forms of N limitation generally had intermediate pH values (in the range 4.6–6.5) where immobilization of P will be relatively weak thus increasing the likelihood of N limitation.
While the growing conditions of S and R stands were strongly divergent the habitat characteristics of C and CS stands overlapped substantially, both with each other and the other FVTs. Habitats ranged from elevated recharge zones subject to predictable winter flooding by nutrient-rich river water and fens subject to a combination of soligenous and topogenous influences (e.g. areas of groundwater discharge within river floodplains), through to the permanently inundated margins of rivers or floodplain water bodies (i.e. open water swamps). Other habitats included groundwater discharge fens with a history of nitrate enrichment of their aquifer, build up of nutrients due to cessation of harvesting or grazing (potentially releasing vegetation from P or K limitation), or a decline in the water table through over-abstraction (Wheeler & Shaw, 1991; Harding, 1993). Although not obvious from our pooled data set, the distribution of C stands was biased towards zones of major nutrient enrichment when examined at an individual site level (Willby et al., 1997). Similar patterns in riverine wetlands have been described by Menges & Waller (1983), Wassen et al. (1995) and Richardson et al. (1999). The greater incidence of nutrient limitation (mainly by N) that we observed in CS stands is consistent with these observations and suggests that in typically productive habitats CS species will persist mostly as subordinates or where the performance of dominant species is locally reduced (e.g. by high divalent metal ion concentrations, Wheeler et al., 1985).
In well-drained sites the effect of increased release of N through peat mineralization should logically be to increase the rate of P limitation (Roem & Berendse, 2000). However, the evidence from our data and from other surveys of high standing crop vegetation is that C and CS type vegetation in fens and marshes is most commonly N limited (Koerselman & Verhoeven, 1995; Bedford et al., 1999; Van Duren & Pegtel, 2000). Presumably, at the level of the environment, this is a consequence of very effective retention and cycling of P (e.g. through high mineralization of P from deep fen peats) under conditions of simultaneous N enrichment (Verhoeven & Arts, 1987). In floodplains and open water swamps widespread N limitation of vegetation, as reported by Van Oorschot et al. (1997) and Wassen et al. (1995), may jointly reflect the scale of alluvial inputs rich in inorganic P (Klopatek, 1978) and the loss of more mobile N from plant litter via leaching, mineralization or denitrification. Conversely, the relatively high proportions of C and R stands that were free of nutrient limitation (none of which had been fertilized for at least 5 yr before this study) are probably testimony to the overall scale of allochthonous nutrient inputs during winter flooding (Wassen et al., 1995; Willby et al., 1997). In the particular case of swamps, the open water nutrient pool, which is continuously replenished by water movement, must be an important supplementary source of nutrients accessible via adventitious roots and submerged stems.
Nutrient signatures of FVTs in relation to plant growth strategies
This study has revealed that wetland FVTs have significantly different nutrient signatures. Since FVTs are distributed nonrandomly within the overall wetland environment these differences will reflect, at least partly, covariation between FVTs and environment. They may relate to indirect correlations with morphological traits, such as the ratio of light harvesting to supportive tissue, that confer a competitive advantage in particular environments (Chapin, 1980; Grime et al., 1988, 1997). Alternatively, they may reflect selection for traits that affect ability to deplete or respond to changes in nutrient supply in resource limited environments (e.g. specific uptake or storage mechanisms) and which determine tissue nutrient contents (e.g. specific root length) or are governed by them (e.g. relative growth rate) (Tilman, 1982; Aerts & Chapin, 2000). Comparison of Fig. 1 and Fig. 6 also reveals that the variation in nutrient content within FVTs is very small relative to the variation in growing conditions. Thus pronounced differences in tissue contents between FVTs are generally preserved even after the covariation between vegetation and environment is removed (Figs 6 and 7). Hence our results also bear the hallmarks of inherent differences in plant growth strategies due to past evolutionary tradeoffs.
Ruderal species are phenotypically plastic and have small but rapidly proliferating root systems with high absorption capacities for limiting nutrients (Grime, 1979; Chapin, 1980; Crick & Grime, 1987; Grime et al., 1997). Consequently they are highly responsive to the marked spatial variation in nutrient supply that is a common feature of disturbed environments, such as riparian zones. These traits reflect a requirement for effective nutrient acquisition strategies in fast-growing species where rapid leaf turnover results in high nutrient losses which must be offset to maintain photosynthetic efficiency (Grime, 1979; Chapin, 1980; Lambers & Poorter, 1992). Consequently, hydrochory, which removes the barrier of seed size on dispersal, is likely to have an important bearing on postgermination nutrient uptake potential in riverine wetlands. Our results, for absolute and standardized nutrient contents clearly testify to the high nutrient affinity of ruderal wetland vegetation. They mirror observations from terrestrial habitats, for example the high nutrient content of plants occurring in the early stages of woodland succession (Woodwell et al., 1975). Auclair (1979) even observed the same trend in nutrient contents from pioneer to seral species within a suite of essentially dominant, stand-forming emergent monocots. McJannet et al. (1995) found that ruderals showed reduced N and P contents relative to other species when grown in excess fertilizer due to rapid reinvestment in new growth as opposed to storage of resource capital. However, under natural conditions where nutrient limitation, particularly by N, appears to be almost routine reinvestment in biomass on a scale that dilutes tissue nutrient concentrations is not feasible. Resources are then likely to be diverted to seed production, and therefore, as we found, ruderal-dominated vegetation is likely to possess comparatively high concentrations of N, P and K (in addition to other mineral nutrients) (Grime et al., 1997; Thompson et al., 1997).
Our observation that N : P ratios are typically lower in ruderal vegetation and higher in vegetation dominated by stress tolerant species is consistent with the results of several recent comparative surveys of mainly terrestrial plants (Grime et al., 1997; Thompson et al., 1997), as well as more general evidence for species and community level adaptations to acquire or conserve the nutrient most limiting to production (Bowman, 1994). Kooijman et al. (1998) also observed that phosphorus uptake was high relative to nitrogen during the early stages of succession in acid dune systems. Meaningful comparisons of N : P ratios in different functional groups growing under field conditions could potentially be distorted by differences in the relative availability of N and P in early vs late successional environments; it is therefore significant that ruderals have been found to maintain markedly lower N : P ratios than other functional groups of wetland plants when grown under standard conditions (McJannet et al., 1995), or, as in our case, when covariation between vegetation and environment is adjusted for. However, the greater importance attributed to phosphorus conflicts with the conventional view of ruderals as nitrophiles, based on the close link between nitrogen nutrition and carbon assimilation (75% of plant N is localized in chloroplasts, mostly in the carbon-fixing enzyme Rubisco; Chapin, 1987). Since P-deficiency restricts flower initiation and seed development (Barry & Miller, 1989) its avoidance has obvious implications in a group of plants characterized by annual/biennial life histories. Consequently a strong positive correlation between P content and relative growth rate (Thompson et al., 1997) may derive partly from the fact that those species with the highest relative growth rates (i.e. ruderals; Grime et al., 1988) also regenerate extensively by seed. Thus we interpret the low N : P ratio in ruderals as evidence of relatively efficient N use due to high nitrogen productivity (sensuBerendse & Aerts, 1987) compared to rapid consumption and diversion of P into reproduction.
Our results demonstrate that S stands contained significantly lower concentrations of all three nutrients than the other FVTs (Figs 3 and 4). These results support the close correlation between low tissue nutrient status and a suite of typical attributes of stress tolerators, including an ability to sustain yield under low nutrient supply, low relative growth rate, high leaf longevity, low phenotypic plasticity, low root absorption capacity and effective nutrient resorption before sensecence (Chapin, 1980; Reich et al., 1992; Grime et al., 1997; Aerts & Chapin, 2000). Hence they support the theory that competitive ability in nutrient limited habitats is governed by effectiveness in lowering the external concentration of a limiting nutrient (Tilman, 1982, 1990; Mamolos et al., 1995) by increasing its rate of acquisition or reducing its loss. These abilities are reflected in minimal tissue concentrations (Aerts & Chapin, 2000).
After removal of the vegetation-environment covariation, our results indicated that nutrient contents of S stands differed markedly from C or CS stands only in terms of lower P and consequently a higher N : P ratio. This supports the existing evidence that stress tolerators focus uptake on more mobile ions such as nitrate while maintaining P reserves due to low internal P demands and efficient conservation (Chapin, 1980; Evans, 1989; Daoust & Childers, 1999). Given the relatively high P : K ratio that we observed this trend apparently does not extend to other mobile ions such as potassium (cf. Veerkamp & Kuiper, 1982). Specific nitrogen uptake mechanisms include preferential use of ammonia where waterlogging favours the reduction of nitrate (De Graaf et al., 1997), although the ionic antagonism between uptake of ammonium (or manganese) and potassium may then lead to K deficiency (Ernst, 1990). Alternatively, radial oxygen release in the rooting zone may be used to promote microbial oxidation of ammonia to nitrate (Engelaar et al., 1995). It is also now known that some nonmycorrhizal sedges utilize organic nitrogen in arctic and alpine environments (Kielland, 1994). Recent studies (e.g. Raab et al., 1999) confirm that this ability extends to plants in subalpine wetlands, comparable to some sites that we studied, where nitrogen mineralization is limited by factors other than temperature. Uptake via a range of mechanisms will be enhanced by increased nitrogen and biomass allocation to below ground organs or a high root surface area or root length per unit root weight, as previously observed in low productivity species (Aerts et al., 1992; Elberse & Berendse, 1993). The emphasis on nitrogen uptake mechanisms may express the need to recover nitrogen losses due to low nitrogen use efficiency in some low productivity species (Bridgham et al., 1995; Aerts & de Caluwe, 1997). These losses arise as a result of the sequestering of N in cell wall materials or secondary compounds, such as polyphenolics (Niemann et al., 1992; Aerts & de Caluwe, 1997), that prolong leaf life span (Poorter & Bergkotte, 1992), deter herbivores (Grime et al., 1996), and ultimately reduce N cycling, thereby delaying the consequences of ecosystem eutrophication (Aerts, 1997). Stress tolerators however, also retain lower relative growth rates than other primary plant strategies under standard growing conditions (Grime et al., 1988). Therefore, from tissue contents alone, we cannot exclude the possibility that luxury consumption of nutrients rather than their investment in growth (Chapin, 1980) contributes to the reduced differential with other strategies in terms of standardized N (and K).
Mechanisms that enhance P uptake in stress tolerators under infertile conditions are often emphasized, including extensive colonization by arbuscular mycorrhiza (Allen, 1991; Grime et al., 1997) and secretion of organic acids by both roots and associated microorganisms (Marschner, 1995; Pérez Corona et al., 1996). However, Pérez Corona et al. (1996) found that the ability to mobilize P from insoluble inorganic sources in a range of Carex species did not correlate with the P availability of their natural habitats. This supports the view that the primary adaptation among stress tolerators to low P availability is an increase in P resorption prior to senescence (Chapin et al., 1982; Berendse & Aerts, 1987; Bowman, 1994). This is borne out by the constitutionally low P contents we found in S stands. Moreover, van Oorschot et al. (1997) have quantified higher phosphorus use efficiency and retranslocation of phosphorus in wet heath vegetation on one site that we studied (Kismeldon Meadows) that provided several examples of S stands. In wetlands the trend for conservation of P might be compounded by the negative effect of waterlogging on root absorption capacities (Gore & Urquhart, 1968). Plant adaptations to reduce stress from high concentrations of divalent metal ions are also likely to impose specific constraints on P nutrition (Laan et al., 1989; Snowden & Wheeler, 1995; De Graaf et al., 1998). Many of the small sedge species predominating in the S stands in this study have extensive root aerenchyma that promotes radial oxygen leakage to the rhizosphere (Green & Etherington, 1977) thereby reducing assimilation of potentially phytotoxic ferrous ions (Snowden & Wheeler, 1993). However, oxidized root plaques are liable to obstruct P uptake (Christensen & Wigand, 1998) or reduce P availability through formation of Fe-P deposits (Snowden & Wheeler, 1995). Separate internal detoxification mechanisms may also result in Fe being immobilized within shoot tissue at the expense of P translocation from the roots (Tannaka et al., 1966; Jones, 1975).
Competitor species achieve high rates of resource capture through active foraging via extensive root systems that provide a large absorptive volume per unit area (Aerts et al., 1992) and therefore tend to have high nutrient contents and a correspondingly high growth rate (Grime et al., 1997). Nutrients are deployed for the formation of canopy foliage (Grime et al., 1988) which requires supportive tissue with a high fraction of cell wall materials such as lignin. Consequently average nutrient contents were generally lower in this group of plants than in ruderals where nutrients reside mainly in the cytoplasm (Grime et al., 1996). In stable, fertile wetlands this is a reflection of the relative importance of effective light interception in the upper canopy layers in determining competitive ability (Elberse & Berendse, 1993; Aerts & de Caluwe, 1994) and therefore the requirement to position the most nitrogen-rich photosynthetic tissue in a way that optimizes carbon gain (Evans, 1989; Poorter et al., 1990). The graminoid growth form meets many of these requirements by having a basal meristem and erect growth while vertically inclined foliage may help reduce self shading. Extensive aerenchyma and the promotion of root aeration via convective gas flow offer significant additional benefits in wetlands (Armstrong et al., 1992) as well as reducing the influx of reduced metal ions and promoting nutrient availability through increased mineralization of organic matter. The average N : P ratio in C and CS stands approximated the supposed optimum for balanced plant growth (c. 10; Aerts & Chapin, 2000). Lower concentrations of P and a higher N : P ratio relative to ruderals are consistent with a strong emphasis on vegetative propagation (mainly via lateral extension of the rhizome). Rhizome storage also facilitates an early onset of growth through translocation of photosynthate (Grime, 1979). In emergent plants, such as Typha latifolia, Phragmites australis and Sparganium erectum, this supports the elevation of new shoots above the water surface and more generally may help synchronize growth to take advantage of temporal fluctuations in resource supply, such as the nutrient flush from decomposing litter (Smith et al., 1988). Competitor species are renowned for producing copious quantities of relatively nutrient-rich litter (Grime, 1979; Grime et al., 1988). The generally more efficient resorption of P and the immobilization of N in litter might be expected to accentuate N limitation (Aerts & Chapin, 2000). However, investigations of reedswamp species indicate that leaching and recycling of N from senesced material may be very rapid (Mason & Bryant, 1975).
CS stands represented the dominant functional type of wetland vegetation. Despite their low phenotypic plasticity, homogenous growth, moderate potential height, low root absorption capacities and intermediate growth rates relative to competitor strategists (Crick & Grime, 1987; Grime et al., 1988; Aerts et al., 1992; Aerts & de Caluwe, 1994) we were unable to detect a significant difference in nutrient contents between CS and C stands, other than lower observed K contents and a higher incidence of inferred N limitation in CS stands. This may highlight a weakness in our approach. Alternatively it might suggest a shift in selection for different components of nutrient use efficiency, namely from high nutrient productivity in fertile habitats to high nutrient retention in less fertile habitats (Berendse & Aerts, 1987), without any overall net affect on tissue contents. CS stands possessed several features including large below-ground biomass, often with massive rhizomes, moderate to large plant size and high relative growth rates compared to S stands that should have provided a competitive advantage in moderately fertile habitats. In wetlands this may include a greater ability to respond to nutrient pulses associated with topogenous inputs and litter decomposition and to translate this into biomass (Crick & Grime, 1987). Thus, in the absence of management, some species (e.g. Cladium mariscus, Filipendula ulmaria) formed extensive monodominant stands. Recent studies have also indicated higher nitrogen use efficiency in high productivity Carex species compared to low productivity congeners. This was due to higher N productivity and higher N resorption caused by lower investment in leaf cell wall materials and phenolics (Aerts & de Caluwe, 1997) which lead to faster rates of litter decomposition and N cycling. A superior nitrogen economy is the expected response in species confronted with N limitation. However, the relatively extravagant rates of leaf turnover in characteristic CS dominants, such as Molinia, should place them at a long-term disadvantage in chronically P-limited sites (Aerts & van der Peijl, 1993). Similarly, although iron tolerance based on exclusion by oxidative precipitation remains high in many CS species (Snowden & Wheeler, 1993), their greater areal capacity for below ground absorption may increase long-term exposure to toxic metal ions with subsequent negative effects on growth.