* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project
Download Interspecific competition in natural plant
Survey
Document related concepts
Introduced species wikipedia , lookup
Overexploitation wikipedia , lookup
Molecular ecology wikipedia , lookup
Biodiversity action plan wikipedia , lookup
Plant defense against herbivory wikipedia , lookup
Biological Dynamics of Forest Fragments Project wikipedia , lookup
Latitudinal gradients in species diversity wikipedia , lookup
Plant breeding wikipedia , lookup
Habitat conservation wikipedia , lookup
Ecological fitting wikipedia , lookup
Lake ecosystem wikipedia , lookup
Renewable resource wikipedia , lookup
Storage effect wikipedia , lookup
Transcript
Journal of Experimental Botany, Vol. 50, No. 330, pp. 29–37, January 1999 Interspecific competition in natural plant communities: mechanisms, trade-offs and plant–soil feedbacks Rien Aerts1 Department of Systems Ecology, Vrije Universiteit, De Boelelaan 1087, NL-1081 HV Amsterdam, The Netherlands Received 14 May 1998; Accepted 21 August 1998 Abstract Introduction Interspecific competition in natural plant communities is highly dependent on nutrient availability. At high levels of nutrient availability, competition is mainly for light. As light is a unidirectional resource, highnutrient habitats are dominated by fast-growing perennials with a tall stature and a rather uniform vertical distribution of leaf area. Moreover, these species have high turnover rates of leaves and roots and a high morphological plasticity during the differentiation of leaves. There is less consensus, however, about the importance and intensity of interspecific competition in nutrient-poor environments. It is argued that selection in nutrient-poor habitats is not necessarily on a high competitive ability for nutrients and a high growth rate, but rather on traits which reduce nutrient losses (low tissue nutrient concentrations, slow tissue turnover rates, high nutrient resorption efficiency). Due to evolutionary trade-offs plants can not maximize both growth rate and nutrient retention. Thus, the low growth rate of species from nutrient-poor habitats should be considered as the consequence of nutrient retention rather than as a feature on which direct selection takes place. The contrasting traits of species from nutrient-poor and nutrient-rich habitats mutually exclude them from each others’ habitats. Moreover, these traits have severe consequences for litter decomposability and thereby also for nutrient cycling. This leads both in nutrient-poor and nutrient-rich habitats to a positive feedback between plant species dominance and nutrient availability, thereby promoting ecosystem stability. Most plant scientists agree that interspecific competition is an important determinant of the structure and the dynamics of plant communities. There is, however, much less agreement about the mechanisms of interspecific competition. The literature about competition has long been dominated by the ‘Grime–Tilman’ debate ( Tilman 1985, 1987, 1988; Tilman and Cowan, 1989; Grime, 1979, 1988; Grime and Hodgson, 1987; Thompson, 1987; Thompson and Grime, 1988). These authors disagree about the traits of successful competitors and about the importance of competition in nutrient-poor environments. Moreover, there is still much discussion about biomass allocation patterns of successful competitors and about the relative importance of above- and below-ground competition for the outcome of competitive interactions. Finally, some authors claim that, in nutrient-poor environments, traits which lead to high nutrient retention are far more important for plant performance than traits which lead to a high competitive ability for nutrient uptake (Berendse and Aerts, 1987; Aerts, 1990, 1997a; Berendse, 1994a, b). A surprising aspect of many papers on competition is that it is not specified for which resources species are competing. This certainly contributes to much of the confusion about the traits of successful competitors because it will be shown in this paper that there is a trade-off between traits which lead to a high fitness in nutrient-poor environments and traits which lead to success in more fertile environments. Moreover, both suites of traits have important implications for nutrient cycling processes which may reinforce patterns of species distributions along gradients of soil fertility. The aim of this paper is to present an overview of the traits of successful competitors in nutrient-poor and nutri- Key words: Competition, growth rate, litter decomposition, nutrient retention, plant strategies. 1 Fax: +31 20 4447123. E-mail: [email protected] © Oxford University Press 1999 30 Aerts ent-rich vascular plant communities in temperate regions, respectively. As there is much less debate on the traits of successful competitors in fertile environments compared with nutrient-poor environments, the main emphasis in this paper will be on competition for nutrients in nutrientpoor environments. To this end, both the growth of individuals and the demographics of their populations have been taken into account. Is competition important? In fertile environments, with dense canopies, competition is mainly for light. As light is a uni-directional resource the traits of successful light competitors can be summarized as ‘traits leading to overtopping of the neighbours’. These traits include (1) a robust perennial life form with a strong capacity to ramify vegetatively throughout the aerial and edaphic environment, (2) the rapid commitment of captured resources to the construction of new leaves and roots, (3) high morphological plasticity during the differentiation of leaves and roots, and (4) rapid turnover of individual leaves and roots (Grime and Hodgson, 1987). Moreover, it has been shown that the spatial arrangement of leaf layers, with relatively more leaf area in the top-layers of the canopy, may also be an important determinant of the competitive ability for light interception (Grime, 1979; Spitters and Aerts, 1983; Mitchley, 1988; Barnes et al., 1988, 1990; Aerts et al., 1990). In nutrient-poor environments, competition is mainly for nutrients. However, there is much discussion about the importance of interspecific competition in nutrientpoor environments. This discussion has long been dominated by the ‘Grime–Tilman’ debate ( Tilman, 1985, 1987, 1988; Tilman and Cowan, 1989; Grime, 1979, 1988; Grime and Hodgson, 1987; Thompson, 1987; Thompson and Grime, 1988). Grime (1979, 1988) claims that competition is rather unimportant in nutrient-poor environments and that the intensity of competition increases with increasing productivity. Under nutrient-poor conditions, traits leading to a high nutrient retention would be far more important than a high competitive ability for nutrient uptake. Tilman (1988) claims that the intensity of competition is constant along soil fertility gradients, but that the relative importance of above- and below-ground competition changes. The equilibrial resource ratio hypothesis of Tilman ( Tilman, 1985, 1988) claims that, during succession, plant species replace one another due to changing selective forces on allocation patterns. Tilman postulated that the availability of above-ground resources ( light) and below-ground resources (mostly nutrients) are naturally inversely related. During succession there would be a gradual increase in the availability of soil nitrogen, and due to the increasing biomass, light penetration to the soil surface would decrease. The dominance of a plant species should depend on the point along the soil– resource–light gradient at which this species is a superior competitor. He postulates that, due to the physical separation of above- and below-ground resources, plants face an unavoidable trade-off between the abilities to compete for these resources: in order to obtain a higher portion of one resource plants must allocate more biomass to structures involved in the acquisition of that resource at the expense of allocation of biomass to structures involved in the acquistion of another resource. The studies in which these theories were tested provide only inconclusive evidence. Some studies supported Tilman’s ideas ( Fowler, 1990; Wilson and Shay, 1990; Wilson and Tilman, 1991, 1993) and others supported Grime’s ideas ( Reader, 1990; Aerts et al., 1991; Campbell and Grime, 1992). However, as pointed out by Grace (1991, 1995), much of the controversy may be explained by the different ways by which competition is defined and/or measured. Moreover, it is questionable if there is indeed a relationship between the intensity of competition and the importance of competition in structuring plant communities ( Welden and Slausen, 1986). Thus, at present there is still much confusion about the importance of competition in nutrient-poor environments. Clearly, further experimentation is needed here. In the remainder of this paper two lines of reasoning will be used. In the first one it will be assumed that competition is important in nutrient-poor environments and then the traits of successful competitors will be discussed. In the second one it will be assumed that competition is of secondary importance and the emphasis will be on traits which reduce nutrient losses. Competition for different nitrogen sources: a stabilizing mechanism In most competition models, nutrient competition is implicitly considered to be competition for inorganic forms of nutrients (nitrate, ammonium). In recent years, however, it has become clear that the uptake of organic nitrogen compounds by both mycorrhizal and nonmycorrhizal plants is an important pathway in the terrestrial nitrogen cycle (Read, 1991; Chapin et al., 1993; Kielland, 1994; Northup et al., 1995). The ability of plants to use this ‘short-cut’ of the N cycle may be of great adaptive significance in nutrient-poor habitats, because it potentially gives some plants access to a nitrogen source of which other species are deprived. This differential use of soil nitrogen sources may be an important mechanism for niche differentation and thus for ecosystem stability in nitrogen-poor habitats. In temperate ecosystems the ability to take up more complex organic N sources is mainly restricted to plants with ericoid mycorrhizae (EM ) and ectomycorrhizae ( ECM ) and hardly occurs in species with vesicular- Competition in natural plant communities arbuscular mycorrhizae (AM ) and in non-mycorrhizal plants (Aerts and Chapin, 1999). However, amino acid uptake has been reported for many species, independent of the presence or form of mycorrhizal infection. For example, Näsholm et al. (1998) have shown that Deschampsia flexuosa, growing in a boreal forest, is capable of utilizing amino nitrogen. The litter of EM plants usually has higher concentrations of secondary compounds than litter from AM plants and nonmycorrhizal plants, which may retard N mineralization and thus decrease the availability of inorganic N in the soil (Aerts, 1997b). It has been hypothesized that the use of differential nitrogen sources by the different mycorrhiza types may create positive feedbacks between plant species dominance, litter chemistry and mycorrhiza type. However, until now there has been hardly any field evidence for this hypothesis. Heathlands are suitable ecosystems for investigating the ecological significance of differential uptake of organic and inorganic nitrogen sources. In nutrient-poor heathlands ericoid species (Erica tetralix L., Calluna vulgaris (L.) Hull and Empetrum nigrum L.) predominate (Aerts and Heil, 1993). These ericoid mycorrhizal species have the ability to use (complex) organic N sources for their mineral nutrition, thus making them less dependent on mineralization of organic matter (Read, 1991). In these heathlands, the vegetation also contains grasses such as Deschampsia flexuosa (L.) Trin. and Molinia caerulea (L.) Moench. These species, with AM, have a limited capacity to utilize organic N sources. This is a strong disadvantage under nutrient-poor conditions. This fascinating mechanism of species coexistence as a result of differential use of soil N sources, may be disrupted due to increased levels of atmospheric N deposition (Aerts and Bobbink, 1998). This results in both higher availability of inorganic N and in an increase of the ratio between inorganic and organic N in the soil. This may affect the degree of ericoid mycorrhizal infection, thus depriving the ericoid species of their relative advantage in nutrientpoor soils, and may increase the competitive ability of the grasses, because they can now utilize a source of inorganic N. Clearly, the investigation of this type of species interactions may significantly contribute to our understanding of the regulation of species distribution along soil fertility gradients. Competition in nutrient-poor environments Nutrient acquisition By definition, competition in nutrient-poor environments is for nutrients. Thus, it is logical to assume that plants in those environments have a high competitive ability for nutrient uptake. Is this true? The literature on nutrient uptake has been dominated by studies performed with 31 agricultural species grown at high levels of soil fertility. These studies showed that the uptake kinetics of plant roots are an important determinant of nutrient acquisition. However, as Chapin (1980) already pointed out, great care should be taken when extrapolating these results to wild plant species from nutrient-poor environments. Nutrient acquisition in natural, nutrient-poor habitats depends on both physiological and morphological plant features and on the habitat type (Aerts and Chapin, 1999). Morphological traits are especially important for the acquisition of slowly diffusing nutrients in the soil such as phosphate. Uptake kinetics are usually expressed as the rate of absorption of a particular mineral nutrient per unit root mass. High uptake kinetics involves the construction of extra proton pumps and proteins per unit absorptive root area (Jackson et al., 1990). It has been shown that in microsites with high nutrient availability, roots of fastgrowing species react rapidly by increasing their uptake kinetics (Crick and Grime, 1987; Jackson et al., 1990; Caldwell et al., 1996). This may lead to a competitive advantage for fast-growing species, because the soil is depleted of nutrients before slow-growing species have access to them. This raises the question why slow-growing species from nutrient-poor natural habitats generally do not have high uptake kinetics. The answer is simple: in nutrient-poor habitats, nutrient availability is on average low and nutrients from outside the depletion zone have to diffuse to the roots. This implies that the limiting factor for nutrient uptake in these environments is not the uptake kinetics, but the diffusion rate of the ions in the soil solution. This implies that species with high uptake kinetics face a disadvantage in nutrient-poor environments, because high uptake kinetics does not lead to higher nutrient uptake, but it does lead to higher carbon costs for the construction and maintenance of proton pumps and proteins. However, the situation may be different for nutrient-rich patches. In a review of the responses of wild plants to nutrient patches, Robinson and Van Vuuren (1998) concluded that the uptake rate per unit of root in some slow-growers can certainly be as rapid in response to a nutrient-rich patch as in faster growing species. The morphological traits related to nutrient acquistion vary from those operating at the plant level (shoot–root ratio) to traits operating at the cellular level (root hair density). Moreover, the capacity of plant roots to proliferate into nutrient-rich patches is of great adaptive significance (Jackson and Caldwell, 1996; Grime et al., 1997). All these traits are directed towards overcoming the constraints on nutrient uptake imposed by the low diffusion rates of nutrients in the soil solution. To put it simply: the roots move towards the mineral nutrients instead of the mineral nutrients moving (slowly) to the roots. Thus, in low-nutrient habitats the morphological 32 Aerts plant traits are probably more important for increasing mineral nutrient uptake than the physiological ones (Jackson and Caldwell, 1996; Aerts and Chapin, 1999). In conclusion, species from nutrient-poor habitats are usually not characterized by high nutrient uptake kinetics, except in situations where nutrient-rich patches occur ( Robinson and Van Vuuren, 1998). Biomass allocation and competitive ability for nutrient uptake It seems logical to assume that species from nutrient-poor environments allocate more biomass to their root systems than do species from more fertile sites (cf. Tilman, 1985, 1988). However, this is not a generally observed pattern. It appears that there are different evolutionary solutions to this ecological problem: plants can indeed allocate more biomass to their root systems in order to increase nutrient uptake or they can show adaptive changes in their root morphology by having a higher root length per unit root mass (SRL). Both adaptations have been found in several studies (Aerts and Chapin, 1999). Morphological plasticity in biomass allocation may increase the competitive ability of a plant over a range of different resource availabilities (Crick and Grime, 1987; Tilman, 1988; Grime et al., 1997). This raises the question how nutrient supply affects biomass allocation patterns. In a competition study with evergreen and deciduous heathland species (Aerts et al., 1991), both the evergreens Erica tetralix and Calluna vulgaris and the perennial deciduous grass Molinia caerulea allocated relatively more biomass to the roots at low nutrient supply, thus probably increasing their competitive ability for below-ground resources. This phenotypic response is common to all plant species (Aerts and Chapin, 1999). In the monocultures the percentage decrease of biomass allocation to the roots in Molinia exceeded that in both evergreens thus pointing to a higher phenotypic plasticity in the partitioning of biomass between shoots and roots. However, no general conclusions can be drawn from these results, because Reynolds and D’Antonio (1996) have shown that there are no strong interspecific differences in the plasticity of root allocation among species and functional groups of species. Contrary to Tilman’s (1988) resource ratio hypothesis, the allocation patterns of the heathland species studied by Aerts et al. (1991) entailed no apparent trade-off between their competitive abilities for above- and belowground resources. Molinia was a superior competitor for below-ground resources, but not at the expense of its competitive ability for above-ground resources, despite its low leaf biomass, which was less than 10% of total plant biomass compared to 25–30% for both evergreens. The lower allocation of biomass to the leaves in Molinia as compared with Erica and Calluna was compensated by its higher Specific Leaf Area (SLA: leaf area per unit leaf mass) (R Aerts, unpublished work). On the other hand, the lower biomass allocation to the roots of Erica and Calluna as compared with Molinia was compensated for by their higher Specific Root Length (Boot, 1989). Thus, the competitive ability for below-ground resources is not merely a function of biomass allocation patterns, but also depends on other morphological characteristics, notably Specific Root Length. Similar patterns were observed by Berendse and Elberse (1989), Olff et al. (1990) and Campbell and Grime (1992). The relative importance of above- and below-ground competition The study on the relative importance of above- and below-ground competition was initiated by the classical paper by Donald (1958). He used an experimental design in which the relative effects of above- and below-ground competition were measured by comparing full competition situations with situations in which root and/or shoot competition was prevented by physically separating roots and/or shoots by using pots and screens, respectively. In these studies it was found that there is strong interaction between root and shoot competition. This approach has been adopted by numerous authors mainly working with agricultural species. In an extensive review of studies on the relative importance of above- and below-ground competition Wilson (1988) found that below-ground competition usually affected the balance between the competing species more than above-ground competition. Moreover, competitive effects appeared to be more severe at high levels of resource availability. Aerts et al. (1991) studied the relation between allocation patterns and competitive ability in three species from heathlands in an experimental garden using the technique developed by Donald (1958). They also found that the outcome of the competitive interactions was triggered by root competition, both at low and at high nutrient supply. Competition or nutrient retention? Although it is certainly true that interspecific competition for nutrients is important in explaining species performance in nutrient-poor environments, the situation is more complicated. Nutrient-poor ecosystems are usually dominated by slow-growing perennial species which predominantly belong to the evergreens (Monk, 1966; Aerts, 1995). The nutrient balance of species in these habitats is determined by the balance between nutrient acquisition and nutrient losses (e.g. due to litter production, herbivory and leaching). Thus, plants from low-nutrient habitats can have large internal nutrient pools by having a high competitive ability for nutrient uptake and/or having low rates of nutrient loss. As already discussed, these species Competition in natural plant communities do not show physiological characteristics which lead to high uptake kinetics, because nutrient acquisition is determined more by the low diffusion rates of mineral nutrients in the soil solution. Thus, it is to be expected that there is strong selection on plant traits which lead to low nutrient loss rates. Model studies (Aerts and Van der Peijl, 1993; Berendse, 1994a) also show that low nutrient loss rates of plant species in habitats where plant growth is nutrient-limited confer clear advantages: low nutrient loss rates can theoretically lead to a higher equilibrium biomass ( Fig. 1) and they lead to competitive replacement of species with higher nutrient loss rates even when these species have a higher competitive ability for nutrient uptake (Berendse, 1994a). It is indeed found that plant species from nutrient-poor environments are characterized by numerous features which reduce nutrient losses, such as long tissue lifespan and low nutrient concentrations in senesced tissues. As high tissue lifespan leads to retention of nutrients within plants, it may be expected that species from nutrient-poor habitats would adopt this strategy. This hypothesis has been confirmed by numerous studies (Aerts, 1990; Escudero et al., 1992; Reich et al., 1992; Ryser and Lambers, 1995; Schläpfer and Ryser, 1996; Eckstein and Karlsson, 1997; Eissenstat and Yanai, 1997). The importance of variation in leaf lifespan for a wide variety of ecological processes, including those related to mineral nutrition, has been extensively treated by Reich et al. (1992). High nutrient retention by the plant is positively correlated with low nutrient concentrations in senesced tissues. These could arise because the tissues held low concentrations in the first place or because nutrients were resorbed efficiently during senescence. The former is certainly a characteristic trait since growth forms are known to differ consistently in nutrient concentration. For instance, evergreen and deciduous shrubs and trees have, on a whole plant basis, lower tissue nutrient concentrations than forbs and grasses (Shaver and Chapin, 1991). This is largely because the biomass of the woody plants is mainly Fig. 1. Simulated long-term biomass dynamics of Calluna vulgaris and Molinia caerulea which have an equal nutrient use efficiency (NUE), but which differ in their components of NUE: mean residence time of nitrogen in the plant (MRT ) and the rate of dry matter production per unit of nitrogen (A). Redrawn from Aerts and Van der Peijl (1993). 33 stem, trunk and roots, consisting of a high proportion of carbon-rich molecules per unit mass of tissue. Individuals are able to hold large absolute quantities of nutrients because they have high biomass compared to forbs and grasses, though nutrient concentrations are inevitably low. Leaf nutrient concentrations are lowest in evergreen shrubs and trees and highest in forbs (Aerts and Chapin, 1999). As carbon assimilation of a leaf is linearly related to nitrogen content of the leaf (Hirose and Werger, 1987; Evans, 1989), the N concentration in leaves has implications for the differential productivity of these growth forms. The relative importance of resorption is less clear. Two recent analyses of data in the literature have shown little difference between growth forms and no nutritional controls on nutrient resorption (Aerts, 1996; Killingbeck, 1996). The conclusion from both papers was that the low nutrient concentration per unit leaf matter in evergreens contributed far more to overall nutrient retention than did resorption during senescence. Trade-offs and plant-soil feedbacks Plant species which are successful in nutrient-poor habitats have different sets of adaptive traits (‘strategies’) than successful competitors in fertile habitats. The strategy of species from infertile habitats comprises traits which lead to nutrient retention, whereas the strategy of species from nutrient-rich habitats comprises traits which lead to rapid growth and quick capture of both aboveand below-ground resources. The fact that this differentiation occurs between species from habitats differing in soil fertility strongly suggests that there is a trade-off between their respective traits. If this were not the case, then the earth would be occupied by a few ‘super-species’ which would dominate all types of habitats. To put it differently: these hypothesized trade-offs form one of the fundamental causes of botanical species diversity on earth. This raises the question if there is any biological logic behind these trade-offs? In fact, there is. Species from nutrient-poor habitats are often characterized by tissues with slow turnover rates, low concentrations of mineral nutrients and high concentrations of secondary compounds, which serve amongst other things as a defence against herbivory (Aerts and Chapin, 1999). All these traits lead to a low growth rate and/or to a low potential of resource capture (Grime et al., 1997). An example of this trade-off is provided by data of Reich et al. (1992) on the relation between leaf lifespan and a wide variety of ecological parameters. They found a significant negative relation between leaf lifespan and the Relative Growth Rate (RGR) of plants ( Fig. 2). On the other hand, traits which do lead to a high growth rate and to high rates of resource capture, such as rapid turnover of leaves and high leaf nutrient concentrations, inevitably lead to high nutrient loss rates and thus low nutrient 34 Aerts Fig. 2. Relative growth rate (RGR) per week of seedlings in relation to leaf lifespan (months). R2=0.61. Redrawn from Reich et al. (1992). retention. Thus, the hypothesized trade-offs have a clear and logical biological basis. It is important to notice that the traits associated with competitive dominance in habitats differing in soil fertility may also have effects on ecosystem nutrient cycling. In nutrient-poor environments, species produce relatively small amounts of litter due to the long lifespans of the various tissues. This litter generally has low nutrient concentrations and high concentrations of secondary compounds such as lignin and phenolics. In a recent analysis, Aerts (1997b) showed that litter decomposition rates are negatively related to the lignin/N ratio in the litter and positively to the N concentration in the litter. Thus, species from nutrient-poor environments produce litter which decomposes slowly and from which only low amounts of nutrients are released. The opposite holds for species from fertile environments. Due to their high tissue turnover rates they produce relatively large amounts of litter. Moreover, this litter contains relatively high concen- trations of mineral nutrients and low concentrations of secondary compounds. As a result, this litter decomposes relatively quickly and releases large amounts of nutrients. An example of this mechanism is provided by work on the interaction between species composition and nutrient cycling in Dutch heathlands (Aerts and Heil, 1993). In these heathlands, the ericaceous species Erica tetralix and Calluna vulgaris dominate the vegetation at low nutrient availability, but they are replaced by the grasses Molinia caerulea or Deschampsia flexuosa when nutrient availability increases. These grasses produce more litter (except Deschampsia) which decomposes faster and releases more nutrients ( Table 1). Thus, these grass species speed up the rate of nutrient cycling and thereby create favourable conditions for their own fitness. This pattern was confirmed by a simulation study of Berendse (1994b) who demonstrated that the plant traits of evergreens ( low nutrient loss rates and low litter decomposition rates) can be favourable under nutrient-limited growth conditions. Low litter decomposability and the resulting low rate of nutrient release from that litter, as observed in evergreen species, can theoretically lead to longer dominance of the evergreen species (Fig. 3). This implies that the plant characteristics of evergreens not only reduce nutrient losses, but may also lead to a higher fitness due to longterm effects on soil fertility and thereby on the competitive balance between evergreen and deciduous species. Thus, in nutrient-poor ecosystems the combination of low productivity (and thus low litter production), and low litter decomposibility may lead to a low rate of ecosystem N cycling (Chapin, 1993; Van Breemen, 1993). This may prevent the invasion of highly competitive species which are dependent on high N availability (Aerts and Van der Peijl, 1993; Berendse, 1994a, b). On the other hand, the traits of species from fertile environments lead to a high rate of ecosystem N cycling and this excludes slow-growing and nutrient-conserving species from these habitats. Fig. 3. Simulated biomass dynamics of an evergreen species (dashed line) with low nutrient loss rates and a competing deciduous species (solid line) with high nutrient loss rates during succession on bare soil. The decomposition constant of the deciduous species is held constant (k=0.1), whereas the decomposition constant (k) of the evergreen species is decreased from 0.2 to 0.05. Lowering the decomposition constant leads to longer dominance of the evergreen species. Redrawn from Berendse (1994b). Competition in natural plant communities 35 Table 1. Litter production (g m−2 year−1), decomposition constants (k: year−1) and N mineralization of dominant heathland species in the Netherlands (after Aerts, 1993) Wet heathland Litter production Total Decomposition constants Shoots Roots N-mineralization (g N m−2 year−1) N-mineralization (mg N g−1 soil N year−1) Dry heathland Erica Molinia Calluna Deschampsia Molinia 800 2060 730 430 2050 0.10 0.03 0.23 0.29 0.17 0.12 4.4 7.8 6.2 16 29 Conclusions Interspecific competition is an important determinant of the structure and dynamics of plant communities. Currently, there is still much debate on the nature and the intensity of interspecific competition in nutrient-poor environments. The experimental data which are available at this moment do not provide any conclusive evidence for either the ‘Grime’ or the ‘Tilman’ theory. Current nutrient competition models only consider competition for inorganic nitrogen. However, recent data show that many species are capable of taking up nitrogen in organic form. Due to this ‘short-cut’ of the terrestrial nitrogen cycle the current models of interspecific competition should be revised. However, quantitative data about the importance of this pathway are lacking. In nutrient-poor environments, root morphology and root allocation are generally more important for determining the outcome of competition for nutrients than nutrient uptake kinetics. An additional factor in this discussion is that the nutrient dynamics of species in nutrient-poor habitats is determined by the balance between nutrient acquisition and nutrient loss rates. Thus, plants from low-nutrient habitats can have large internal nutrient pools by having a high competitive ability for nutrient uptake and/or having low nutrient loss rates. The data available so far strongly suggest that there is strong selection on traits which lead to low nutrient loss rates and less on those which lead to a high competitive ability for nutrient uptake. Thus, in nutrient-poor ecosystems the combination of low productivity (and thus low litter production), and low litter decomposibility may lead to a low rate of ecosystem N cycling. This may prevent the invasion of highly competitive species which are dependent on high N availability. On the other hand, the traits of species from fertile environments lead to a high rate of ecosystem N cycling and this excludes slowgrowing and nutrient-conserving species from these habitats. From these patterns, it can be concluded that the strategies of species from nutrient-poor and nutrient-rich habitats promote long-term ecosystem stability. This is 25 0.34 0.24 0.21 0.37 12.6 10.9 36 35 an important evolutionary consequence of these strategies, although it is questionable if long-term ecosystem stability is prone to natural selection. Acknowledgements This paper was one of a series of invited presentations at a session on Stabilizing processes in mixed plant communities held as part of the Society for Experimental Biology Annual Meeting at York in March 1998. Funding for the session was given by the Scottish Office Agriculture Environment and Fisheries Department, the Journal of Experimental Botany and the Society for Experimental Biology. References Aerts R. 1990. Nutrient use efficiency in evergreen and deciduous species from heathlands. Oecologia 84, 391–397. Aerts R. 1995. The advantages of being evergreen. Trends in Ecology and Evolution 10, 402–407. Aerts R. 1996. Nutrient resorption from senescing leaves of perennials: are there general patterns? Journal of Ecology 84, 597–608. Aerts R. 1997a. Nitrogen partitioning between resorption and decomposition pathways: a trade-off between nitrogen use efficiency and litter decomposability ? Oikos 80, 603–606. Aerts R. 1997b. Climate, leaf litter chemistry and leaf litter decomposition in terrestrial ecosystems: a triangular relationship. Oikos 79, 439–449. Aerts R, Bobbink R. 1998. The impact of atmospheric nitrogen deposition on vegetation processes in non-forest ecosystems. In: Langan S, Wilson JF, eds. The impact of nitrogen deposition on natural and semi-natural ecosystems. London: Chapman and Hall. Aerts R, Chapin III FS. 1999. The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Advances in Ecological Research 29, (in press). Aerts R, Heil GW (eds). 1993. Heathlands, patterns and processes in a changing environment. Dordrecht: Kluwer Academic Publishers. Aerts R, van der Peijl MJ. 1993. A simple model to explain the dominance of low-productive perennials in nutrient-poor habitats. Oikos 66, 144–147. Aerts R, Boot RGA, Van der Aart PJM. 1991. The relation between above- and below-ground biomass allocation patterns and competitive ability. Oecologia 87, 551–559. 36 Aerts Aerts R, Berendse F, De Caluwe H, Schmitz M. 1990. Competition in heathland along an experimental gradient of nutrient availability. Oikos 57, 310–318. Barnes PW, Jordan PW, Gold WG, Caldwell MM. 1988. Competition, morphology and canopy structure in wheat (Triticum aestivum L.) and wild oat (Avena fatua L.) exposed to enhanced ultraviolet-B radiation. Functional Ecology 2, 319–330. Barnes PW, Beyschlag W, Ryel RJ, Flint SD, Caldwell MM. 1990. Plant competition for light analysed with a multispecies canopy model. III. Influence of canopy structure in mixtures and monocultures of wheat and wild oat. Oecologia 82, 560–566. Berendse F. 1994a. Competition between plant populations at low and high nutrient supplies. Oikos 71, 253–260. Berendse F. 1994b. Litter decomposability—a neglected component of plant fitness. Journal of Ecology 82, 187–190. Berendse F, Aerts R. 1987. Nitrogen-use-efficiency: a biologically meaningful definition? Functional Ecology 1, 293–296. Berendse F, Elberse WTh. 1989. Competition and nutrient losses from the plant. In: Lambers H, Cambridge ML, Konings H, Pons TL, eds. Causes and consequences of variation and productivity of higher plants. The Hague: SPB Academic Publishing, 269–284. Boot RGA. 1989. The significance of size and morphology of root systems for nutrient acquisition and competition. In: Lambers H, Cambridge ML, Konings H, Pons TL, eds. Causes and consequences of variation in growth rate and productivity of higher plants. The Hague: SPB Academic Publishing, 299–311. Caldwell MM, Manwaring JH, Durham SL. 1996. Species interactions at the level of fine roots in the field influence soil heterogeneity and plant size. Oecologia 106, 440–447. Campbell BD, Grime JP. 1992. An experimental test of plant strategy theory. Ecology 73, 15–29. Chapin FS. 1980. The mineral nutrition of wild plants. Annual Review of Ecology and Systematics 11, 233–260. Chapin FS. 1993. The evolutionary basis of biogeochemical soil development. Geoderma 57, 223–227. Chapin FS, Moilanen L, Kielland K. 1993. Preferential use of organic nitrogen for growth by a non-mycorrhizal arctic sedge. Nature 361, 150–153. Crick JC, Grime JP. 1987. Morphological plasticity and mineral nutrient capture in two herbaceous species of contrasted ecology. New Phytologist 107, 403–414. Donald CM. 1958. The interaction of competition for light and for nutrients. Australian Journal of Agricultural Research 9, 421–435. Eckstein RL, Karlsson PS. 1997. Above-ground growth and nutrient use by plants in a subarctic environment: effects of habitat, life-form and species. Oikos 79, 311–324. Eissenstat DM, Yanai RD. 1997. The ecology of root lifespan. Advances in Ecological Research 27, 1–60. Escudero A, del Arco JM, Sanz IC, Ayala J. 1992. Effects of leaf longevity and retranslocation efficiency on the retention time of nutrients in the leaf biomass of different woody species. Oecologia 90, 80–87. Evans JR. 1989. Photosynthesis and nitrogen relationships in leaves of C plants. Oecologia 78, 9–19. 3 Fowler NL. 1990. The effects of competition and environmental heterogeneity on three coexisting grasses. Journal of Ecology 78, 389–402. Grace JB. 1991. A clarification of the debate between Grime and Tilman. Functional Ecology 5, 583–587. Grace JB. 1995. On the measurement of plant competition intensity. Ecology 76, 305–308. Grime JP. 1979. Plant strategies and vegetation processes. Chichester: Wiley. Grime JP. 1988. Limiting factors for modellers. Nature 336, 630. Grime JP, Hodgson JG. 1987. Botanical contributions to contemporary ecological theory. In: Rorison IH, Grime JP, Hunt R, Hendry GAF, Lewis DH, eds. Frontiers of comparative plant ecology. London: Academic Press. New Phytologist (Supplement) 106, 283–296. Grime JP and 32 others. 1997. Integrated screening validates primary axes of specialisation in plants. Oikos 79, 259–281. Hirose T, Werger MJA. 1987. Nitrogen use efficiency in instantaneous and daily photosynthesis of leaves in the canopy of a Solidago altissima stand. Physiologia Plantarum 70, 215–222. Jackson RB, Caldwell MM. 1996. Integrating resource heterogeneity and plant plasticity modelling nitrate and phosphate uptake in a patchy soil environment. Journal of Ecology 84, 891–903. Jackson RB, Manwaring JH, Caldwell MM. 1990. Rapid physiological adjustment of roots to localized soil enrichment. Nature 344, 58–60. Kielland K. 1994. Amino acid absorption by arctic plants: implications for plant nutrition and nitrogen cycling. Ecology 75, 2373–2383. Killingbeck KT. 1996. Nutrients in senesced leaves: keys to the search for potential resorption and resorption proficiency. Ecology 77, 1716–1727. Mitchley J. 1988. Control of relative abundance of perennials in chalk grassland in southern England. II. Vertical canopy structure. Journal of Ecology 76, 341–350. Monk CD. 1966. An ecological significance of evergreenness. Ecology 47, 504–505. Näsholm T, Ekblad A, Nordin A, Giesler R, Högberg M, Högberg P. 1998. Boreal forest plants take up organic nitrogen. Nature 392, 914–916. Northup RR, Yu Z, Dahlgren RA, Vogt KA. 1995. Polyphenol control of nitrogen release from pine litter. Nature 377, 227–229. Olff H, Van Andel J, Bakker JP. 1990. Biomass and shoot/root allocation of five species from a grassland succession series at different combinations of light and nutrient supply. Functional Ecology 4, 193–200. Read DJ. 1991. Mycorrhizas in ecosystems. Experientia 47, 376–391. Reader RJ. 1990. Competition constrained by low nutrient supply: an example involving Hieracium floribundum Wimm & Grab. (Compositae). Functional Ecology 4, 573–577. Reich PB, Walters MB, Ellsworth DS. 1992. Leaf life-span in relation to leaf, plant, and stand characteristics among diverse ecosystems. Ecological Monographs 62, 365–392. Reynolds HL, D’Antonio C. 1996. The ecological significance of plasticity in root weigh ratio in response to nitrogen: opinion. Plant and Soil 185, 75–97. Robinson D, Van Vuuren MMI. 1998. Responses of wild plants to nutrient patches in relation to growth rate and life-form. In: Lambers H, Poorter H, Van Vuuren MMI, eds. Inherent variation in plant growth. Physiological mechanisms and ecological consequences. Leiden: Backhuys Publishers, 1–21. Ryser P, Lambers H. 1995. Root and leaf atributes accounting for the performance of fast- and slow- growing grasses at different nutrient supply. Plant and Soil 170, 251–265. Schläpfer B, Ryser P. 1996. Leaf and root turnover of three ecologically contrasting grass species in relation to their performance along a productivity gradient. Oikos 75, 398–406. Competition in natural plant communities Shaver GR, Chapin FS. 1991. Production:biomass relationships and element cycling in contrasting arctic vegetation types. Ecological Monographs 61, 1–31. Spitters CJT, Aerts R. 1983. Simulation of competition for light and water in crop-weed associations. Aspects of Applied Biology 4, 467–483. Thompson K. 1987. The resource ratio hypothesis and the meaning of competition. Functional Ecology 1, 297–303. Thompson K, Grime JP. 1988. Competition reconsidered—a reply to Tilman. Functional Ecology 2, 114–116. Tilman D. 1985. The resource-ratio hypothesis of plant succession. American Naturalist 125, 827–852. Tilman D. 1987. On the meaning of competition and the mechanisms of competitive superiority. Functional Ecology 1, 304–315. Tilman D. 1988. Plant strategies and the dynamics and structure of plant communities. Princeton University Press. 37 Tilman D, Cowan ML. 1989. Growth of old field herbs on a nitrogen gradient. Functional Ecology 3, 425–438. Van Breemen N. 1993. Soils as biotic constructs favouring net primary productivity. Geoderma 57, 183–211. Welden CW, Slausen WL. 1986. The intensity of competition versus its importance: an overlooked distinction and some implications. Quarterly Review of Biology 61, 23–43. Wilson JB. 1988. Shoot competition and root competition. Journal of Applied Ecology 25, 279–296. Wilson SD, Shay JM. 1990. Competition, fire, and nutrients in a mixed-grass prairie. Ecology 71, 1959–1967. Wilson SD, Tilman D. 1991. Components of plant competition along an experimental gradient of nitrogen availability. Ecology 72, 1050–1065. Wilson SD, Tilman D. 1993. Plant competition and resource availability in response to disturbance and fertilization. Ecology 74, 599–611.