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- Materials and methods
Plant species dominance is, to a great extent, determined by abiotic factors, such as light and nutrient competition (Tilman 1982). Recent work, however, shows that soil biota affect plant biomass production, plant species diversity and plant succession. Soil biota can enhance plant diversity and plant succession by a specific reduction of dominant plant species (Van der Putten et al. 1993; De Deyn et al. 2003) or by promotion of subordinate plant species (Van der Heijden et al. 1998). The effects of these direct interactions between plants and soil biota on the plant community are, however, context dependent, because arbuscular mycorrhizal fungi can also promote dominant plant species (Hartnett & Wilson 1999) and soil pathogens may reduce rare plants more than dominants (Klironomos 2002), resulting in reduced plant species diversity.
Positive plant-soil microbe feedback has been suggested to play a central role in early successional communities on nutrient poor soils, while negative feedback is expected to contribute to species replacement and diversification in later successional communities at more fertile sites (Reynolds et al. 2003). In general, positive feedback involves mutualistic associations with symbionts or decomposers, while negative feedback involves pathogens, parasites or herbivores. It is suggested that the impact of plant-soil biota feedback on plant community dynamics interacts with soil nutrient availability (Van der Putten & Peters 1997; Wardle 2002; Reynolds et al. 2003). However, the consequences of such interactions for plant community development have hardly been studied experimentally (Bardgett & Wardle 2003).
In order to investigate the interaction between soil fertility and soil biota on plant community development we performed a microcosm experiment in which grassland plants representative of different stages of secondary succession were grown together in sterilized or non-sterilized soil of intermediate productivity, with three levels of nutrient supply. The development of the plant community was evaluated over 1 year. The shoot biomass distribution over the different plant species was assessed three times and the total root biomass was determined at the end of the experiment. The effect of nutrient supply on different trophic groups of soil fauna was studied via the response of the nematode and microarthropod communities of the non-sterilized soils in relation to nutrient supply level and root biomass, as well as via the soil decomposer activity. We hypothesized that increased soil fertility would stimulate plant dominance, but the effect would be less marked when a natural soil biota community was present. We expected that the fast growing plant species that dominate at high nutrient availability (i.e. early successional grasses) would be relatively most reduced by the presence of soil biota.
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- Materials and methods
As soil sterilization changes both (micro)biological and chemical soil properties, the differential response of the synthesized plant communities to the nutrient supply treatments in sterilized and non-sterilized soil results from the net effect of the absence of root pathogens, root herbivores and root symbionts (Bever et al. 1997), as well as from the initial nutrient flush and the temporary absence of nutrient immobilization into soil microbial biomass in the sterilized soil (Troelstra et al. 2001). The original soil was nutrient poor and, assuming the critical N : P ratio to be 16, A. odoratum and P. lanceolata appeared to be P limited (Koerselman & Meuleman 1996). However, according to the triaxial diagram of Venterink (2000), the percentages of N/(N + 10P + K), K/(N + 10P + K) and 10P/N + 10P + K in the foliage of unfertilized A. odoratum and P. lanceolata plants pointed to limitation by K or by both K and N.
As expected, total plant biomass increased with increased nutrient supply. Root biomass was relatively more affected than shoot biomass, suggesting significant below-ground plant community changes. The shoot biomass distribution over the different plant species depended on nutrient supply and on soil sterilization. Soil sterilization favoured fast growing mid- and early successional plant species (L. perenne, P. trivialis and A. capillaris), whilst in non-sterilized soil mid- and late successional forbs (P. lanceolata, C. rotundifolia, C. jacea and S. pratensis) established well, resulting in higher plant community diversity. A low level of nutrient addition to non-sterilized soil increased the biomass of all plant species proportionally and, in contrast to Rajaniemi et al. (2003), plant community diversity was not reduced. Higher nutrient supply, however, favoured A. odoratum disproportionately, increasing its dominance and consequently decreasing plant community diversity. Nutrient supply had the opposite effect in sterilized soil, where there was a trend of increasing Shannon-Weiner evenness with increasing nutrients.
Differences between grasses and later successional forbs in growth rate and in tolerance to herbivory might explain our results. Slow growing plants of nutrient-poor (or late secondary successional) habitats often have longer lived and better defended leaves and roots than faster growing plants from more fertile, or earlier successional, habitats (Grime 1977; Bazzaz 1979; Chapin 1980; Coley 1988; Herms & Mattson 1992; Van der Krift & Berendse 2002). Generalist herbivores tend to prefer nitrogen-rich, poorly defended plant species (Mattson 1980; White 1984; Buckland & Grime 2000), while nutrient supply can enhance the tolerance of plants to and regrowth after herbivory (Steinger & Müller-Schärer 1992). The observed increase in evenness in communities in sterilized soil as nutrient supply increased could be explained by the dominant species needing a smaller proportion of the available nutrients and therefore more being left for the subordinate plants.
Total shoot and root biomass produced in the non-sterilized soil with the highest nutrient supply equalled that in sterilized soil without added nutrients. Although, according to theory, plant diversity is expected to be similar at similar productivity levels (Al-Mufti et al. 1977; Grime 1979; Marrs 1993), plant diversity (Shannon-Weiner evenness) at the end of the experiment differed between these two treatments. Patterns of shoot biomass production during the experiment also differed, suggesting that the production process, over time, may be as important as single observations.
Several plant species showed significantly different responses to nutrient supply in non-sterilized and sterilized soil. Forbs only benefited from (low) nutrient addition in non-sterilized soil, while for grasses the outcome of the interaction between soil sterilization and nutrient supply differed between plant species. The proportional biomass of P. trivialis increased with nutrient supply in sterilized soil, while A. capillaris increased proportionally with nutrient supply in non-sterilized but decreased with nutrient supply in sterilized soil. The decrease in sterilized soil was probably due to interspecific competition with A. odoratum, a plant species that also benefited strongly from increased nutrient supply in the non-sterilized soil. This might be due to its superficial rooting system (Berendse 1983), in combination with nutrient supply at the soil surface. However, as deep-rooting plants (P. lanceolata) were also favoured by nutrient supply in the non-sterilized soil, a higher herbivore tolerance in A. odoratum than in A. capillaris is not unlikely. The observations that P. lanceolata is a poor host for plant-parasitic nematodes (Wardle et al. 2003; De Deyn et al. 2004), while A. capillaris appears to be sensitive to root herbivory (De Deyn et al. 2003) also support the possible involvement of differences in tolerance to herbivory between A. capillaris and A. odoratum.
In diverse plant communities shoot herbivores reduce plants with high relative growth rate more at increased soil fertility, indirectly enhancing slower growing, stress-tolerant plant species (Fraser & Grime 1999) and promoting plant species diversity (Proulx & Mazumder 1998). In our experiment, fast growing early secondary successional plant species were most reduced by soil biota in unfertilized soil and least affected at high nutrient level, probably due to compensatory growth. In natural communities, above-ground herbivory should be more important in suppressing dominant plant species at high soil fertility, while the relative importance of soil biota in suppressing dominant plant species will increase with decreasing soil fertility. Verschoor et al. (2002a) did not find an interaction between root herbivory and nutrient availability on shoot biomass production in Holcus lanatus–A. odoratum mixtures, although grasses and forbs in species mixtures might respond very differently. Regrowth depends on resource availability such that at high resource availability herbivory enhances regrowth of grasses while forbs are favoured at lower nutrient levels (Hawkes & Sullivan 2001).
In contrast to Verschoor et al. (2002b), plant-feeding nematode abundance increased in response to nutrient supply and increased root biomass. However, not only did root quantity increase but also it is likely that root quality, in terms of nitrogen content, and species composition did as well. The plant-feeding nematodes recovered are all known to have a wide host range, consuming roots of most, if not all, of the plant species present. Nematode preference for certain plant species and differences in plant tolerance to nematode feeding are, however, likely (Yeates 1987; Trudgill 1991; De Deyn et al. 2004). The decline of omnivorous nematode abundance with increased nutrient supply could be due to increased competition with specialist plant-feeding nematodes, but their higher sensitivity to nutrient addition, in combination with their slow recovery rate, seems a more likely explanation (Bongers 1990; Bongers & Bongers 1998).
The activity of the decomposer soil biota results in nutrient cycling via decomposition. In contrast to our expectation, cellulose decomposed faster in sterilized than in non-sterilized soil. Air-borne microorganisms such as saprophytic fungi and bacteria may have re-colonized the sterilized soil and could easily have spread and reproduced due to reduced fungistasis and the absence of fungivores (De Boer et al. 2003). The reduced decomposition rate in non-sterilized soil at higher nutrient supply might be due to reduced nitrogen availability. Decomposers of cellulose require nitrogen (McClaugherty et al. 1985), the availability of which was lower in the nutrient-supplied plant communities. Moreover, in the non-sterilized soil the fungivorous nematodes and microarthropods were more abundant at higher nutrient levels, which might have caused top-down control of the fungi (Wardle 2002), hence reducing their ability to decompose cellulose.
In conclusion, our results show that the effect of increased nutrient availability on plant community development and diversity depends on the interaction with soil biota. In the absence of root-feeding invertebrates and high initial nutrient availability, fast growing grass species increase in dominance, independent of subsequent nutrient levels, while other plant species are suppressed. Lower initial nutrient availability and presence of soil biota reduced the growth rate of fast growing plant species, resulting in higher plant community diversity. Grass dominance declined over time, except at high nutrient availability, when increased growth was probably able to compensate for the negative effects of soil biota.
Nutrient supply increased root production, which correlated well with root-feeding nematode density. When nutrient supply is ceased a negative feedback to the most nutrient-responsive plant species can be expected, because nutrients for compensatory growth will no longer be available. Our data suggest that the effect of higher nutrient availability on the interspecific competition of successional plants is not only determined by their nutrient acquisition and growth rates but also by the degree to which they benefit from the interaction with soil biota.