Effects of six grassland plant species on soil nematodes: A glasshouse experiment

https://doi.org/10.1016/j.soilbio.2007.11.006Get rights and content

Abstract

The effects of six individual plant species on the abundance and composition of nematode communities were studied in a glasshouse experiment during 16 weeks. The effect of the presence of plants, the correlation between nematode abundance and plant biomass, the response of plant-feeding nematodes and other nematode groups to different plant species was examined and also whether the effect differed between plant species within a plant functional group. The total number of nematodes increased during the study period in all treatments, although in some treatments, the increase levelled off after 8 or 12 weeks. The identity of the plant species affected both the total abundance of nematodes and the nematode community composition. The number of bacterial-feeding nematodes was greatest under grasses and legumes and was positively correlated with shoot biomass and negatively with root biomass. The response of the plant-feeding nematodes, which differed in abundance under both the investigated legume and the forb species, suggests that the identity of the plant species is more important than the plant functional group. A possible explanation could be related to differences in plant secondary metabolites. Despite some differences in the nematode species pool, the effects of plant species appear quite consistent between the present glasshouse study and previous field experiments.

Introduction

Plant species identity and the composition of the plant community are important determinants of decomposer function and community composition in soil (Wardle, 2005). For microorganisms, this has been shown both in terms of microbial biomass and activity in microcosms with soil from grasslands (Bardgett et al., 1999; Innes et al., 2004) as well as microbial community composition in microcosms (Grayston et al., 1998; Marschner et al., 2001), field experiments (e.g., Smalla et al., 2001; Kowalchuk et al., 2002) and in a naturally mixed spruce-birch stand (Saetre and Bååth, 2000).

Soil fauna are also affected by individual plant species. In both field and pot experiments, nematodes responded to the identity of different grassland species, with plant-feeding and microbial-feeding nematodes (bacterial and fungal feeders) being the groups most clearly influenced by plant species identity (Wardle et al., 2003; De Deyn et al., 2004; Viketoft et al., 2005). Collembolans have been shown to respond to grass and legume species in pot and field experiments with an assembly of grassland species (Salamon et al., 2004; Milcu et al., 2006), and both mites and collembolans responded to plant species in high Arctic heath vegetation (Coulson et al., 2003). In addition, mites have also been shown to be affected by different plant species used in agroforestry (Badejo and Tian, 1999).

Plants affect the belowground community through differences in the amount and quality of resources allocated to the soil, in the extent to which they deplete nutrients and water from the soil, in the chemical composition of the litter produced and through the formation and modification of habitats (Wardle, 2002). For example, many legumes differ from other forbs in their ability to fix atmospheric nitrogen and therefore increase the amount of nitrogen in the soil, principally in the form of nitrate (Palmborg et al., 2005). They also produce more high-quality litter that is more easily decomposed (Scherer-Lorenzen et al., 2003). Previous studies on the effect of plant species on nematodes have shown that, in general, plant feeders seem to be most abundant under grasses and have a lower presence under some forbs, while microbial feeders show varying responses to the investigated plant species in different studies (Wardle et al., 2003; De Deyn et al., 2004; Viketoft et al., 2005). In addition, different feeding types of plant feeders, e.g., ecto- and endoparasites, have been shown to respond differently to grasses and forbs (De Deyn et al., 2004).

The aim of the present study was to examine, in a glasshouse pot experiment, how six plant species, belonging to three plant functional groups (grasses, legumes and forbs), affect total nematode abundance, nematode community composition and the response of individual nematode genera. A defaunated soil from an experimental grassland that was reinoculated with both microflora and nematodes was used. Thus, the effect of plant species during the establishment phase of nematode communities was evaluated under controlled conditions. In addition, a treatment containing no plants was included, top-down effects by micro- and mesofauna other than nematodes were removed and soil characteristics (e.g., pH, inorganic nitrogen), missing in other studies (Wardle et al., 2003; De Deyn et al., 2004; Viketoft et al., 2005), were determined to relate to the nematode data.

Specifically, the following hypotheses are addressed:

  • 1.

    Low numbers of nematodes should be found in the treatment with no plants, due to the lack of plant-derived resources.

  • 2.

    There is a positive correlation between total nematode abundance and plant productivity (Yeates, 1987).

  • 3.

    Plant-feeding nematodes should show the strongest response to the identity of plant species because they feed directly on them, although the speed of the response between bacterial- and plant feeders likely differs because of different generation times. Based on previous studies, plant feeders are also expected to be most abundant under grasses.

  • 4.

    Legumes, due to their N-fixing ability, will affect the nitrogen levels in the soil and hence the bacterial community. This should affect the nematode community composition by promotion of bacterial-feeding nematodes, especially Rhabditis and Panagrolaimus.

  • 5.

    Different plant species within a functional group will have quite different influences on the nematodes (Viketoft et al., 2005). The division into plant functional groups was based on growth form and N-fixing ability, but the plant species may contain different secondary substances.

The nematode fauna under monocultures of the plant species used in this study have previously been investigated after seven growing seasons in an experimental grassland in northern Sweden (Viketoft et al., 2005). Although the present study is a 16-week experiment, where plants were getting established and a limited number of nematodes were inoculated, it had higher replication and a treatment containing no plants compared to the field experiment. A comparison between these studies may illustrate interesting aspects of the interactions between plants and soil communities.

Section snippets

Site and soil

In November 2004, soil was collected to 10 cm depth from the experimental field of the BIODEPTH project of the Swedish University of Agricultural Sciences, Umeå, northern Sweden (63°45′N, 20°17′E). The soil is classified as silt loam (4.1% clay, 57.9% silt, 38.0% fine sand) and was taken from an area between the experimental plots, which is dominated by Phleum pratense and Trifolium repens. The soil was stored at 4 °C until further processed in February 2005. The vegetation was then removed and

Plant growth and soil chemistry

Shoot and root biomass differed significantly between the plant treatments (Table 1). In general, the legumes had the highest shoot biomass and forbs the lowest. No such pattern among plant functional groups was found for the root biomass. Instead, R. acetosa clearly had the greatest root biomass. The presence of plants affected the soil during the experimental period, which is demonstrated by the pots without plants having the highest nitrate levels and the lowest organic matter content (Table

Discussion

As hypothesised, the no-plant treatment had the lowest total number of nematodes. However, a correlation between total nematode abundance and plant biomass was not found, but the abundance of bacterial feeders correlated with both shoot and root biomass. Plant-feeding nematodes showed the strongest response to the different plant species but in contrast to the hypothesis they did not have their greatest abundances under grasses. In addition, legumes did not specifically promote

Acknowledgements

The author thanks Cecilia Palmborg for collecting the soil, Karin Önneby for help with the set-up of the experiment and Birgitta Vegerfors-Persson for statistical advice. Author also thanks Jan Bengtsson, Björn Sohlenius and Cecilia Palmborg for valuable comments on previous versions of the manuscript and the anonymous reviewers for constructive comments on the manuscript. This study was funded by the Oscar and Lili Lamm Foundation and the Swedish Research Council (grant to Jan Bengtsson).

References (43)

  • S. Athanasiadou et al.

    Plant secondary metabolites: antiparasitic effects and their role in ruminant production systems

    Proceedings of the Nutrition Society

    (2004)
  • M.A. Badejo et al.

    Abundance of soil mites under four agroforestry tree species with contrasting litter quality

    Biology and Fertility of Soils

    (1999)
  • R.D. Bardgett et al.

    Plant species and nitrogen effects on soil biological properties of temperate upland grasslands

    Functional Ecology

    (1999)
  • N.L. Bell et al.

    Population dynamics of Paratylenchus nanus in soil under pasture: 1. Aggregation and abiotic factors

    Nematology

    (2001)
  • N.L. Bell et al.

    Identification and host range assessment of Paratylenchus nanus (Tylenchida: Tylenchulidae) and Paratrichodorus minor (Triplonchida: Trichodoridae)

    Nematology

    (2001)
  • Bernard, E.C., Gwinn, K.D., Griffin, G.D., 1998. Forage grasses. In: Barker, K.R., Pederson, G.A., Windham, G.L....
  • T. Bongers

    The maturity index: an ecological measure of environmental disturbance based on nematode species composition

    Oecologia

    (1990)
  • S.J. Coulson et al.

    Microscale distribution patterns in high Arctic soil microarthropod communities: the influence of plant species within the vegetation mosaic

    Ecography

    (2003)
  • G.B. De Deyn et al.

    Plant species identity and diversity effects on different trophic levels of nematodes in the soil food web

    Oikos

    (2004)
  • R.E. Ingham et al.

    Interactions of bacteria, fungi, and their nematode grazers: effects on nutrient cycling and plant growth

    Ecological Monographs

    (1985)
  • L. Innes et al.

    The impacts of individual plant species on rhizosphere microbial communities in soils of different fertility

    Biology and Fertility of Soils

    (2004)
  • Cited by (36)

    • Mixed grass species differ in rhizosphere microbial community structure and function response to drought compared to monocultures

      2022, Rhizosphere
      Citation Excerpt :

      Across multiple systems, there is growing evidence that soil microbial communities are primarily determined by plant species (Zhang et al., 2015; Ke and Wan, 2020). Plant species identity, rather than functional group, is more reliable for predicting the composition of the soil microbial community (Viketoft, 2008; Leff et al., 2018). The quantity and quality of rhizodeposits vary with plant species, resulting in a plant species-specific microbial community structure in the rhizosphere (Ladygina and Hedlund, 2010; Bouasria et al., 2012).

    • Carbon nanomaterial addition changes soil nematode community in a tall fescue mesocosm

      2022, Pedosphere
      Citation Excerpt :

      The EI and SI were calculated as EI = 100[e/(e + b)] and SI = 100[s/(s + b)], where b = Σkbnb, e = Σkene, s = Σksns, k is the weight given to each guild, n is the density of nematodes within that guild, e is the enrichment component (Ba1 and Fu2), b is the basal component (Ba2 and Fu2), and s is the structure component (Ba3–5, Fu3–5, Om3–5, Pr2–5) (Ferris et al., 2001). The NCR was calculated as NCR = ABa/(ABa + AFu), where AFu and ABa are the abundances of Ba and Fu, respectively (Yeates, 2003; Zhang et al., 2007; Viketoft, 2008). Impact of carbon nanomaterials on the nematode abundance (in trophic groups and in total) and community parameters was tested using one-way analysis of variance (ANOVA).

    • Toxicity of the bionematicide 1,4-naphthoquinone on non-target soil organisms

      2017, Chemosphere
      Citation Excerpt :

      They were homogenized, sieved (5 mm) and defaunated through two freeze-thawing (F-T) cycles (48 h F: 48 h T: 48 h F). For the nematode community test, two weeks before its start, the soil was defaunated by freezing at −20 ± 1 °C, for 48 h, and heating to 65 °C for 24 h (Viketoft, 2008). This process was done twice.

    View all citing articles on Scopus
    View full text